Steve has long been fascinated by how quickly the world around us changes. Work on the genomics of marine organisms tries to focus on basic evolutionary questions but also on practical solutions to questions about how to preserve and protect the diverse life in the sea. Steve has lectured extensively on human-induced evolutionary change, has used genetic detective work to identify whales, seahorses, rockfish and sharks for sale in retail markets, and is developing genomic methods to help find ocean species resistant to climate change. Work on corals in American Samoa and Palau has identified corals more resilient to heat stress. Work at the Hopkins Marine Station focuses on how kelp, sea urchins, abalone and mussels respond to short term environmental changes and to environmental shifts over small spatial scales.
Steve’s latest book for non-scientists is about the amazing species in the sea, written with Steve’s son and novelist Anthony. The Extreme Life of the Sea tells about the fastest species in the sea, and hottest, coldest, oldest etc. Steve's previous book, The Death and Life of Monterey Bay: A Story of Revival, written with Carolyn Sotka, brought to life the unusual environmental success story of the recovery of Monterey Bay. Steve's first science book for non-scientists The Evolution Explosion explored how human accelerate evolutionary change in the species around us. Steve helped write, research and also appears in the BBC series The Future is Wild and the History Channel's World Without People. Other recent films appearances include The End of the Line, and the Canadian Broadcasting series One Ocean. Major work continues on the microdocumentary project, the Short Attention Span Science Theater. Steve's band Sustainable Soul has several songs out, including Crab Love and The Last Fish Left.
Current Research and Scholarly Interests
Stephen R. Palumbi received his Ph.D. from University of Washington in marine ecology. His research group studies the genetics, evolution, conservation, population biology and systematics of a diverse array of marine organisms.
Professor Palumbi's own research interests are similarly widespread, and he has published on the genetics and evolution of sea urchins, whales, cone snails, corals, sharks, spiders, shrimps, bryozoans, and butterflyfishes. A primary focus is the use of molecular genetic techniques in conservation, including the identification of whale and dolphin products available in commercial markets.
Current conservation work centers on the genetics of marine reserves designed for conservation and fisheries enhancement, with projects in the Philippines, Bahamas and western U.S. coast. In addition, basic work on the molecular evolution of reproductive isolation and its influence on patterns of speciation uses marine model systems such as sea urchins. This work is expanding our view of the evolution of gamete morphology and the genes involved.
Steve is based at Stanford University's Hopkins Marine Station, where he is now the Director. Steve is a Pew Fellow in Marine Conservation, senior fellow at the Woods Institute for the Environment, married to physician Mary Roberts, father of two grown children, and founding member of the band Sustainable Sole.
- Get to Know Your Oceans
OCEANS 300A (Aut)
- Planet Ocean
BIO 71, ESS 71, OCEANS 71 (Win)
Independent Studies (15)
- Directed Individual Study in Earth Systems
EARTHSYS 297 (Aut, Win, Spr, Sum)
- Directed Instruction or Reading
OCEANS 198H (Aut, Win, Spr)
- Directed Reading in Biology
BIO 198 (Aut, Win, Spr, Sum)
- Directed Reading in Environment and Resources
ENVRES 398 (Aut, Win, Spr, Sum)
- Directed Research
EARTHSYS 250 (Aut, Win, Spr, Sum)
- Directed Research in Environment and Resources
ENVRES 399 (Aut, Win, Spr, Sum)
- Graduate Research
BIO 300 (Aut)
- Honors Program in Earth Systems
EARTHSYS 199 (Aut, Win, Spr, Sum)
- Out-of-Department Directed Reading
BIO 198X (Sum)
- Out-of-Department Undergraduate Research
BIO 199X (Sum)
OCEANS 300 (Aut, Win, Spr)
- Teaching Practicum in Biology
BIO 290 (Aut, Win, Spr)
- Teaching Practicum in Biology
OCEANS 290H (Win, Spr)
- Undergraduate Research
BIO 199 (Sum)
- Undergraduate Research
OCEANS 199H (Aut, Win, Spr)
- Directed Individual Study in Earth Systems
Prior Year Courses
- Ecology of the Hawaiian Islands
BIO 116, SUSTAIN 116 (Aut)
- Planet Ocean
BIO 71, ESS 71 (Win)
- Taking the Pulse of the Ocean: Innovative Technologies for the Blue Planet
BIO 170, BIOHOPK 170H, BIOHOPK 270H, OCEANS 170, OCEANS 270 (Spr)
- Ocean Forensics: Ecological, Conservation and Market Data from Environmental DNA
BIOHOPK 159H, BIOHOPK 259H (Spr)
- Planet Ocean
BIO 71, ESS 71 (Win)
- The Science of Extreme Life of the Sea
BIO 140 (Spr)
- Conservation and Population Genomics
BIO 386 (Win)
- Coral Reefs of the Western Pacific: Interdisciplinary Perspectives, Emerging Crises, and Solutions
BIO 355, BIOHOPK 355, CEE 363I, ESS 355 (Aut)
- The Science of Extreme Life of the Sea
BIO 140 (Spr)
- Ecology of the Hawaiian Islands
Graduate and Fellowship Programs
Biology (School of Humanities and Sciences) (Phd Program)
Footprints of local adaptation span hundreds of linked genes in the Atlantic silverside genome.
2020; 4 (5): 430-443
The study of local adaptation in the presence of ongoing gene flow is the study of natural selection in action, revealing the functional genetic diversity most relevant to contemporary pressures. In addition to individual genes, genome-wide architecture can itself evolve to enable adaptation. Distributed across a steep thermal gradient along the east coast of North America, Atlantic silversides (Menidia menidia) exhibit an extraordinary degree of local adaptation in a suite of traits, and the capacity for rapid adaptation from standing genetic variation, but we know little about the patterns of genomic variation across the species range that enable this remarkable adaptability. Here, we use low-coverage, whole-transcriptome sequencing of Atlantic silversides sampled along an environmental cline to show marked signatures of divergent selection across a gradient of neutral differentiation. Atlantic silversides sampled across 1371 km of the southern section of its distribution have very low genome-wide differentiation (median FST = 0.006 across 1.9 million variants), consistent with historical connectivity and observations of recent migrants. Yet almost 14,000 single nucleotide polymorphisms (SNPs) are nearly fixed (FST > 0.95) for alternate alleles. Highly differentiated SNPs cluster into four tight linkage disequilibrium (LD) blocks that span hundreds of genes and several megabases. Variants in these LD blocks are disproportionately nonsynonymous and concentrated in genes enriched for multiple functions related to known adaptations in silversides, including variation in lipid storage, metabolic rate, and spawning behavior. Elevated levels of absolute divergence and demographic modeling suggest selection maintaining divergence across these blocks under gene flow. These findings represent an extreme case of heterogeneity in levels of differentiation across the genome, and highlight how gene flow shapes genomic architecture in continuous populations. Locally adapted alleles may be common features of populations distributed along environmental gradients, and will likely be key to conserving variation to enable future responses to environmental change.
View details for DOI 10.1002/evl3.189
View details for PubMedID 33014419
View details for PubMedCentralID PMC7523562
- Footprints of local adaptation span hundreds of linked genes in the Atlantic silverside genome EVOLUTION LETTERS 2020
Ocean acidification causes variable trait shifts in a coral species.
Global change biology
High pCO2 habitats and their populations provide an unparalleled opportunity to assess how species may survive under future ocean acidification conditions, and help to reveal the traits that confer tolerance. Here we utilize a unique CO2 vent system to study the effects of exposure to elevated pCO2 on trait-shifts observed throughout natural populations of Astroides calycularis, an azooxanthellate scleractinian coral endemic to the Mediterranean. Unexpected shifts in skeletal and growth patterns were found. Colonies shifted to a skeletal phenotype characterized by encrusting morphology, smaller size, reduced coenosarc tissue, fewer polyps, and less porous and denser skeletons at low pH. Interestingly, while individual polyps calcified more and extended faster at low pH, whole colonies found at low pH site calcified and extended their skeleton at the same rate as did those at ambient pH sites. Transcriptomic data revealed strong genetic differentiation among local populations of this warm water species whose distribution range is currently expanding northward. We found excess differentiation in the CO2 vent population for genes central to calcification, including genes for calcium management (calmodulin, calcium-binding proteins), pH regulation (V-type proton ATPase), and inorganic carbon regulation (carbonic anhydrase). Combined, our results demonstrate how coral populations can persist in high pCO2 environments, making this system a powerful candidate for investigating acclimatization and local adaptation of organisms to global environmental change.
View details for DOI 10.1111/gcb.15372
View details for PubMedID 33002274
Somatic mutations and genome stability maintenance in clonal coral colonies.
Molecular biology and evolution
One challenge for multicellular organisms is maintaining genome stability in the face of mutagens across long life spans. Imperfect genome maintenance leads to mutation accumulation in somatic cells, which is associated with tumors and senescence in vertebrates. Colonial reef-building corals are often large, can live for hundreds of years, rarely develop recognizable tumors, and are thought to convert somatic cells into gamete producers, so they are a pivotal group in which to understand long-term genome maintenance. To measure rates and patterns of somatic mutations, we analyzed transcriptomes from 17-22 branches from each of four Acropora hyacinthus colonies, determined putative single nucleotide variants, and verified them with Sanger resequencing. Unlike for human skin carcinomas, there is no signature of mutations caused by UV damage, indicating either higher efficiency of repair than in vertebrates, or strong sunscreen protection in these shallow water tropical animals. The somatic mutation frequency per nucleotide in A. hyacinthus is on the same order of magnitude (10-7) as noncancerous human somatic cells, and accumulation of mutations with age is similar. Unlike mammals, loss of heterozygosity variants outnumber gain of heterozygosity mutations about 2:1. Although the mutation frequency is similar in mammals and corals, the preponderance of loss of heterozygosity changes and potential selection may reduce the frequency of deleterious mutations in colonial animals like corals. This may limit the deleterious effects of somatic mutations on the coral organism as well as potential offspring.
View details for DOI 10.1093/molbev/msz270
View details for PubMedID 31722397
- PRESENT AND FUTURE ADAPTATION OF MARINE SPECIES ASSEMBLAGES DNA-Based Insights into Climate Change from Studies of Physiology, Genomics, and Evolution OCEANOGRAPHY 2019; 32 (3): 82–93
- Connectivity, Dispersal, and Recruitment CONNECTING BENTHIC COMMUNITIES AND THE COASTAL OCEAN OCEANOGRAPHY 2019; 32 (3): 50–59
- SIDEBAR. Empirical Approaches to Measure Connectivity OCEANOGRAPHY 2019; 32 (3): 60–61
- PLANNING FOR CHANGE Assessing the Potential Role of Marine Protected Areas and Fisheries Management Approaches for Resilience Management in a Changing Ocean OCEANOGRAPHY 2019; 32 (3): 116–25
Cobble community DNA as a tool to monitor patterns of biodiversity within kelp forest ecosystems.
Molecular ecology resources
Kelp forest ecosystems dominate 150,000km of global temperate coastline, rivalling the coastal occurrence of coral reefs. Despite the astounding biological diversity and productive ecological communities associated with kelp forests, patterns of species richness and composition are difficult to monitor and compare. Crustose coralline algae are a critically important substrate for propagule settlement for a range of kelp forest species. Coralline-covered cobbles are home to hundreds of species of benthic animals and algae and form a replicable unit for ecological assays. Here, we use DNA metabarcoding of bulk DNA extracts sampled from cobbles to explore patterns of species diversity in kelp forests of the central California coast. The data from 97 cobbles within kelp forest ecosystems at three sites in Central California show the presence of 752 molecular operational taxonomic units (MOTUs) and 53 MOTUs assigned up to the species level with >95% similarity to current databases. We are able to detect spatial patterns of important management targets such as abalone recruits, and localized abundance of sea stars in 2012. Comparison of classic ecological surveys of these sites reveals large differences in species targets for these two approaches. In order to make such comparisons more quantitative, we use Presence/Absence Metabarcoding, using the fraction of replicate cobbles showing a species as a measure of its local abundance. This approach provides a fast and repeatable survey method that can be applied for biodiversity assessments across systems to shed light on the impact of different ecological disturbances and the role played by marine protected areas.
View details for DOI 10.1111/1755-0998.13067
View details for PubMedID 31436907
- Management for network diversity speeds evolutionary adaptation to climate change NATURE CLIMATE CHANGE 2019; 9 (8): 632-+
- Sub-weekly coral linear extension measurements in a coral reef JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY 2019; 516: 114–22
Transcriptomic resilience, symbiont shuffling, and vulnerability to recurrent bleaching in reef-building corals.
As climate change progresses and extreme temperature events increase in frequency, rates of disturbance may soon outpace the capacity of certain species of reef-building coral to recover from bleaching. This may lead to dramatic shifts in community composition and ecosystem function. Understanding variation in rates of bleaching recovery among species and how that translates to resilience to recurrent bleaching is fundamental to predicting the impacts of increasing disturbances on coral reefs globally. We tracked the response of two heat sensitive species in the genus Acropora to repeated bleaching events during the austral summers of 2015 and 2017. Despite a similar bleaching response, the species Acropora gemmifera recovered faster based on transcriptome-wide gene expression patterns and had a more dynamic algal symbiont community than Acropora hyacinthus growing on the same reef. Moreover, A. gemmifera had higher survival to repeated heat extremes, with sixfold lower mortality than A. hyacinthus. These patterns suggest that speed of recovery from a first round of bleaching, based on multiple mechanisms, contributes strongly to sensitivity to a second round of bleaching. Furthermore, our data uncovered intra-genus variation in a group of corals thought generally to be heat-sensitive and therefore paint a more nuanced view of the future health of coral reef ecosystems against a backdrop of increasing thermal disturbances. This article is protected by copyright. All rights reserved.
View details for DOI 10.1111/mec.15143
View details for PubMedID 31177587
- Empowering conservation practice with efficient and economical genotyping from poor quality samples METHODS IN ECOLOGY AND EVOLUTION 2019; 10 (6): 853–59
Empowering conservation practice with efficient and economical genotyping from poor quality samples.
Methods in ecology and evolution
2019; 10 (6): 853-859
Moderate- to high-density genotyping (100 + SNPs) is widely used to determine and measure individual identity, relatedness, fitness, population structure and migration in wild populations.However, these important tools are difficult to apply when high-quality genetic material is unavailable. Most genomic tools are developed for high-quality DNA sources from laboratory or medical settings. As a result, most genetic data from market or field settings is limited to easily amplified mitochondrial DNA or a few microsatellites.To enable genotyping in conservation contexts, we used next-generation sequencing of multiplex PCR products from very low-quality DNA extracted from faeces, hair and cooked samples. We demonstrated utility and wide-ranging potential application in endangered wild tigers and tracking commercial trade in Caribbean queen conch.We genotyped 100 SNPs from degraded tiger samples to identify individuals, discern close relatives and detect population differentiation. Co-occurring carnivores do not amplify (e.g. Indian wild dog/dhole) or are monomorphic (e.g. leopard). Sixty-two SNPs from conch fritters and field-collected samples were used to test relatedness and detect population structure.We provide proof of concept for a rapid, simple, cost-effective and scalable method (for both samples and number of loci), a framework that can be applied to other conservation scenarios previously limited by low-quality DNA samples. These approaches provide a critical advance for wildlife monitoring and forensics, open the door to field-ready testing, and will strengthen the use of science in policy decisions and wildlife trade.
View details for DOI 10.1111/2041-210X.13173
View details for PubMedID 31511786
View details for PubMedCentralID PMC6738957
- Using naturally occurring climate resilient corals to construct bleaching-resistant nurseries PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 2019; 116 (21): 10586–91
Using naturally occurring climate resilient corals to construct bleaching-resistant nurseries.
Proceedings of the National Academy of Sciences of the United States of America
Ecological restoration of forests, meadows, reefs, or other foundational ecosystems during climate change depends on the discovery and use of individuals able to withstand future conditions. For coral reefs, climate-tolerant corals might not remain tolerant in different environments because of widespread environmental adjustment of coral physiology and symbionts. Here, we test if parent corals retain their heat tolerance in nursery settings, if simple proxies predict successful colonies, and if heat-tolerant corals suffer lower growth or survival in normal settings. Before the 2015 natural bleaching event in American Samoa, we set out 800 coral fragments from 80 colonies of four species selected by prior tests to have a range of intraspecific natural heat tolerance. After the event, nursery stock from heat-tolerant parents showed two to three times less bleaching across species than nursery stock from less tolerant parents. They also retained higher individual genetic diversity through the bleaching event than did less heat-tolerant corals. The three best proxies for thermal tolerance were response to experimental heat stress, location on the reef, and thermal microclimate. Molecular biomarkers were also predictive but were highly species specific. Colony genotype and symbiont genus played a similarly strong role in predicting bleaching. Combined, our results show that selecting for host and symbiont resilience produced a multispecies coral nursery that withstood multiple bleaching events, that proxies for thermal tolerance in restoration can work across species and be inexpensive, and that different coral clones within species reacted very differently to bleaching.
View details for PubMedID 31061118
Contrasting genomic shifts underlie parallel phenotypic evolution in response to fishing.
Science (New York, N.Y.)
2019; 365 (6452): 487–90
Humans cause widespread evolutionary change in nature, but we still know little about the genomic basis of rapid adaptation in the Anthropocene. We tracked genomic changes across all protein-coding genes in experimental fish populations that evolved pronounced shifts in growth rates due to size-selective harvest over only four generations. Comparisons of replicate lines show parallel allele frequency shifts that recapitulate responses to size-selection gradients in the wild across hundreds of unlinked variants concentrated in growth-related genes. However, a supercluster of genes also rose rapidly in frequency and dominated the evolutionary dynamic in one replicate line but not in others. Parallel phenotypic changes thus masked highly divergent genomic responses to selection, illustrating how contingent rapid adaptation can be in the face of strong human-induced selection.
View details for DOI 10.1126/science.aaw7271
View details for PubMedID 31371613
- Risk-sensitive planning for conserving coral reefs under rapid climate change CONSERVATION LETTERS 2018; 11 (6)
- Accurate population genetic measurements require cryptic species identification in corals CORAL REEFS 2018; 37 (2): 549–63
- Long-term growth rates and effects of bleaching in Acropora hyacinthus CORAL REEFS 2018; 37 (1): 267–77
Polygenic evolution drives species divergence and climate adaptation in corals
2018; 72 (1): 82–94
Closely related species often show substantial differences in ecological traits that allow them to occupy different environmental niches. For few of these systems is it clear what the genomic basis of adaptation is and whether a few loci of major effect or many genome-wide differences drive species divergence. Four cryptic species of the tabletop coral Acropora hyacinthus are broadly sympatric in American Samoa; here we show that two common species have differences in key environmental traits such as microhabitat distributions and thermal stress tolerance. We compared gene expression patterns and genetic polymorphism between these two species using RNA-Seq. The vast majority of polymorphisms are shared between species, but the two species show widespread differences in allele frequencies and gene expression, and tend to host different symbiont types. We find that changes in gene expression are related to changes in the frequencies of many gene regulatory variants, but that many of these differences are consistent with the action of genetic drift. However, we observe greater genetic divergence between species in amino acid replacement polymorphisms compared to synonymous variants. These findings suggest that polygenic evolution plays a major role in driving species differences in ecology and resilience to climate change.
View details for PubMedID 29098686
Genomic models predict successful coral adaptation if future ocean warming rates are reduced.
2017; 3 (11): e1701413
Population genomic surveys suggest that climate-associated genetic variation occurs widely across species, but whether it is sufficient to allow population persistence via evolutionary adaptation has seldom been quantified. To ask whether rapid adaptation in reef-building corals can keep pace with future ocean warming, we measured genetic variation at predicted warm-adapted loci and simulated future evolution and persistence in a high-latitude population of corals from Rarotonga, Cook Islands. Alleles associated with thermal tolerance were present but at low frequencies in this cooler, southerly locality. Simulations based on predicted ocean warming in Rarotonga showed rapid evolution of heat tolerance resulting in population persistence under mild warming scenarios consistent with low CO2 emission plans, RCP2.6 and RCP4.5. Under more severe scenarios, RCP6.0 and RCP8.5, adaptation was not rapid enough to prevent extinction. Population adaptation was faster for models based on smaller numbers of additive loci that determine thermal tolerance and for higher population growth rates. Finally, accelerated migration via transplantation of thermally tolerant individuals (1 to 5%/year) sped adaptation. These results show that cool-water corals can adapt to warmer oceans but only under mild scenarios resulting from international emissions controls. Incorporation of genomic data into models of species response to climate change offers a promising method for estimating future adaptive processes.
View details for PubMedID 29109975
The genomics of recovery from coral bleaching.
Proceedings. Biological sciences
2017; 284 (1865)
Ecological damage from periodic environmental extremes is often repaired in resilient ecosystems, but the rate of return to a non-damaged state is critical. Measures of recovery of communities include biomass, productivity and diversity, while measures of recovery of individuals tend to focus on physiological conditions and the return to normal metabolic functioning. Transcriptomics offers a window into the entire physiology of the organism under stress and can represent a holistic view of organismal recovery. In this study, we track the recovery of seven colonies of Acropora hyacinthus following a natural bleaching event. We identified a large environmental stress response in the field that involved approximately 20% of the host transcriptome. The transcriptome remained largely perturbed for at least six months after temperatures had cooled and four months after symbiont populations had recovered. Moreover, a small set of genes did not recover to previous expression levels even 12 months after the event, about the time that normal growth rates resumed. This study is among the first to incorporate transcriptomics into a longitudinal dataset of recovery from environmental stress. The data demonstrate large and lasting effects on coral physiology long after environmental conditions return to normal and symbiont populations recover.
View details for PubMedID 29070726
Calcifying algae maintain settlement cues to larval abalone following algal exposure to extreme ocean acidification.
2017; 7 (1): 5774
Ocean acidification (OA) increasingly threatens marine systems, and is especially harmful to calcifying organisms. One important question is whether OA will alter species interactions. Crustose coralline algae (CCA) provide space and chemical cues for larval settlement. CCA have shown strongly negative responses to OA in previous studies, including disruption of settlement cues to corals. In California, CCA provide cues for seven species of harvested, threatened, and endangered abalone. We exposed four common CCA genera and a crustose calcifying red algae, Peyssonnelia (collectively CCRA) from California to three pCO2 levels ranging from 419-2,013 µatm for four months. We then evaluated abalone (Haliotis rufescens) settlement under ambient conditions among the CCRA and non-algal controls that had been previously exposed to the pCO2 treatments. Abalone settlement and metamorphosis increased from 11% in the absence of CCRA to 45-69% when CCRA were present, with minor variation among CCRA genera. Though all CCRA genera reduced growth during exposure to increased pCO2, abalone settlement was unaffected by prior CCRA exposure to increased pCO2. Thus, we find no impacts of OA exposure history on CCRA provision of settlement cues. Additionally, there appears to be functional redundancy in genera of CCRA providing cues to abalone, which may further buffer OA effects.
View details for DOI 10.1038/s41598-017-05502-x
View details for PubMedID 28720836
View details for PubMedCentralID PMC5515930
- Robert Treat Paine III (1933-2016). Proceedings of the National Academy of Sciences of the United States of America 2017; 114 (27): 6881-6882
Transcriptome predictors of coral survival and growth in a highly variable environment.
Ecology and evolution
2017; 7 (13): 4794-4803
Concern over rapid environmental shifts associated with climate change has led to a search for molecular markers of environmental tolerance. Climate-associated gene expression profiles exist for a number of systems, but have rarely been tied to fitness outcomes, especially in nonmodel organisms. We reciprocally transplanted corals between two backreef locations with more and less variable temperature regimes to disentangle effects of recent and native environment on survival and growth. Coral growth over 12 months was largely determined by local environment. Survival, however, was impacted by native environment; corals from the more variable environment had 22% higher survivorship. By contrast, corals native to the less variable environment had more variable survival. This might represent a "selective sieve" where poor survivors are filtered from the more stressful environment. We also find a potential fitness trade-off-corals with high survival under stressful conditions grew less in the more benign environment. Transcriptome samples taken a year before transplantation were used to examine gene expression patterns that predicted transplant survival and growth. Two separate clusters of coexpressed genes were predictive of survival in the two locations. Genes from these clusters are candidate biomarkers for predicting persistence of corals under future climate change scenarios.
View details for DOI 10.1002/ece3.2685
View details for PubMedID 28690808
View details for PubMedCentralID PMC5496549
Coral reefs in the Anthropocene
2017; 546 (7656): 82–90
Coral reefs support immense biodiversity and provide important ecosystem services to many millions of people. Yet reefs are degrading rapidly in response to numerous anthropogenic drivers. In the coming centuries, reefs will run the gauntlet of climate change, and rising temperatures will transform them into new configurations, unlike anything observed previously by humans. Returning reefs to past configurations is no longer an option. Instead, the global challenge is to steer reefs through the Anthropocene era in a way that maintains their biological functions. Successful navigation of this transition will require radical changes in the science, management and governance of coral reefs.
View details for PubMedID 28569801
Highly localized divergence within supergenes in Atlantic cod (Gadus morhua) within the Gulf of Maine
Atlantic cod (Gadus morhua), is known to vary genetically across the North Atlantic, Greenland, and Newfoundland. This genetic variation occurs both spatially and temporally through decades of heavy fishing, and is concentrated in three linkage disequilibrium blocks, previously defined by pedigreed linkage mapping analysis. Variation within these genomic regions is correlated with both seawater temperature and behavioral ecotype. The full extent and nature of these linkage groups is important information for interpreting cod genetic structure as a tool for future fisheries management.We conducted whole genome sequencing for 31 individual cod from three sub-populations in the Gulf of Maine. Across the genome, we found 3,390,654 intermediate to high frequency Single Nucleotide Polymorphisms (SNPs). We show that pairwise linkage analysis among these SNPs is a powerful tool to detect linkage disequilibrium clusters by recovering the three previously detected linkage groups and identifying the 1031 genes contained therein. Across these genes, we found significant population differentiation among spawning groups in the Gulf of Maine and between Georges Bank and Gulf of Maine. Coordinated divergence among these genes and their differentiation at both short and long spatial scales suggests that they are acting as linked supergenes in local adaptation of cod populations.Differentiation between SNPs in linkage disequilibrium blocks is the major signal of genetic differentiation between all groups tested within the Gulf of Maine. Our data provide a map of genes contained in these blocks, allowing an enhanced search for neutral genetic structure for demographic inference and fisheries modeling. Patterns of selection and the history of populations may be possible to identify in cod using this description of linkage disequilibrium blocks and future data sets to robustly separate neutral and selected genetic markers.
View details for DOI 10.1186/s12864-017-3660-3
View details for Web of Science ID 000397757500003
View details for PubMedID 28359300
The cell specificity of gene expression in the response to heat stress in corals.
journal of experimental biology
Previous transcriptional studies in heat stressed corals have shown that many genes are responsive to generalized heat stress whereas the expression patterns of specific gene networks after heat stress show strong correlations with variation in bleaching outcomes. However, where these specific genes are expressed is unknown. Here we employed in situ hybridization to identify patterns of spatial gene expression of genes previously predicted to be involved in general stress response and bleaching. We found that Tumor Necrosis Factor Receptors (TNFRs), known to be strong responders to heat stress, were not expressed in gastrodermal symbiont-containing cells but were widely expressed in specific cells of the epidermal layer. The transcription factors AP-1 and FosB implicated as early signals of heat stress and were widely expressed throughout the oral gastrodermis and epidermis. By contrast, a G-protein coupled receptor gene (GPCR), and a fructose bisphosphate aldolase C gene (Aldolase), previously implicated in bleaching, was expressed in symbiont containing gastrodermal cells, and in epidermal tissue. Finally, Chordin-like/Kielin (Chordin-like) a gene highly correlated to bleaching was expressed solely in the oral gastrodermis. From this study we confirm that heat responsive genes occur widely in coral tissues outside of symbiont containing cells, and that gene expression in response to heat stress that causes bleaching does not signal by itself that a gene is expressed in the symbiotic cells where bleaching occurs. Joint information about expression patterns in response to heat and cell specificity will allow greater dissection of the regulatory pathways and specific cell reactions that lead to coral bleaching.
View details for DOI 10.1242/jeb.155275
View details for PubMedID 28254881
Practical low-coverage genomewide sequencing of hundreds of individually barcoded samples for population and evolutionary genomics in nonmodel species.
Molecular ecology resources
2017; 17 (2): 194-208
Today most population genomic studies of nonmodel organisms either sequence a subset of the genome deeply in each individual or sequence pools of unlabelled individuals. With a step-by-step workflow, we illustrate how low-coverage whole-genome sequencing of hundreds of individually barcoded samples is now a practical alternative strategy for obtaining genomewide data on a population scale. We used a highly efficient protocol to generate high-quality libraries for ~6.5 USD from each of 876 Atlantic silversides (a teleost fish with a genome size ~730 Mb) that we sequenced to 1-4× genome coverage. In the absence of a reference genome, we developed a bioinformatic pipeline for mapping the genomic reads to a de novo assembled reference transcriptome. This provides an 'in silico' method for exome capture that avoids the complexities and expenses of using wet chemistry for target isolation. Using novel tools for analysis of low-coverage data, we extracted population allele frequencies, individual genotype likelihoods and polymorphism data for 2 504 335 SNPs across the exome for the 876 fish. To illustrate the use of the resulting data, we present a preliminary analysis of geographical patterns in the exome data and a comparison of complete mitochondrial genome sequences for each individual (constructed from the low-coverage data) that show population colonization patterns along the US east coast. With a total cost per sample of less than 50 USD (including sequencing) and ability to prepare 96 libraries in only 5 h, our approach adds a viable new option to the population genomics toolbox.
View details for DOI 10.1111/1755-0998.12593
View details for PubMedID 27496322
Tidal heat pulses on a reef trigger a fine-tuned transcriptional response in corals to maintain homeostasis.
2017; 3 (3)
For reef-building corals, extreme stress exposure can result in loss of endosymbionts, leaving colonies bleached. However, corals in some habitats are commonly exposed to natural cycles of sub-bleaching stress, often leading to higher stress tolerance. We monitored transcription in the tabletop coral Acropora hyacinthus daily for 17 days over a strong tidal cycle that included extreme temperature spikes, and show that increases in temperature above 30.5°C triggered a strong transcriptional response. The transcriptomic time series data allowed us to identify a set of genes with coordinated expression that were activated only on days with strong tides, high temperature, and large diel pH and oxygen changes. The responsive genes are enriched for gene products essential to the unfolded protein response, an ancient cellular response to endoplasmic reticulum stress. After the temporary heat pulses passed, expression of these genes immediately decreased, suggesting that homeostasis was restored to the endoplasmic reticulum. In a laboratory temperature stress experiment, we found that the expression of these environmentally responsive genes increased as corals bleached, showing that the unfolded protein response becomes more intense during more severe stress. Our results point to the unfolded protein response as a first line of defense that acroporid corals use when coping with environmental stress on the reef, thus enhancing our understanding of coral stress physiology during a time of major concern for reefs.
View details for DOI 10.1126/sciadv.1601298
View details for PubMedID 28345029
Bacterial community dynamics are linked to patterns of coral heat tolerance
Ocean warming threatens corals and the coral reef ecosystem. Nevertheless, corals can be adapted to their thermal environment and inherit heat tolerance across generations. In addition, the diverse microbes that associate with corals have the capacity for more rapid change, potentially aiding the adaptation of long-lived corals. Here, we show that the microbiome of reef corals is different across thermally variable habitats and changes over time when corals are reciprocally transplanted. Exposing these corals to thermal bleaching conditions changes the microbiome for heat-sensitive corals, but not for heat-tolerant corals growing in habitats with natural high heat extremes. Importantly, particular bacterial taxa predict the coral host response in a short-term heat stress experiment. Such associations could result from parallel responses of the coral and the microbial community to living at high natural temperatures. A competing hypothesis is that the microbial community and coral heat tolerance are causally linked.
View details for DOI 10.1038/ncomms14213
View details for Web of Science ID 000393656200001
View details for PubMedID 28186132
View details for PubMedCentralID PMC5309854
Transcriptomic responses to seawater acidification among sea urchin populations inhabiting a natural pH mosaic.
Increasing awareness of spatial and temporal variation in ocean pH suggests some marine populations may be adapted to local pH regimes and will therefore respond differently to present-day pH variation and to long-term ocean acidification. In the Northeast Pacific Ocean, differences in the strength of coastal upwelling cause latitudinal variation in prevailing pH regimes that are hypothesized to promote local adaptation and unequal pH tolerance among resident populations. In this study, responses to experimental seawater acidification were compared among embryos and larvae from six populations of purple sea urchins (Strongylocentrotus purpuratus) inhabiting areas that differ in their frequency of low pH exposure and that prior research suggests are locally adapted to seawater pH. Transcriptomic analyses demonstrate urchin populations most frequently exposed to low pH seawater responded to experimental acidification by expressing genes within major ATP-producing pathways at greater levels than populations encountering low pH less often. Multiple genes within the tricarboxylic acid cycle, electron transport chain and fatty acid beta oxidation pathways were upregulated in urchin populations experiencing low pH conditions most frequently. These same metabolic pathways were significantly over-represented among genes both expressed in a population-specific manner and putatively under selection to enhance low pH tolerance. Collectively, these data suggest natural selection is acting on metabolic gene networks to redirect ATP toward maintaining acid-base homeostasis and enhance tolerance of seawater acidification. As a trade-off, marine populations more tolerant of low pH may have less energy to put towards other aspects of fitness and to respond to additional ocean change.
View details for DOI 10.1111/mec.14038
View details for PubMedID 28141889
A keystone ecologist: Robert Treat Paine, 1933-2016.
2016; 97 (11): 2905-2909
Robert T. Paine, who passed away on 13 June 2016, is among the most influential people in the history of ecology. Paine was an experimentalist, a theoretician, a practitioner, and proponent of the "ecology of place," and a deep believer in the importance of natural history to ecological understanding. His scientific legacy grew from the discovery of a link between top-down forcing and species diversity, a breakthrough that led to the ideas of both keystone species and trophic cascades, and to our early understanding of the mosaic nature of biological communities, causes of zonation across physical gradients, and the intermediate-disturbance hypothesis of species diversity. Paine's influence as a mentor was equally important to the growth of ecological thinking, natural resource conservation, and policy. He served ecology as an Ecological Society of America president, an editor of the Society's journals, a member of and contributor to the National Academy of Sciences and the National Research Council, and an in-demand advisor to various state and federal agencies. Paine's broad interests, enthusiasm, charisma, and humor deeply affected our lives and the lives of so many others.
View details for DOI 10.1002/ecy.1572
View details for PubMedID 27870047
- What are we missing about marine invasions? Filling in the gaps with evolutionary genomics MARINE BIOLOGY 2016; 163 (10)
- Gene Networks in the Wild: Identifying Transcriptional Modules that Mediate Coral Resistance to Experimental Heat Stress GENOME BIOLOGY AND EVOLUTION 2016; 8 (1): 243-252
Transcriptome sequencing reveals both neutral and adaptive genome dynamics in a marine invader
2015; 24 (16): 4145-4158
Species invasions cause significant ecological and economic damage, and genetic information is important to understanding and managing invasive species. In the ocean, many invasive species have high dispersal and gene flow, lowering the discriminatory power of traditional genetic approaches. High-throughput sequencing holds tremendous promise for increasing resolution and illuminating the relative contributions of selection and drift in marine invasion, but has not yet been used to compare the diversity and dynamics of a high-dispersal invader in its native and invaded ranges. We test a transcriptome-based approach in the European green crab (Carcinus maenas), a widespread invasive species with high gene flow and a well-known invasion history, in two native and five invasive populations. A panel of 10 809 transcriptome-derived nuclear SNPs identified significant population structure among highly bottlenecked invasive populations that were previously undifferentiated with traditional markers. Comparing the full data set and a subset of 9246 putatively neutral SNPs strongly suggested that non-neutral processes are the primary driver of population structure within the species' native range, while neutral processes appear to dominate in the invaded range. Non-neutral native range structure coincides with significant differences in intraspecific thermal tolerance, suggesting temperature as a potential selective agent. These results underline the importance of adaptation in shaping intraspecific differences even in high geneflow marine invasive species. They also demonstrate that high-throughput approaches have broad utility in determining neutral structure in recent invasions of such species. Together, neutral and non-neutral data derived from high-throughput approaches may increase the understanding of invasion dynamics in high-dispersal species.
View details for DOI 10.1111/mec.13294
View details for Web of Science ID 000359355900008
View details for PubMedID 26118396
Ocean acidification research in the 'post-genomic' era: Roadmaps from the purple sea urchin Strongylocentrotus purpuratus
COMPARATIVE BIOCHEMISTRY AND PHYSIOLOGY A-MOLECULAR & INTEGRATIVE PHYSIOLOGY
2015; 185: 33-42
Advances in nucleic acid sequencing technology are removing obstacles that historically prevented use of genomics within ocean change biology. As one of the first marine calcifiers to have its genome sequenced, purple sea urchins (Strongylocentrotus purpuratus) have been the subject of early research exploring genomic responses to ocean acidification, work that points to future experiments and illustrates the value of expanding genomic resources to other marine organisms in this new 'post-genomic' era. This review presents case studies of S. purpuratus demonstrating the ability of genomic experiments to address major knowledge gaps within ocean acidification. Ocean acidification research has focused largely on species vulnerability, and studies exploring mechanistic bases of tolerance toward low pH seawater are comparatively few. Transcriptomic responses to high pCO₂ seawater in a population of urchins already encountering low pH conditions have cast light on traits required for success in future oceans. Secondly, there is relatively little information on whether marine organisms possess the capacity to adapt to oceans progressively decreasing in pH. Genomics offers powerful methods to investigate evolutionary responses to ocean acidification and recent work in S. purpuratus has identified genes under selection in acidified seawater. Finally, relatively few ocean acidification experiments investigate how shifts in seawater pH combine with other environmental factors to influence organism performance. In S. purpuratus, transcriptomics has provided insight into physiological responses of urchins exposed simultaneously to warmer and more acidic seawater. Collectively, these data support that similar breakthroughs will occur as genomic resources are developed for other marine species.
View details for DOI 10.1016/j.cbpa.2015.03.007
View details for Web of Science ID 000355037200005
View details for PubMedID 25773301
Transcriptome-wide Changes in Coral Gene Expression at Noon and Midnight Under Field Conditions
2015; 228 (3): 227-241
Reef-building corals experience high daily variation in their environment, food availability, and physiological activities such as calcification and photosynthesis by endosymbionts. On Ofu Island, American Samoa, we investigated day-night differences in gene expression under field conditions of changing pH, temperature, light, and oxygen. Using RNASeq techniques, we compared two replicate transcriptomes from a single coral colony of Acropora hyacinthus over six noons and five midnights. We identified 344 contigs with significant expression differences across 16,800 contigs in the transcriptome, most with small fold-changes. However, there were 21 contigs with fold-changes ranging from 10 to 141. The largest changes were in a set of transcription factors strongly associated with day-night gene regulation in other animals, including cryptochromes, thyrotroph embryonic factor, and D site-binding protein. We also found large daytime increases in a set of genes involved in glucose transport and glycogen storage. We found small expression differences in genes associated with aerobic ATP production and hypoxia response, along with slightly higher expression of most calcification genes at noon. Although >40-fold-changes in expression occur in important transcription factors, downstream gene regulation seems very stable in corals from day to night compared to other animals studied.
View details for Web of Science ID 000357026300006
View details for PubMedID 26124449
- Marine biology. Uncovering hidden worlds of ocean biodiversity. Science 2015; 348 (6237): 865-867
SNP genotyping and population genomics from expressed sequences - current advances and future possibilities
2015; 24 (10): 2310-2323
With the rapid increase in production of genetic data from new sequencing technologies, a myriad of new ways to study genomic patterns in nonmodel organisms are currently possible. Because genome assembly still remains a complicated procedure, and because the functional role of much of the genome is unclear, focusing on SNP genotyping from expressed sequences provides a cost-effective way to reduce complexity while still retaining functionally relevant information. This review summarizes current methods, identifies ways that using expressed sequence data benefits population genomic inference and explores how current practitioners evaluate and overcome challenges that are commonly encountered. We focus particularly on the additional power of functional analysis provided by expressed sequence data and how these analyses push beyond allele pattern data available from nonfunction genomic approaches. The massive data sets generated by these approaches create opportunities and problems as well - especially false positives. We discuss methods available to validate results from expressed SNP genotyping assays, new approaches that sidestep use of mRNA and review follow-up experiments that can focus on evolutionary mechanisms acting across the genome.
View details for DOI 10.1111/mec.13165
View details for Web of Science ID 000353961500003
View details for PubMedID 25808983
The role of transcriptome resilience in resistance of corals to bleaching
2015; 24 (7): 1467-1484
Wild populations increasingly experience extreme conditions as climate change amplifies environmental variability. How individuals respond to environmental extremes determines the impact of climate change overall. The variability of response from individual to individual can represent the opportunity for natural selection to occur as a result of extreme conditions. Here, we experimentally replicated the natural exposure to extreme temperatures of the reef lagoon at Ofu Island (American Samoa), where corals can experience severe heat stress during midday low tide. We investigated the bleaching and transcriptome response of 20 Acropora hyacinthus colonies 5 and 20 h after exposure to control (29 °C) or heated (35 °C) conditions. We found a highly dynamic transcriptome response: 27% of the coral transcriptome was significantly regulated 1 h postheat exposure. Yet 15 h later, when heat-induced coral bleaching became apparent, only 12% of the transcriptome was differentially regulated. A large proportion of responsive genes at the first time point returned to control levels, others remained differentially expressed over time, while an entirely different subset of genes was successively regulated at the second time point. However, a noteworthy variability in gene expression was observed among individual coral colonies. Among the genes of which expression lingered over time, fast return to normal levels was associated with low bleaching. Colonies that maintained higher expression levels of these genes bleached severely. Return to normal levels of gene expression after stress has been termed transcriptome resilience, and in the case of some specific genes may signal the physiological health and response ability of individuals to environmental stress.
View details for DOI 10.1111/mec.13125
View details for Web of Science ID 000351631500006
View details for PubMedID 25728233
Marine defaunation: animal loss in the global ocean.
2015; 347 (6219)
Marine defaunation, or human-caused animal loss in the oceans, emerged forcefully only hundreds of years ago, whereas terrestrial defaunation has been occurring far longer. Though humans have caused few global marine extinctions, we have profoundly affected marine wildlife, altering the functioning and provisioning of services in every ocean. Current ocean trends, coupled with terrestrial defaunation lessons, suggest that marine defaunation rates will rapidly intensify as human use of the oceans industrializes. Though protected areas are a powerful tool to harness ocean productivity, especially when designed with future climate in mind, additional management strategies will be required. Overall, habitat degradation is likely to intensify as a major driver of marine wildlife loss. Proactive intervention can avert a marine defaunation disaster of the magnitude observed on land.
View details for DOI 10.1126/science.1255641
View details for PubMedID 25593191
Rapid Acclimation Ability Mediated by Transcriptome Changes in Reef-Building Corals.
Genome biology and evolution
2015; 7 (6): 1602-1612
Population response to environmental variation involves adaptation, acclimation, or both. For long-lived organisms, acclimation likely generates a faster response but is only effective if the rates and limits of acclimation match the dynamics of local environmental variation. In coral reef habitats, heat stress from extreme ocean warming can occur over several weeks, resulting in symbiont expulsion and widespread coral death. However, transcriptome regulation during short-term acclimation is not well understood. We examined acclimation during a 11-day experiment in the coral Acropora nana. We acclimated colonies to three regimes: ambient temperature (29 °C), increased stable temperature (31 °C), and variable temperature (29-33 °C), mimicking local heat stress conditions. Within 7-11 days, individuals acclimated to increased temperatures had higher tolerance to acute heat stress. Despite physiological changes, no gene expression changes occurred during acclimation before acute heat stress. However, we found strikingly different transcriptional responses to heat stress between acclimation treatments across 893 contigs. Across these contigs, corals acclimated to higher temperatures (31 °C or 29-33 °C) exhibited a muted stress response--the magnitude of expression change before and after heat stress was less than in 29 °C acclimated corals. Our results show that corals have a rapid phase of acclimation that substantially increases their heat resilience within 7 days and that alters their transcriptional response to heat stress. This is in addition to a previously observed longer term response, distinguishable by its shift in baseline expression, under nonstressful conditions. Such rapid acclimation may provide some protection for this species of coral against slow onset of warming ocean temperatures.
View details for DOI 10.1093/gbe/evv085
View details for PubMedID 25979751
View details for PubMedCentralID PMC4494073
Gene Networks in the Wild: Identifying Transcriptional Modules that Mediate Coral Resistance to Experimental Heat Stress.
Genome biology and evolution
2015; 8 (1): 243-252
Organisms respond to environmental variation partly through changes in gene expression, which underlie both homeostatic and acclimatory responses to environmental stress. In some cases, so many genes change in expression in response to different influences that understanding expression patterns for all these individual genes becomes difficult. To reduce this problem, we use a systems genetics approach to show that variation in the expression of thousands of genes of reef-building corals can be explained as variation in the expression of a small number of coexpressed "modules." Modules were often enriched for specific cellular functions and varied predictably among individuals, experimental treatments, and physiological state. We describe two transcriptional modules for which expression levels immediately after heat stress predict bleaching a day later. One of these early "bleaching modules" is enriched for sequence-specific DNA-binding proteins, particularly E26 transformation-specific (ETS)-family transcription factors. The other module is enriched for extracellular matrix proteins. These classes of bleaching response genes are clear in the modular gene expression analysis we conduct but are much more difficult to discern in single gene analyses. Furthermore, the ETS-family module shows repeated differences in expression among coral colonies grown in the same common garden environment, suggesting a heritable genetic or epigenetic basis for these expression polymorphisms. This finding suggests that these corals harbor high levels of gene-network variation, which could facilitate rapid evolution in the face of environmental change.
View details for DOI 10.1093/gbe/evv258
View details for PubMedID 26710855
- Marine Spatial Planning 2.0: genes and satellites to conserve seascape dynamics AQUATIC CONSERVATION-MARINE AND FRESHWATER ECOSYSTEMS 2014; 24 (6): 742-744
Multilocus Adaptation Associated with Heat Resistance in Reef-Building Corals
2014; 24 (24)
The evolution of tolerance to future climate change depends on the standing stock of genetic variation for resistance to climate-related impacts [1, 2], but genes contributing to climate tolerance in wild populations are poorly described in number and effect. Physiology and gene expression patterns have shown that corals living in naturally high-temperature microclimates are more resistant to bleaching because of both acclimation and fixed effects, including adaptation . To search for potential genetic correlates of these fixed effects, we genotyped 15,399 single nucleotide polymorphisms (SNPs) in 23 individual tabletop corals, Acropora hyacinthus, within a natural temperature mosaic in backreef lagoons on Ofu Island, American Samoa. Despite overall lack of population substructure, we identified 114 highly divergent SNPs as candidates for environmental selection, via multiple stringent outlier tests, and correlations with temperature. Corals from the warmest reef location had higher minor allele frequencies across these candidate SNPs, a pattern not seen for noncandidate loci. Furthermore, within backreef pools, colonies in the warmest microclimates had a higher number and frequency of alternative alleles at candidate loci. These data suggest mild selection for alternate alleles at many loci in these corals during high heat episodes and possible maintenance of extensive polymorphism through multilocus balancing selection in a heterogeneous environment. In this case, a natural population harbors a reservoir of alleles preadapted to high temperatures, suggesting potential for future evolutionary response to climate change.
View details for DOI 10.1016/j.cub.2014.10.044
View details for Web of Science ID 000346580700028
View details for PubMedID 25454780
Lineage-Specific Transcriptional Profiles of Symbiodinium spp. Unaltered by Heat Stress in a Coral Host.
Molecular biology and evolution
2014; 31 (6): 1343-1352
Dinoflagellates of the genus Symbiodinium form an endosymbiosis with reef building corals, in which photosynthetically derived nutrients comprise the majority of the coral energy budget. An extraordinary amount of functional and genetic diversity is contained within the coral-associated Symbiodinium, with some phylotypes (i.e., genotypic groupings), conferring enhanced stress tolerance to host corals. Recent advances in DNA sequencing technologies have enabled transcriptome-wide profiling of the stress response of the cnidarian coral host; however, a comprehensive understanding of the molecular response to stress of coral-associated Symbiodinium, as well as differences among physiologically susceptible and tolerant types, remains largely unexplored. Here, we examine the transcriptome-wide response to heat stress via RNA-Seq of two types of Symbiodinium, the putatively thermotolerant type D2 and the more susceptible type C3K, resident within the same coral host species, Acropora hyacinthus. Contrary to previous findings with coral hosts, we find no detectable change in gene expression across the dinoflagellate transcriptome after 3 days of elevated thermal exposure, despite physical evidence of symbiosis breakdown. However, hundreds of genes identified as orthologs between the C and D types exhibited significant expression differences within treatments (i.e., attributable solely to type, not heat exposure). These include many genes related to known thermotolerance mechanisms including heat shock proteins and chloroplast membrane components. Additionally, both the between-treatment similarities and between-type differences remained pervasive after 12-18 months of common garden acclimation and in mixed Symbiodinium assemblages within the same coral host colony.
View details for DOI 10.1093/molbev/msu107
View details for PubMedID 24651035
Mechanisms of reef coral resistance to future climate change.
2014; 344 (6186): 895-898
Reef corals are highly sensitive to heat, yet populations resistant to climate change have recently been identified. To determine the mechanisms of temperature tolerance, we reciprocally transplanted corals between reef sites experiencing distinct temperature regimes and tested subsequent physiological and gene expression profiles. Local acclimatization and fixed effects, such as adaptation, contributed about equally to heat tolerance and are reflected in patterns of gene expression. In less than 2 years, acclimatization achieves the same heat tolerance that we would expect from strong natural selection over many generations for these long-lived organisms. Our results show both short-term acclimatory and longer-term adaptive acquisition of climate resistance. Adding these adaptive abilities to ecosystem models is likely to slow predictions of demise for coral reef ecosystems.
View details for DOI 10.1126/science.1251336
View details for PubMedID 24762535
Translational environmental biology: cell biology informing conservation.
Trends in cell biology
2014; 24 (5): 265-267
Typically, findings from cell biology have been beneficial for preventing human disease. However, translational applications from cell biology can also be applied to conservation efforts, such as protecting coral reefs. Recent efforts to understand the cell biological mechanisms maintaining coral health such as innate immunity and acclimatization have prompted new developments in conservation. Similar to biomedicine, we urge that future efforts should focus on better frameworks for biomarker development to protect coral reefs.
View details for DOI 10.1016/j.tcb.2014.03.001
View details for PubMedID 24766840
For the Underwater Record ... A RANGE OF MARINE SPECIES LIVE SURPRISINGLY LONG LIVES.
2014; 122 (3): 34-39
View details for Web of Science ID 000358891100012
Meta-analysis reveals lower genetic diversity in overfished populations
2014; 23 (1): 29-39
While population declines can drive the loss of genetic diversity under some circumstances, it has been unclear whether this loss is a general consequence of overharvest in highly abundant marine fishes. We compiled data from 11 049 loci across 140 species and found that allelic richness was lower in overfished populations within 9 of 12 genera and families. A multiple linear regression showed that allelic richness was on average 12% lower (P < 0.0001) in overharvested populations after accounting for the effects of body size, latitude and other factors. Heterozygosity was on average 2% lower (P = 0.030). Simulations confirmed that these patterns are consistent with a recent bottleneck in abundant species and also showed that our analysis likely underestimates the loss of rare alleles by a factor of two or three. This evidence suggests that overharvest drives the decay of genetic diversity across a wide range of marine fishes. Such reductions of genetic diversity in some of the world's most abundant species may lead to a long-term impact of fishing on their evolutionary potential, particularly if abundance remains low and diversity continues to decay.
View details for DOI 10.1111/mec.12509
View details for Web of Science ID 000330950900006
View details for PubMedID 24372754
Forensic genomics as a novel tool for identifying the causes of mass mortality events.
2014; 5: 3652-?
Toxic spills, hypoxia, disease outbreaks and toxin-producing algal blooms are all possible causes of mass mortality events, but in many cases it can be difficult to pinpoint the cause of death. Here we present a new approach that we name 'forensic genomics', combining field surveys, toxin testing and genomic scans. Forensic genomics queries allele frequencies of surviving animals for signatures of agents causing mass mortality and, where genetic diversity is high, is uniquely suited to identify natural selection in action. As a proof of concept, we use this approach to investigate the causes of an invertebrate mass mortality event, and its genetic effects on an abalone population. Our results support that a harmful algal bloom producing a yessotoxin was a major causative agent to the event.
View details for DOI 10.1038/ncomms4652
View details for PubMedID 24736548
Signs of Adaptation to Local pH Conditions across an Environmental Mosaic in the California Current Ecosystem.
Integrative and comparative biology
2013; 53 (5): 857-870
Little is known about the potential for rapid evolution in natural populations in response to the high rate of contemporary climatic change. Organisms that have evolved in environments that experience high variability across space and time are of particular interest as they may harbor genetic variation that can facilitate evolutionary response to changing conditions. Here we review what is known about genetic capacity for adaptation in the purple sea urchin, Strongylocentrotus purpuratus, a species that has evolved in the upwelling ecosystem of the Northeast Pacific Ocean. We also present new results testing for adaptation to local pH conditions in six populations from Oregon to southern California. We integrate data on 19,493 genetic polymorphisms with data on local pH conditions. We find correlations between allele frequency and rank average time spent at pH <7.8 in 318 single-nucleotide polymorphisms in 275 genes. Two of the genes most correlated with local pH are a protein associated with the cytoskeleton and a proton pump, with functional roles in maintenance of cell volume and with internal regulation of pH, respectively. Across all loci tested, high correlations with local pH were concentrated in genes related to transport of ions, biomineralization, lipid metabolism, and cell-cell adhesion, functional pathways important for maintaining homeostasis at low pH. We identify a set of seven genes as top candidates for rapid evolutionary response to acidification of the ocean. In these genes, the putative low-pH-adapted allele, based on allele frequencies in natural populations, rapidly increases in frequency in purple sea urchin larvae raised at low pH. We also found that populations from localities with high pH show a greater change in allele frequency toward putative low-pH-adapted alleles under experimental acidification, compared with low-pH populations, suggesting that both natural and artificial selection favor the same alleles for response to low pH. These results illustrate that purple sea urchins may be adapted to local pH and suggest that this species may possess the genetic capacity for rapid evolution in response to acidification. This adaptive capacity likely comes from standing genetic variation maintained in nature by balancing selection across the spatial and temporal environmental mosaic that characterizes the California Current Ecosystem.
View details for DOI 10.1093/icb/ict094
View details for PubMedID 23980118
Coral bleaching independent of photosynthetic activity.
2013; 23 (18): 1782-1786
The global decline of reef-building corals is due in part to the loss of algal symbionts, or "bleaching," during the increasingly frequent periods of high seawater temperatures [1, 2]. During bleaching, endosymbiotic dinoflagellate algae (Symbiodinium spp.) either are lost from the animal tissue or lose their photosynthetic pigments, resulting in host mortality if the Symbiodinium populations fail to recover . The >1,000 studies of the causes of heat-induced bleaching have focused overwhelmingly on the consequences of damage to algal photosynthetic processes [4-6], and the prevailing model for bleaching invokes a light-dependent generation of toxic reactive oxygen species (ROS) by heat-damaged chloroplasts as the primary trigger [6-8]. However, the precise mechanisms of bleaching remain unknown, and there is evidence for involvement of multiple cellular processes [9, 10]. In this study, we asked the simple question of whether bleaching can be triggered by heat in the dark, in the absence of photosynthetically derived ROS. We used both the sea anemone model system Aiptasia [11, 12] and several species of reef-building corals to demonstrate that symbiont loss can occur rapidly during heat stress in complete darkness. Furthermore, we observed damage to the photosynthetic apparatus under these conditions in both Aiptasia endosymbionts and cultured Symbiodinium. These results do not directly contradict the view that light-stimulated ROS production is important in bleaching, but they do show that there must be another pathway leading to bleaching. Elucidation of this pathway should help to clarify bleaching mechanisms under the more usual conditions of heat stress in the light.
View details for DOI 10.1016/j.cub.2013.07.041
View details for PubMedID 24012312
Signals of selection in outlier loci in a widely dispersing species across an environmental mosaic.
2013; 22 (13): 3580-3597
Local adaptation reflects a balance between natural selection and gene flow and is classically thought to require the retention of locally adapted alleles. However, organisms with high dispersal potential across a spatially or temporally heterogeneous landscape pose an interesting challenge to this view requiring local selection every generation or when environmental conditions change to generate adaptation in adults. Here, we test for geographical and sequence-based signals of selection in five putatively adaptive and two putatively neutral genes identified in a previous genome scan of the highly dispersing purple sea urchin, Strongylocentrotus purpuratus. Comparing six populations spanning the species' wide latitudinal range from Canada to Baja California, Mexico, we find positive tests for selection in the putative adaptive genes and not in the putative neutral genes. Specifically, we find an excess of low-frequency and nonsynonymous polymorphisms in two transcription factors and a transporter protein, and an excess of common amino acid polymorphisms in the two transcription factors, suggestive of spatially balancing selection. We test for a genetic correlation with temperature, a dominant environmental variable in this coastal ecosystem. We find mild clines and a stronger association of genetic variation with temperature than latitude in four of the five putative adaptive loci and a signal of local adaptation in the Southern California Bight. Overall, patterns of genetic variation match predictions based on spatially or temporally balancing selection in a heterogeneous landscape and illustrate the value of geographical and coalescent tests on candidate loci identified in a genome-wide scan for selection.
View details for DOI 10.1111/mec.12337
View details for PubMedID 23802552
DIFFERENCES IN THE REGULATION OF GROWTH AND BIOMINERALIZATION GENES REVEALED THROUGH LONG-TERM COMMON-GARDEN ACCLIMATION AND EXPERIMENTAL GENOMICS IN THE PURPLE SEA URCHIN
2013; 67 (7): 1901-1914
Across heterogeneous landscapes, populations may have adaptive differences in gene regulation that adjust their physiologies to match local environments. Such differences could have origins in acclimation or in genetically fixed variation between habitats. Here we use common-garden experiments to evaluate differences in gene expression between populations of the purple sea urchin, Strongylocentrotus purpuratus, spanning 1700 km and average temperature differences of 5°C to 8°C. Across expression profiles from 18,883 genes after 3 years of common conditions, we find highly correlated expression patterns (Pearson's r = 0.992) among most genes. However, 66 genes were differentially expressed, including many ribosomal protein and biomineralization genes, which had higher expression in urchins originally from the southern population. Gene function analyses revealed slight but pervasive expression differences in genes related to ribosomal function, metabolism, transport, "bone" development, and response to stimuli. In accord with gene expression patterns, a post-hoc spine regrowth experiment revealed that urchins of southern origin regrew spines at a faster rate than northern urchins. These results suggest that there may be genetically controlled, potentially adaptive differences in gene regulation across habitats and that gene expression differences may be under strong enough selection to overcome high, dispersal-mediated gene flow in this marine species.
View details for DOI 10.1111/evo.12036
View details for Web of Science ID 000321184500007
View details for PubMedID 23815648
The Ecology of Microbial Communities Associated with Macrocystis pyrifera.
2013; 8 (6): e67480
Kelp forests are characterized by high biodiversity and productivity, and the cycling of kelp-produced carbon is a vital process in this ecosystem. Although bacteria are assumed to play a major role in kelp forest carbon cycling, knowledge of the composition and diversity of these bacterial communities is lacking. Bacterial communities on the surface of Macrocystis pyrifera and adjacent seawater were sampled at the Hopkins Marine Station in Monterey Bay, CA, and further studied using 454-tag pyrosequencing of 16S RNA genes. Our results suggest that M. pyrifera-dominated kelp forests harbor distinct microbial communities that vary temporally. The distribution of sequence tags assigned to Gammaproteobacteria, Alphaproteobacteria and Bacteriodetes differed between the surface of the kelp and the surrounding water. Several abundant Rhodobacteraceae, uncultivated Gammaproteobacteria and Bacteriodetes-associated tags displayed considerable temporal variation, often with similar trends in the seawater and the surface of the kelp. Bacterial community structure and membership correlated with the kelp surface serving as host, and varied over time. Several kelp-specific taxa were highly similar to other bacteria known to either prevent the colonization of eukaryotic larvae or exhibit antibacterial activities. Some of these kelp-specific bacterial associations might play an important role for M. pyrifera. This study provides the first assessment of the diversity and phylogenetic profile of the bacterial communities associated with M. pyrifera.
View details for DOI 10.1371/journal.pone.0067480
View details for PubMedID 23840715
View details for PubMedCentralID PMC3686729
- The Ecology of Microbial Communities Associated with Macrocystis pyrifera PLOS ONE 2013; 8 (6)
Transcriptome-wide polymorphisms of red abalone (Haliotis rufescens) reveal patterns of gene flow and local adaptation.
2013; 22 (11): 2884-2897
Global climate change is projected to accelerate during the next century, altering oceanic patterns in temperature, pH and oxygen concentrations. Documenting patterns of genetic adaptation to these variables in locations that currently experience geographic variation in them is an important tool in understanding the potential for natural selection to allow populations to adapt as climate change proceeds. We sequenced the mantle transcriptome of 39 red abalone (Haliotis rufescens) individuals from three regions (Monterey Bay, Sonoma, north of Cape Mendocino) distinct in temperature, aragonite saturation, exposure to hypoxia and disease pressure along the California coast. Among 1.17 × 10(6) Single Nucleotide Polymorphisms (SNPs) identified in this study (1.37% of the transcriptome), 21 579 could be genotyped for all individuals. A principal components analysis concluded that the vast majority of SNPs show no population structure from Monterey, California to the Oregon border, in corroboration with several previous studies. In contrast, an FST outlier analysis indicated 691 SNPs as exhibiting significantly higher than expected differentiation (experiment-wide P < 0.05). From these, it was possible to identify 163 genes through BLAST annotation, 34 of which contained more than one outlier SNP. A large number of these genes are involved in biomineralization, energy metabolism, heat-, disease- or hypoxia-tolerance. These genes are candidate loci for spatial adaptation to geographic variation that is likely to increase in the future.
View details for DOI 10.1111/mec.12081
View details for PubMedID 23106543
Microevolution in time and space: SNP analysis of historical DNA reveals dynamic signatures of selection in Atlantic cod
2013; 22 (9): 2424-2440
Little is known about how quickly natural populations adapt to changes in their environment and how temporal and spatial variation in selection pressures interact to shape patterns of genetic diversity. We here address these issues with a series of genome scans in four overfished populations of Atlantic cod (Gadus morhua) studied over an 80-year period. Screening of >1000 gene-associated single-nucleotide polymorphisms (SNPs) identified 77 loci that showed highly elevated levels of differentiation, likely as an effect of directional selection, in either time, space or both. Exploratory analysis suggested that temporal allele frequency shifts at certain loci may correlate with local temperature variation and with life history changes suggested to be fisheries induced. Interestingly, however, largely nonoverlapping sets of loci were temporal outliers in the different populations and outliers from the 1928 to 1960 period showed almost complete stability during later decades. The contrasting microevolutionary trajectories among populations resulted in sequential shifts in spatial outliers, with no locus maintaining elevated spatial differentiation throughout the study period. Simulations of migration coupled with observations of temporally stable spatial structure at neutral loci suggest that population replacement or gene flow alone could not explain all the observed allele frequency variation. Thus, the genetic changes are likely to at least partly be driven by highly dynamic temporally and spatially varying selection. These findings have important implications for our understanding of local adaptation and evolutionary potential in high gene flow organisms and underscore the need to carefully consider all dimensions of biocomplexity for evolutionarily sustainable management.
View details for DOI 10.1111/mec.12260
View details for Web of Science ID 000318111100009
View details for PubMedID 23551301
- Dispersal at a Snail's Pace: Historical Processes Affect Contemporary Genetic Structure in the Exploited Wavy Top Snail (Megastraea undosa) JOURNAL OF HEREDITY 2013; 104 (3): 327-340
Dispersal at a snail's pace: historical processes affect contemporary genetic structure in the exploited wavy top snail (Megastraea undosa).
journal of heredity
2013; 104 (3): 327-340
We used population genetics to assess historical and modern demography of the exploited wavy top snail, Megastraea undosa, which has a 5-10 day pelagic larval duration. Foot tissue was sampled from an average of 51 individuals at 17 sites across the range of M. undosa. Genetic structure at the mtDNA locus is strikingly high (ΦST of 0.19 across 1000 km), and a major cline occurs in northern Baja California (ΦCT of 0.29 between northern and southern populations). Genetic data indicate that the northern region is highly connected through larval dispersal, whereas the southern region exhibits low genetic structure. However, additional analyses based on patterns of haplotype diversity and relationships among haplotypes indicate that M. undosa has likely recently expanded into the Southern California Bight or expanded from a small refugial population, and analysis using isolation by distance to calculate dispersal distance indicates surprisingly short estimates of dispersal from 30 m to 3 km. This scenario of a northward expansion and limited larval dispersal is supported by coalescent-based simulations of genetic data. The different patterns of genetic variation between northern and southern populations are likely artifacts of evolutionary history rather than differences in larval dispersal and this may have applications to management of this species. Specifically, these data can help to inform the scale at which this species should be managed, and given the potentially very small dispersal distances, this species should be managed at local scales. Consideration of the evolutionary history of target species allows for a more accurate interpretation of genetic data for management.
View details for DOI 10.1093/jhered/est002
View details for PubMedID 23450089
Evolutionary change during experimental ocean acidification.
Proceedings of the National Academy of Sciences of the United States of America
2013; 110 (17): 6937-6942
Rising atmospheric carbon dioxide (CO2) conditions are driving unprecedented changes in seawater chemistry, resulting in reduced pH and carbonate ion concentrations in the Earth's oceans. This ocean acidification has negative but variable impacts on individual performance in many marine species. However, little is known about the adaptive capacity of species to respond to an acidified ocean, and, as a result, predictions regarding future ecosystem responses remain incomplete. Here we demonstrate that ocean acidification generates striking patterns of genome-wide selection in purple sea urchins (Strongylocentrotus purpuratus) cultured under different CO2 levels. We examined genetic change at 19,493 loci in larvae from seven adult populations cultured under realistic future CO2 levels. Although larval development and morphology showed little response to elevated CO2, we found substantial allelic change in 40 functional classes of proteins involving hundreds of loci. Pronounced genetic changes, including excess amino acid replacements, were detected in all populations and occurred in genes for biomineralization, lipid metabolism, and ion homeostasis-gene classes that build skeletons and interact in pH regulation. Such genetic change represents a neglected and important impact of ocean acidification that may influence populations that show few outward signs of response to acidification. Our results demonstrate the capacity for rapid evolution in the face of ocean acidification and show that standing genetic variation could be a reservoir of resilience to climate change in this coastal upwelling ecosystem. However, effective response to strong natural selection demands large population sizes and may be limited in species impacted by other environmental stressors.
View details for DOI 10.1073/pnas.1220673110
View details for PubMedID 23569232
View details for PubMedCentralID PMC3637708
- Long-term population size of the North Atlantic humpback whale within the context of worldwide population structure CONSERVATION GENETICS 2013; 14 (1): 103-114
Genomic basis for coral resilience to climate change
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
2013; 110 (4): 1387-1392
Recent advances in DNA-sequencing technologies now allow for in-depth characterization of the genomic stress responses of many organisms beyond model taxa. They are especially appropriate for organisms such as reef-building corals, for which dramatic declines in abundance are expected to worsen as anthropogenic climate change intensifies. Different corals differ substantially in physiological resilience to environmental stress, but the molecular mechanisms behind enhanced coral resilience remain unclear. Here, we compare transcriptome-wide gene expression (via RNA-Seq using Illumina sequencing) among conspecific thermally sensitive and thermally resilient corals to identify the molecular pathways contributing to coral resilience. Under simulated bleaching stress, sensitive and resilient corals change expression of hundreds of genes, but the resilient corals had higher expression under control conditions across 60 of these genes. These "frontloaded" transcripts were less up-regulated in resilient corals during heat stress and included thermal tolerance genes such as heat shock proteins and antioxidant enzymes, as well as a broad array of genes involved in apoptosis regulation, tumor suppression, innate immune response, and cell adhesion. We propose that constitutive frontloading enables an individual to maintain physiological resilience during frequently encountered environmental stress, an idea that has strong parallels in model systems such as yeast. Our study provides broad insight into the fundamental cellular processes responsible for enhanced stress tolerances that may enable some organisms to better persist into the future in an era of global climate change.
View details for DOI 10.1073/pnas.1210224110
View details for Web of Science ID 000314453900053
View details for PubMedID 23297204
View details for PubMedCentralID PMC3557039
Protein evolution in two co-occurring types of Symbiodinium: an exploration into the genetic basis of thermal tolerance in Symbiodinium clade D
BMC EVOLUTIONARY BIOLOGY
The symbiosis between reef-building corals and photosynthetic dinoflagellates (Symbiodinium) is an integral part of the coral reef ecosystem, as corals are dependent on Symbiodinium for the majority of their energy needs. However, this partnership is increasingly at risk due to changing climatic conditions. It is thought that functional diversity within Symbiodinium may allow some corals to rapidly adapt to different environments by changing the type of Symbiodinium with which they partner; however, very little is known about the molecular basis of the functional differences among symbiont groups. One group of Symbiodinium that is hypothesized to be important for the future of reefs is clade D, which, in general, seems to provide the coral holobiont (i.e., coral host and associated symbiont community) with elevated thermal tolerance. Using high-throughput sequencing data from field-collected corals we assembled, de novo, draft transcriptomes for Symbiodinium clades C and D. We then explore the functional basis of thermal tolerance in clade D by comparing rates of coding sequence evolution among the four clades of Symbiodinium most commonly found in reef-building corals (A-D).We are able to highlight a number of genes and functional categories as candidates for involvement in the increased thermal tolerance of clade D. These include a fatty acid desaturase, molecular chaperones and proteins involved in photosynthesis and the thylakoid membrane. We also demonstrate that clades C and D co-occur within most of the sampled colonies of Acropora hyacinthus, suggesting widespread potential for this coral species to acclimatize to changing thermal conditions via 'shuffling' the proportions of these two clades from within their current symbiont communities.Transcriptome-wide analysis confirms that the four main Symbiodinium clades found within corals exhibit extensive evolutionary divergence (18.5-27.3% avg. pairwise nucleotide difference). Despite these evolutionary distinctions, many corals appear to host multiple clades simultaneously, which may allow for rapid acclimatization to changing environmental conditions. This study provides a first step toward understanding the molecular basis of functional differences between Symbiodinium clades by highlighting a number of genes with signatures consistent with positive selection along the thermally tolerant clade D lineage.
View details for DOI 10.1186/1471-2148-12-217
View details for Web of Science ID 000315454200001
View details for PubMedID 23145489
The simple fool's guide to population genomics via RNA-Seq: an introduction to high-throughput sequencing data analysis
MOLECULAR ECOLOGY RESOURCES
2012; 12 (6): 1058-1067
High-throughput sequencing technologies are currently revolutionizing the field of biology and medicine, yet bioinformatic challenges in analysing very large data sets have slowed the adoption of these technologies by the community of population biologists. We introduce the 'Simple Fool's Guide to Population Genomics via RNA-seq' (SFG), a document intended to serve as an easy-to-follow protocol, walking a user through one example of high-throughput sequencing data analysis of nonmodel organisms. It is by no means an exhaustive protocol, but rather serves as an introduction to the bioinformatic methods used in population genomics, enabling a user to gain familiarity with basic analysis steps. The SFG consists of two parts. This document summarizes the steps needed and lays out the basic themes for each and a simple approach to follow. The second document is the full SFG, publicly available at http://sfg.stanford.edu, that includes detailed protocols for data processing and analysis, along with a repository of custom-made scripts and sample files. Steps included in the SFG range from tissue collection to de novo assembly, blast annotation, alignment, gene expression, functional enrichment, SNP detection, principal components and F(ST) outlier analyses. Although the technical aspects of population genomics are changing very quickly, our hope is that this document will help population biologists with little to no background in high-throughput sequencing and bioinformatics to more quickly adopt these new techniques.
View details for DOI 10.1111/1755-0998.12003
View details for Web of Science ID 000309739700010
View details for PubMedID 22931062
Open and closed seascapes: Where does habitat patchiness create populations with high fractions of self-recruitment?
2012; 22 (4): 1257-1267
Which populations are replenished primarily by immigrants (open) and which by local production (closed) remains an important question for management with implications for response to exploitation, protection, and disturbance. However, we lack methods for predicting population openness. Here, we develop a model for openness and show that considering habitat isolation explains the existence of surprisingly closed populations in high-dispersal species, including many marine organisms. Relatively closed populations are expected when patch spacing is more than twice the standard deviation of a species'. dispersal kernel. In addition, natural scales of habitat patchiness on coral reefs are sufficient to create both largely open and largely closed populations. Contrary to some previous interpretations, largely closed marine populations do not require mean dispersal distances that are unusually short, even for species with relatively long pelagic larval durations. We predict that habitat patchiness has strong control over population openness for many marine and terrestrial species with a highly dispersive life stage and relatively sedentary adults. This information can be used to make initial predictions about where populations will be more or less resilient to local exploitation and disturbance.
View details for Web of Science ID 000305836600016
View details for PubMedID 22827133
Pre-Whaling Genetic Diversity and Population Ecology in Eastern Pacific Gray Whales: Insights from Ancient DNA and Stable Isotopes
2012; 7 (5)
Commercial whaling decimated many whale populations, including the eastern Pacific gray whale, but little is known about how population dynamics or ecology differed prior to these removals. Of particular interest is the possibility of a large population decline prior to whaling, as such a decline could explain the ~5-fold difference between genetic estimates of prior abundance and estimates based on historical records. We analyzed genetic (mitochondrial control region) and isotopic information from modern and prehistoric gray whales using serial coalescent simulations and Bayesian skyline analyses to test for a pre-whaling decline and to examine prehistoric genetic diversity, population dynamics and ecology. Simulations demonstrate that significant genetic differences observed between ancient and modern samples could be caused by a large, recent population bottleneck, roughly concurrent with commercial whaling. Stable isotopes show minimal differences between modern and ancient gray whale foraging ecology. Using rejection-based Approximate Bayesian Computation, we estimate the size of the population bottleneck at its minimum abundance and the pre-bottleneck abundance. Our results agree with previous genetic studies suggesting the historical size of the eastern gray whale population was roughly three to five times its current size.
View details for DOI 10.1371/journal.pone.0035039
View details for Web of Science ID 000305336100005
View details for PubMedID 22590499
View details for PubMedCentralID PMC3348926
Extensive sympatry, cryptic diversity and introgression throughout the geographic distribution of two coral species complexes
2012; 21 (9): 2224-2238
The identification of species is one of the most basic, and yet critically important, issues in biology with far-reaching potential implications for fields such as biodiversity conservation, population ecology and epidemiology. Morphology has long been the primary tool biologists have used to categorize life. However, we now know that a significant portion of natural diversity is morphologically hidden, and therefore, we must integrate nonmorphological tools into the description of biodiversity. Here, we demonstrate the utility of multilocus population genetic data for identifying and characterizing cryptic species complexes, even when species share large amounts of genetic variability. Specifically, we have used DNA sequence data from 12 genomic regions to characterize two widespread species complexes in the coral genus Acropora: A. cytherea and A. hyacinthus. These two morphospecies have each been sampled from 5 to 7 locations throughout their Indo-Pacific distributions, and with the use of structure and hierarchical clustering, we demonstrate the presence of at least six widespread cryptic species within these two morphospecies complexes. After identifying cryptic lineages, we then utilize the genetic data to examine the history of introgressive hybridization within and between these morphospecies complexes. Our data indicate that these two complexes form a global syngameon with consistent patterns of introgression between species across large geographic distributions.
View details for DOI 10.1111/j.1365-294X.2012.05528.x
View details for Web of Science ID 000302932500014
View details for PubMedID 22439812
OCEANOGRAPHY Ultra marine
2012; 484 (7395): 445-446
View details for Web of Science ID 000303200400023
Genome-wide polymorphisms show unexpected targets of natural selection
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES
2012; 279 (1732): 1412-1420
Natural selection can act on all the expressed genes of an individual, leaving signatures of genetic differentiation or diversity at many loci across the genome. New power to assay these genome-wide effects of selection comes from associating multi-locus patterns of polymorphism with gene expression and function. Here, we performed one of the first genome-wide surveys in a marine species, comparing purple sea urchins, Strongylocentrotus purpuratus, from two distant locations along the species' wide latitudinal range. We examined 9112 polymorphic loci from upstream non-coding and coding regions of genes for signatures of selection with respect to gene function and tissue- and ontogenetic gene expression. We found that genetic differentiation (F(ST)) varied significantly across functional gene classes. The strongest enrichment occurred in the upstream regions of E3 ligase genes, enzymes known to regulate protein abundance during development and environmental stress. We found enrichment for high heterozygosity in genes directly involved in immune response, particularly NALP genes, which mediate pro-inflammatory signals during bacterial infection. We also found higher heterozygosity in immune genes in the southern population, where disease incidence and pathogen diversity are greater. Similar to the major histocompatibility complex in mammals, balancing selection may enhance genetic diversity in the innate immune system genes of this invertebrate. Overall, our results show that how genome-wide polymorphism data coupled with growing databases on gene function and expression can combine to detect otherwise hidden signals of selection in natural populations.
View details for DOI 10.1098/rspb.2011.1823
View details for Web of Science ID 000300822400021
View details for PubMedID 21993504
View details for PubMedCentralID PMC3282374
- The role of genes in understanding the evolutionary ecology of reef building corals EVOLUTIONARY ECOLOGY 2012; 26 (2): 317-335
- Coastal fronts set recruitment and connectivity patterns across multiple taxa LIMNOLOGY AND OCEANOGRAPHY 2012; 57 (2): 582-596
- Do fluctuating temperature environments elevate coral thermal tolerance? CORAL REEFS 2011; 30 (2): 429-440
Populations of Symbiodinium muscatinei Show Strong Biogeographic Structuring in the Intertidal Anemone Anthopleura elegantissima
2011; 220 (3): 199-208
Among temperate cnidarian symbioses, the partnership between the intertidal anemone Anthopleura elegantissima and its dinoflagellate and chlorophyte symbionts is one of the most well characterized. Biogeographic, reciprocal transplant, and physiological studies have convincingly demonstrated a relationship between environmental factors such as temperature and irradiance and the distribution of symbionts from both algal phyla. However, little is known about the fine-scale diversity or biogeographic distribution within symbiont lineages of this anemone. We used sequence information from the mitochondrial cytochrome b and chloroplast 23S ribosomal genes and restriction fragment length polymorphism data from the 18S nuclear ribosomal gene to characterize the Symbiodinium populations in tentacles clipped from 105 anemones at 14 sites along the entire California coast, spanning about 1200 km. Our results show the presence of at least three primary biogeographic regions with breaks around Cape Mendocino and Monterey Bay, each dominated by a different Symbiodinium muscatinei genotype. Sharp clines suggest limited gene flow between adjacent regions. Few sampling locations or individual anemones showed symbiont diversity at either organellar locus within the limits of our detection method, while sequence analysis of cloned nr18S polymerase chain reaction product suggests that nuclear pseudogenes may underlie intra-host diversity observed at that locus.
View details for Web of Science ID 000292532300005
View details for PubMedID 21712228
Unexpected patterns of fisheries collapse in the world's oceans
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
2011; 108 (20): 8317-8322
Understanding which species are most vulnerable to human impacts is a prerequisite for designing effective conservation strategies. Surveys of terrestrial species have suggested that large-bodied species and top predators are the most at risk, and it is commonly assumed that such patterns also apply in the ocean. However, there has been no global test of this hypothesis in the sea. We analyzed two fisheries datasets (stock assessments and landings) to determine the life-history traits of species that have suffered dramatic population collapses. Contrary to expectations, our data suggest that up to twice as many fisheries for small, low trophic-level species have collapsed compared with those for large predators. These patterns contrast with those on land, suggesting fundamental differences in the ways that industrial fisheries and land conversion affect natural communities. Even temporary collapses of small, low trophic-level fishes can have ecosystem-wide impacts by reducing food supply to larger fish, seabirds, and marine mammals.
View details for DOI 10.1073/pnas.1015313108
View details for Web of Science ID 000290719600050
View details for PubMedID 21536889
View details for PubMedCentralID PMC3100948
- Many corals host thermally resistant symbionts in high-temperature habitat CORAL REEFS 2011; 30 (1): 241-250
- Coastal upwelling is linked to temporal genetic variability in the acorn barnacle Balanus glandula MARINE ECOLOGY PROGRESS SERIES 2011; 439: 139-150
Designing marine reserve networks for both conservation and fisheries management
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
2010; 107 (43): 18286-18293
Marine protected areas (MPAs) that exclude fishing have been shown repeatedly to enhance the abundance, size, and diversity of species. These benefits, however, mean little to most marine species, because individual protected areas typically are small. To meet the larger-scale conservation challenges facing ocean ecosystems, several nations are expanding the benefits of individual protected areas by building networks of protected areas. Doing so successfully requires a detailed understanding of the ecological and physical characteristics of ocean ecosystems and the responses of humans to spatial closures. There has been enormous scientific interest in these topics, and frameworks for the design of MPA networks for meeting conservation and fishery management goals are emerging. Persistent in the literature is the perception of an inherent tradeoff between achieving conservation and fishery goals. Through a synthetic analysis across these conservation and bioeconomic studies, we construct guidelines for MPA network design that reduce or eliminate this tradeoff. We present size, spacing, location, and configuration guidelines for designing networks that simultaneously can enhance biological conservation and reduce fishery costs or even increase fishery yields and profits. Indeed, in some settings, a well-designed MPA network is critical to the optimal harvest strategy. When reserves benefit fisheries, the optimal area in reserves is moderately large (mode ≈30%). Assessing network design principals is limited currently by the absence of empirical data from large-scale networks. Emerging networks will soon rectify this constraint.
View details for DOI 10.1073/pnas.0906473107
View details for Web of Science ID 000283677400015
View details for PubMedID 20200311
- Guiding ecological principles for marine spatial planning MARINE POLICY 2010; 34 (5): 955-966
USING ISOLATION BY DISTANCE AND EFFECTIVE DENSITY TO ESTIMATE DISPERSAL SCALES IN ANEMONEFISH
2010; 64 (9): 2688-2700
Robust estimates of dispersal are critical for understanding population dynamics and local adaptation, as well as for successful spatial management. Genetic isolation by distance patterns hold clues to dispersal, but understanding these patterns quantitatively has been complicated by uncertainty in effective density. In this study, we genotyped populations of a coral reef fish (Amphiprion clarkii) at 13 microsatellite loci to uncover fine-scale isolation by distance patterns in two replicate transects. Temporal changes in allele frequencies between generations suggested that effective densities in these populations are 4-21 adults/km. A separate estimate from census densities suggested that effective densities may be as high as 82-178 adults/km. Applying these effective densities with isolation by distance theory suggested that larval dispersal kernels in A. clarkii had a spread near 11 km (4-27 km). These kernels predicted low fractions of self-recruitment in continuous habitats, but the same kernels were consistent with previously reported, high self-recruitment fractions (40-60%) when realistic levels of habitat patchiness were considered. Our results suggested that ecologically relevant larval dispersal can be estimated with widely available genetic methods when effective density is measured carefully through cohort sampling and ecological censuses, and that self-recruitment studies should be interpreted in light of habitat patchiness.
View details for DOI 10.1111/j.1558-5646.2010.01003.x
View details for Web of Science ID 000281636400016
View details for PubMedID 20394657
Seascape genetics along a steep cline: using genetic patterns to test predictions of marine larval dispersal
2010; 19 (17): 3692-3707
Coupled biological and physical oceanographic models are powerful tools for studying connectivity among marine populations because they simulate the movement of larvae based on ocean currents and larval characteristics. However, while the models themselves have been parameterized and verified with physical empirical data, the simulated patterns of connectivity have rarely been compared to field observations. We demonstrate a framework for testing biological-physical oceanographic models by using them to generate simulated spatial genetic patterns through a simple population genetic model, and then testing these predictions with empirical genetic data. Both agreement and mismatches between predicted and observed genetic patterns can provide insights into mechanisms influencing larval connectivity in the coastal ocean. We use a high-resolution ROMS-CoSINE biological-physical model for Monterey Bay, California specifically modified to simulate dispersal of the acorn barnacle, Balanus glandula. Predicted spatial genetic patterns generated from both seasonal and annual connectivity matrices did not match an observed genetic cline in this species at either a mitochondrial or nuclear gene. However, information from this mismatch generated hypotheses testable with our modelling framework that including natural selection, larval input from a southern direction and/or increased nearshore larval retention might provide a better fit between predicted and observed patterns. Indeed, moderate selection and a range of combined larval retention and southern input values dramatically improve the fit between simulated and observed spatial genetic patterns. Our results suggest that integrating population genetic models with coupled biological-physical oceanographic models can provide new insights and a new means of verifying model predictions.
View details for DOI 10.1111/j.1365-294X.2010.04694.x
View details for Web of Science ID 000281285200015
View details for PubMedID 20723046
A Method for Detecting Population Genetic Structure in Diverse, High Gene-Flow Species
JOURNAL OF HEREDITY
2010; 101 (4): 423-436
Detecting small amounts of genetic subdivision across geographic space remains a persistent challenge. Often a failure to detect genetic structure is mistaken for evidence of panmixia, when more powerful statistical tests may uncover evidence for subtle geographic differentiation. Such slight subdivision can be demographically and evolutionarily important as well as being critical for management decisions. We introduce here a method, called spatial analysis of shared alleles (SAShA), that detects geographically restricted alleles by comparing the spatial arrangement of allelic co-occurrences with the expectation under panmixia. The approach is allele-based and spatially explicit, eliminating the loss of statistical power that can occur with user-defined populations and statistical averaging within populations. Using simulated data sets generated under a stepping-stone model of gene flow, we show that this method outperforms spatial autocorrelation (SA) and Phi(ST) under common real-world conditions: at relatively high migration rates when diversity is moderate or high, especially when sampling is poor. We then use this method to show clear differences in the genetic patterns of 2 nearshore Pacific mollusks, Tegula funebralis (= Chlorostoma funebralis) and Katharina tunicata, whose overall patterns of within-species differentiation are similar according to traditional population genetics analyses. SAShA meaningfully complements Phi(ST)/F(ST), SA, and other existing geographic genetic analyses and is especially appropriate for evaluating species with high gene flow and subtle genetic differentiation.
View details for DOI 10.1093/jhered/esq022
View details for Web of Science ID 000279430300004
View details for PubMedID 20219885
- Life history, ecology and the biogeography of strong genetic breaks among 15 species of Pacific rockfish, Sebastes MARINE BIOLOGY 2010; 157 (7): 1433-1452
Parallel amino acid replacements in the rhodopsins of the rockfishes (Sebastes spp.) associated with shifts in habitat depth
JOURNAL OF EVOLUTIONARY BIOLOGY
2010; 23 (6): 1159-1169
Among various groups of fishes, a shift in peak wavelength sensitivity has been correlated with changes in their photic environments. The genus Sebastes is a radiation of marine fish species that inhabit a wide range of depths from intertidal to over 600 m. We examined 32 species of Sebastes for evidence of adaptive amino acid substitution at the rhodopsin gene. Fourteen amino acid positions were variable among these species. Maximum likelihood analyses identify several of these to be targets of positive selection. None of these correspond to previously identified critical amino acid sites, yet they may in fact be functionally important. The occurrence of independent parallel changes at certain amino acid positions reinforces this idea. Reconstruction of habitat depths of ancestral nodes in the phylogeny suggests that shallow habitats have been colonized independently in different lineages. The evolution of rhodopsin appears to be associated with changes in depth, with accelerated evolution in lineages that have had large changes in depth.
View details for DOI 10.1111/j.1420-9101.2010.01977.x
View details for Web of Science ID 000277710100005
View details for PubMedID 20345807
COMPREHENSIVE PLANNING, DOMINANT-USE ZONES, AND USER RIGHTS: A NEW ERA IN OCEAN GOVERNANCE
7th William R and Lenore Mote International Symposium in Fisheries Ecology
ROSENSTIEL SCH MAR ATMOS SCI. 2010: 273–85
View details for Web of Science ID 000278021900009
Genetic Structure Among 50 Species of the Northeastern Pacific Rocky Intertidal Community
2010; 5 (1)
Comparing many species' population genetic patterns across the same seascape can identify species with different levels of structure, and suggest hypotheses about the processes that cause such variation for species in the same ecosystem. This comparative approach helps focus on geographic barriers and selective or demographic processes that define genetic connectivity on an ecosystem scale, the understanding of which is particularly important for large-scale management efforts. Moreover, a multispecies dataset has great statistical advantages over single-species studies, lending explanatory power in an effort to uncover the mechanisms driving population structure. Here, we analyze a 50-species dataset of Pacific nearshore invertebrates with the aim of discovering the most influential structuring factors along the Pacific coast of North America. We collected cytochrome c oxidase I (COI) mtDNA data from populations of 34 species of marine invertebrates sampled coarsely at four coastal locations in California, Oregon, and Alaska, and added published data from 16 additional species. All nine species with non-pelagic development have strong genetic structure. For the 41 species with pelagic development, 13 show significant genetic differentiation, nine of which show striking FST levels of 0.1-0.6. Finer scale geographic investigations show unexpected regional patterns of genetic change near Cape Mendocino in northern California for five of the six species tested. The region between Oregon and Alaska is a second focus of intraspecific genetic change, showing differentiation in half the species tested. Across regions, strong genetic subdivision occurs more often than expected in mid-to-high intertidal species, a result that may reflect reduced gene flow due to natural selection along coastal environmental gradients. Finally, the results highlight the importance of making primary research accessible to policymakers, as unexpected barriers to marine dispersal break the coast into separate demographic zones that may require their own management plans.
View details for DOI 10.1371/journal.pone.0008594
View details for Web of Science ID 000273414100004
View details for PubMedID 20062807
View details for PubMedCentralID PMC2799524
Restriction Site Tiling Analysis: accurate discovery and quantitative genotyping of genome-wide polymorphisms using nucleotide arrays
2010; 11 (4)
High-throughput genotype data can be used to identify genes important for local adaptation in wild populations, phenotypes in lab stocks, or disease-related traits in human medicine. Here we advance microarray-based genotyping for population genomics with Restriction Site Tiling Analysis. The approach simultaneously discovers polymorphisms and provides quantitative genotype data at 10,000s of loci. It is highly accurate and free from ascertainment bias. We apply the approach to uncover genomic differentiation in the purple sea urchin.
View details for DOI 10.1186/gb-2010-11-4-r44
View details for Web of Science ID 000279625000015
View details for PubMedID 20403197
View details for PubMedCentralID PMC2884547
Whole-Genome Positive Selection and Habitat-Driven Evolution in a Shallow and a Deep-Sea Urchin
GENOME BIOLOGY AND EVOLUTION
2010; 2: 800-814
Comparisons of genomic sequence between divergent species can provide insight into the action of natural selection across many distinct classes of proteins. Here, we examine the extent of positive selection as a function of tissue-specific and stage-specific gene expression in two closely-related sea urchins, the shallow-water Strongylocentrotus purpuratus and the deep-sea Allocentrotus fragilis, which have diverged greatly in their adult but not larval habitats. Genes that are expressed specifically in adult somatic tissue have significantly higher dN/dS ratios than the genome-wide average, whereas those in larvae are indistinguishable from the genome-wide average. Testis-specific genes have the highest dN/dS values, whereas ovary-specific have the lowest. Branch-site models involving the outgroup S. franciscanus indicate greater selection (ω(FG)) along the A. fragilis branch than along the S. purpuratus branch. The A. fragilis branch also shows a higher proportion of genes under positive selection, including those involved in skeletal development, endocytosis, and sulfur metabolism. Both lineages are approximately equal in enrichment for positive selection of genes involved in immunity, development, and cell-cell communication. The branch-site models further suggest that adult-specific genes have experienced greater positive selection than those expressed in larvae and that ovary-specific genes are more conserved (i.e., experienced greater negative selection) than those expressed specifically in adult somatic tissues and testis. Our results chart the patterns of protein change that have occurred after habitat divergence in these two species and show that the developmental or functional context in which a gene acts can play an important role in how divergent species adapt to new environments.
View details for DOI 10.1093/gbe/evq063
View details for Web of Science ID 000291467300022
View details for PubMedID 20935062
View details for PubMedCentralID PMC2975446
Are Antarctic minke whales unusually abundant because of 20th century whaling?
2010; 19 (2): 281-291
Severe declines in megafauna worldwide illuminate the role of top predators in ecosystem structure. In the Antarctic, the Krill Surplus Hypothesis posits that the killing of more than 2 million large whales led to competitive release for smaller krill-eating species like the Antarctic minke whale. If true, the current size of the Antarctic minke whale population may be unusually high as an indirect result of whaling. Here, we estimate the long-term population size of the Antarctic minke whale prior to whaling by sequencing 11 nuclear genetic markers from 52 modern samples purchased in Japanese meat markets. We use coalescent simulations to explore the potential influence of population substructure and find that even though our samples are drawn from a limited geographic area, our estimate reflects ocean-wide genetic diversity. Using Bayesian estimates of the mutation rate and coalescent-based analyses of genetic diversity across loci, we calculate the long-term population size of the Antarctic minke whale to be 670,000 individuals (95% confidence interval: 374,000-1,150,000). Our estimate of long-term abundance is similar to, or greater than, contemporary abundance estimates, suggesting that managing Antarctic ecosystems under the assumption that Antarctic minke whales are unusually abundant is not warranted.
View details for DOI 10.1111/j.1365-294X.2009.04447.x
View details for Web of Science ID 000273550100007
View details for PubMedID 20025655
Big and Slow: Phylogenetic Estimates of Molecular Evolution in Baleen Whales (Suborder Mysticeti)
MOLECULAR BIOLOGY AND EVOLUTION
2009; 26 (11): 2427-2440
Baleen whales are the largest animals that have ever lived. To develop an improved estimation of substitution rate for nuclear and mitochondrial DNA for this taxon, we implemented a relaxed-clock phylogenetic approach using three fossil calibration dates: the divergence between odontocetes and mysticetes approximately 34 million years ago (Ma), between the balaenids and balaenopterids approximately 28 Ma, and the time to most recent common ancestor within the Balaenopteridae approximately 12 Ma. We examined seven mitochondrial genomes, a large number of mitochondrial control region sequences (219 haplotypes for 465 bp) and nine nuclear introns representing five species of whales, within which multiple species-specific alleles were sequenced to account for within-species diversity (1-15 for each locus). The total data set represents >1.65 Mbp of mitogenome and nuclear genomic sequence. The estimated substitution rate for the humpback whale control region (3.9%/million years, My) was higher than previous estimates for baleen whales but slow relative to other mammal species with similar generation times (e.g., human-chimp mean rate > 20%/My). The mitogenomic third codon position rate was also slow relative to other mammals (mean estimate 1%/My compared with a mammalian average of 9.8%/My for the cytochrome b gene). The mean nuclear genomic substitution rate (0.05%/My) was substantially slower than average synonymous estimates for other mammals (0.21-0.37%/My across a range of studies). The nuclear and mitogenome rate estimates for baleen whales were thus roughly consistent with an 8- to 10-fold slowing due to a combination of large body size and long generation times. Surprisingly, despite the large data set of nuclear intron sequences, there was only weak and conflicting support for alternate hypotheses about the phylogeny of balaenopterid whales, suggesting that interspecies introgressions or a rapid radiation has obscured species relationships in the nuclear genome.
View details for DOI 10.1093/molbev/msp169
View details for Web of Science ID 000271422300003
View details for PubMedID 19648466
Rebuilding Global Fisheries
2009; 325 (5940): 578-585
After a long history of overexploitation, increasing efforts to restore marine ecosystems and rebuild fisheries are under way. Here, we analyze current trends from a fisheries and conservation perspective. In 5 of 10 well-studied ecosystems, the average exploitation rate has recently declined and is now at or below the rate predicted to achieve maximum sustainable yield for seven systems. Yet 63% of assessed fish stocks worldwide still require rebuilding, and even lower exploitation rates are needed to reverse the collapse of vulnerable species. Combined fisheries and conservation objectives can be achieved by merging diverse management actions, including catch restrictions, gear modification, and closed areas, depending on local context. Impacts of international fleets and the lack of alternatives to fishing complicate prospects for rebuilding fisheries in many poorer regions, highlighting the need for a global perspective on rebuilding marine resources.
View details for DOI 10.1126/science.1173146
View details for Web of Science ID 000268493000042
View details for PubMedID 19644114
- Managing for ocean biodiversity to sustain marine ecosystem services FRONTIERS IN ECOLOGY AND THE ENVIRONMENT 2009; 7 (4): 204-211
Comparing Evolutionary Patterns and Variability in the Mitochondrial Control Region and Cytochrome b in Three Species of Baleen Whales
JOURNAL OF MOLECULAR EVOLUTION
2009; 68 (1): 97-111
The rapidly evolving mitochondrial control region remains an important source of information on phylogeography and demographic history for cetaceans and other vertebrates, despite great uncertainty in the rate of nucleotide substitution across both nucleotide positions and lineages. Patterns of variation in linked markers with slower rates of evolution can potentially be used to calibrate the rate of nucleotide substitution in the control region and to better understand the interplay of evolutionary and demographic forces across the mitochondrial genome above and below the species level. We have examined patterns of diversity within and between three baleen whale species (gray, humpback, and Antarctic minke whales) in order to determine how patterns of molecular evolution differ between cytochrome b and the control region. Our results show that cytochrome b is less variable than expected given the diversity in the control region for gray and humpback whales, even after functional differences are taken into account, but more variable than expected for minke whales. Differences in the frequency distributions of polymorphic sites and in best-fit models of nucleotide substitution indicate that these patterns may be the result of hypervariability in the control region in gray and humpback whales but, in minke whales, may result from a large, stable or expanding population size coupled with saturation at the control region. Using paired cytochrome b and control region data across individuals, we show that the average rate of nucleotide substitution in the control region may be on average 2.6 times higher than phylogenetically derived estimates in cetaceans. These results highlight the complexity of making inferences from control region data alone and suggest that applying simple rules of DNA sequence analyses across species may be difficult.
View details for DOI 10.1007/s00239-008-9193-2
View details for Web of Science ID 000263147100009
View details for PubMedID 19116685
General-use polymerase chain reaction primers for amplification and direct sequencing of enolase, a single-copy nuclear gene, from different animal phyla
MOLECULAR ECOLOGY RESOURCES
2009; 9 (1): 144-147
In contrast to mitochondrial DNA, remarkably few general-use primer sets are available for single-copy nuclear genes across animal phyla. Here, we present a primer set that yields a c. 364-bp coding fragment of the metabolic gene enolase, which includes an intron in some taxa. In species where introns are absent or have few insertions/deletions, the amplified fragment can be sequenced directly for phylogenetic or population analysis. Between-species variation in the coding region occurs widely at third codon positions, even between closely related taxa, making the fragment useful for species-level systematics. In low gene-flow species, the primers may also be of use for population genetics, as intraspecific polymorphisms occur at several silent positions in the taxa examined.
View details for DOI 10.1111/j.1755-0998.2008.02210.x
View details for Web of Science ID 000262678900026
View details for PubMedID 21564585
Speciation and the evolution of gamete recognition genes: pattern and process
2009; 102 (1): 66-76
Proteins on gamete surfaces are major determinants of fertilization success, particularly in free-spawning animals. Molecular analyses of these simple genetic systems show rapid evolution, positive selection, accelerated coalescence and, sometimes, extensive polymorphism. Careful analysis of the behavior of sperm produced by males with different gamete alleles shows that these alleles can deliver significant functional differences. Three forms of allele-specific fertilization advantage have been shown: assortative mating based on gamete type, rare allele advantage and heterozygote superiority. Models suggest that sperm and egg proteins may be coevolutionary partners that can alternate between directional selection for high fertilization ability and cyclic adaptation of eggs and sperm driven by sexual conflict. These processes act within allopatric populations and may accelerate their divergence if gamete adaptations in separate demes reduce cross-fertilization. Reproductive character displacement by reinforcement may play a diversifying role when previously allopatric populations rejoin. In circumstance that might prove to be common, divergence in sympatry can be driven by sexual conflict or by association of mating types with ecological differences. The ecology of fertilization, especially the degree of sperm competition and egg death via polyspermy, are important determinants of the strength and direction of selection on gametes. Free-spawning animals allow careful analysis of gamete recognition -from the behavior of adults and interactions of gametes, to molecular patterns of allele divergence. Future research efforts on the evolutionary consequences of fertilization ecology, and the interaction between extensive variation in egg surface proteins and sperm fertilization ability, are particularly needed.
View details for DOI 10.1038/hdy.2008.104
View details for Web of Science ID 000261774400010
View details for PubMedID 19018273
Mitochondrial and Nuclear Genetic Variation across Calving Lagoons in Eastern North Pacific Gray Whales (Eschrichtius robustus)
JOURNAL OF HEREDITY
2009; 100 (1): 34-46
Accurate knowledge of population structure in cetaceans is critical for preserving and managing breeding habitat, particularly when habitat is not uniformly protected. Most eastern gray whales return to their major breeding range each winter along the Pacific coast of Baja California, Mexico, concentrating in 3 major calving lagoons, but it is unknown whether genetic differences exist between lagoons. Previous photo-identification studies and genetic studies suggest that gray whales may return to their natal lagoons to breed, potentially resulting in the buildup of genetic differences. However, an earlier genetic study used only one genetic marker and did not include samples from Bahia Magdalena, a major calving lagoon not currently designated as a wildlife refuge. To expand on this previous study, we collected genetic data from the mitochondrial control region (442 bp) and 9 microsatellite markers from 112 individuals across all 3 major calving lagoons. Our data suggest that migration rates between calving lagoons are high but that a small but significant departure from panmixia exists between Bahia Magdalena and Laguna San Ignacio (Fisher's Exact test, P < 0.0001; F(ST) = 0.006, P = 0.025). Coalescent simulations show that the lack of extensive population structure may result from the disruption of structure due to whaling. Another possibility is that rates of migration have always been high (>10% per generation). In addition, microsatellite data showed evidence of a severe population bottleneck. Eastern gray whales are still recovering from the impacts of whaling on their breeding grounds, and these populations should be protected and monitored for future genetic changes.
View details for DOI 10.1093/jhered/esn090
View details for Web of Science ID 000261901400005
View details for PubMedID 18974400
- Distributions of stress-resistant coral symbionts match environmental patterns at local but not regional scales MARINE ECOLOGY PROGRESS SERIES 2009; 378: 93-103
Better Evolution Through Chemistry: Rapid Evolution Driven by Human Changes to the Chemical Environment
Symposium on Chemical Evolution II held at the 235th ACS National Meeting
AMER CHEMICAL SOC. 2009: 333–343
View details for Web of Science ID 000280805500017
Intraspecific divergence in sperm morphology of the green sea urchin, Strongylocentrotus droebachiensis: implications for selection in broadcast spawners
BMC EVOLUTIONARY BIOLOGY
Sperm morphology can be highly variable among species, but less is known about patterns of population differentiation within species. Most studies of sperm morphometric variation are done in species with internal fertilization, where sexual selection can be mediated by complex mating behavior and the environment of the female reproductive tract. Far less is known about patterns of sperm evolution in broadcast spawners, where reproductive dynamics are largely carried out at the gametic level. We investigated variation in sperm morphology of a broadcast spawner, the green sea urchin (Strongylocentrotus droebachiensis), within and among spawnings of an individual, among individuals within a population, and among populations. We also examined population-level variation between two reproductive seasons for one population. We then compared among-population quantitative genetic divergence (QST) for sperm characters to divergence at neutral microsatellite markers (FST).All sperm traits except total length showed strong patterns of high diversity among populations, as did overall sperm morphology quantified using multivariate analysis. We also found significant differences in almost all traits among individuals in all populations. Head length, axoneme length, and total length had high within-male repeatability across multiple spawnings. Only sperm head width had significant within-population variation across two reproductive seasons. We found signatures of directional selection on head length and head width, with strong selection possibly acting on head length between the Pacific and West Atlantic populations. We also discuss the strengths and limitations of the QST-FST comparison.Sperm morphology in S. droebachiensis is highly variable, both among populations and among individuals within populations, and has low variation within an individual across multiple spawnings. Selective pressures acting among populations may differ from those acting within, with directional selection implicated in driving divergence among populations and balancing selection as a possible mechanism for producing variability among males. Sexual selection in broadcast spawners may be mediated by different processes from those acting on internal fertilizers. Selective divergence in sperm head length among populations is associated with ecological differences among populations that may play a large role in mediating sexual selection in this broadcast spawner.
View details for DOI 10.1186/1471-2148-8-283
View details for Web of Science ID 000262179700001
View details for PubMedID 18851755
View details for PubMedCentralID PMC2613923
- An impediment to consumer choice: Overfished species are sold as Pacific red snapper BIOLOGICAL CONSERVATION 2008; 141 (6): 1591-1599
- The tip of the tail: molecular identification of seahorses for sale in apothecary shops and curio stores in California CONSERVATION GENETICS 2008; 9 (1): 65-71
- Sources of invasions of a northeastern Pacific acorn barnacle, Balanus glandula, in Japan and Argentina MARINE ECOLOGY PROGRESS SERIES 2008; 358: 211-218
- Ecosystems in action: Lessons from marine ecology about recovery, resistance, and reversibility BIOSCIENCE 2008; 58 (1): 33-42
DNA evidence for historic population size and past ecosystem impacts of gray whales
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
2007; 104 (38): 15162-15167
Ecosystem restoration may require returning threatened populations of ecologically pivotal species to near their former abundances, but it is often difficult to estimate historic population size of species that have been heavily exploited. Eastern Pacific gray whales play a key ecological role in their Arctic feeding grounds and are widely thought to have returned to their prewhaling abundance. Recent mortality spikes might signal that the population has reached long-term carrying capacity, but an alternative is that this decline was due to shifting climatic conditions on Arctic feeding grounds. We used a genetic approach to estimate prewhaling abundance of gray whales and report DNA variability at 10 loci that is typical of a population of approximately 76,000-118,000 individuals, approximately three to five times more numerous than today's average census size of 22,000. Coalescent simulations indicate these estimates may include the entire Pacific metapopulation, suggesting that our average measurement of approximately 96,000 individuals was probably distributed between the eastern and currently endangered western Pacific populations. These levels of genetic variation suggest the eastern population is at most at 28-56% of its historical abundance and should be considered depleted. If used to inform management, this would halve acceptable human-caused mortality for this population from 417 to 208 per year. Potentially profound ecosystem impacts may have resulted from a decline from 96,000 gray whales to the current population. At previous levels, gray whales may have seasonally resuspended 700 million cubic meters of sediment, as much as 12 Yukon Rivers, and provided food to a million sea birds.
View details for DOI 10.1073/pnas.0706056104
View details for Web of Science ID 000249715100052
View details for PubMedID 17848511
View details for PubMedCentralID PMC1975855
- Response to comments on "Impacts of biodiversity loss on ocean ecosystem services" SCIENCE 2007; 316 (5829): 1285-1286
- Economic ecology - In the market for minke whales NATURE 2007; 447 (7142): 267-?
Restricted gene flow in the Caribbean staghorn coral Acropora cervicomis: Implications for the recovery of endangered reefs
JOURNAL OF HEREDITY
2007; 98 (1): 40-50
Coral reef conservation requires information about the distance over which healthy reefs can rescue damaged reefs through input of coral larvae. This information is desperately needed in the Caribbean where the 2 dominant shallow water corals Acropora cervicornis and Acropora palmata have suffered unprecedented declines. Here we compare the population genetic structure in the staghorn coral A. cervicornis across the greater Caribbean using DNA sequence data from 1 mitochondrial and 3 nuclear genes. Data from 160 individuals from 22 populations and 9 regions show that A. cervicornis exhibits significant population genetic structure across the greater Caribbean in both the mitochondrial (Phi(st) = 0.130) and nuclear data (Phi(st) = 0.067). The highest population structure was observed in the species' own, native mtDNA haplotypes (Phi(st) = 0.235). Introgressed alleles from A. palmata tempered higher population structure in A. cervicornis over regional scales but in some cases generated highly localized "introgression hot spots" and fine-scale genetic structure among reefs separated by as few as 2 km. These data show that larval dispersal over moderate or long distances (>500 km) is limited for this threatened species and in some cases locally limited as well. Thus, the endangered Caribbean staghorn corals require local source populations for their recovery and targeted conservation efforts over spatial scales much smaller than the hundreds to thousands of kilometers usually proposed for marine reserves.
View details for DOI 10.1093/jhered/esl057
View details for Web of Science ID 000243585900005
View details for PubMedID 17158464
Impacts of biodiversity loss on ocean ecosystem services
2006; 314 (5800): 787-790
Human-dominated marine ecosystems are experiencing accelerating loss of populations and species, with largely unknown consequences. We analyzed local experiments, long-term regional time series, and global fisheries data to test how biodiversity loss affects marine ecosystem services across temporal and spatial scales. Overall, rates of resource collapse increased and recovery potential, stability, and water quality decreased exponentially with declining diversity. Restoration of biodiversity, in contrast, increased productivity fourfold and decreased variability by 21%, on average. We conclude that marine biodiversity loss is increasingly impairing the ocean's capacity to provide food, maintain water quality, and recover from perturbations. Yet available data suggest that at this point, these trends are still reversible.
View details for DOI 10.1126/science.1132294
View details for Web of Science ID 000241729800037
View details for PubMedID 17082450
Comparative phylogeography of three codistributed stomatopods: Origins and timing of regional lineage diversification in the coral triangle
2006; 60 (9): 1825-1839
The Indonesian-Australian Archipelago is the center of the world's marine biodiversity. Although many biogeographers have suggested that this region is a "center of origin," criticism of this theory has focused on the absence of processes promoting lineage diversification in the center. In this study we compare patterns of phylogeographic structure and gene flow in three codistributed, ecologically similar Indo-West Pacific stomatopod (mantis shrimp) species. All three taxa show evidence for limited gene flow across the Maluku Sea with deep genetic breaks between populations from Papua and Northern Indonesia, suggesting that limited water transport across the Maluku Sea may limit larval dispersal and gene flow across this region. All three taxa also show moderate to strong genetic structure between populations from Northern and Southern Indonesia, indicating limited gene flow across the Flores and Java Seas. Despite the similarities in phylogeographic structure, results indicate varied ages of the genetic discontinuities, ranging from the middle Pleistocene to the Pliocene. Concordance of genetic structure across multiple taxa combined with temporal discordance suggests that regional genetic structures have arisen from the action of common physical processes operating over extended time periods. The presence in all three species of both intraspecific genetic structure as well as deeply divergent lineages that likely represent cryptic species suggests that these processes may promote lineage diversification within the Indonesian-Australian Archipelago, providing a potential mechanism for the center of origin. Efforts to conserve biodiversity in the Coral Triangle should work to preserve both existing biodiversity as well as the processes creating the biodiversity.
View details for Web of Science ID 000241226800008
View details for PubMedID 17089967
Seascape genetics: A coupled oceanographic-genetic model predicts population structure of Caribbean corals
2006; 16 (16): 1622-1626
Population genetics is a powerful tool for measuring important larval connections between marine populations [1-4]. Similarly, oceanographic models based on environmental data can simulate particle movements in ocean currents and make quantitative estimates of larval connections between populations possible [5-9]. However, these two powerful approaches have remained disconnected because no general models currently provide a means of directly comparing dispersal predictions with empirical genetic data (except, see ). In addition, previous genetic models have considered relatively simple dispersal scenarios that are often unrealistic for marine larvae [11-15], and recent landscape genetic models have yet to be applied in a marine context [16-20]. We have developed a genetic model that uses connectivity estimates from oceanographic models to predict genetic patterns resulting from larval dispersal in a Caribbean coral. We then compare the predictions to empirical data for threatened staghorn corals. Our coupled oceanographic-genetic model predicts many of the patterns observed in this and other empirical datasets; such patterns include the isolation of the Bahamas and an east-west divergence near Puerto Rico [3, 21-23]. This new approach provides both a valuable tool for predicting genetic structure in marine populations and a means of explicitly testing these predictions with empirical data.
View details for DOI 10.1016/j.cub.2006.06.052
View details for Web of Science ID 000240155400025
View details for PubMedID 16920623
The use of genetic clines to estimate dispersal distances of marine larvae
2006; 87 (5): 1094-1103
Many unresolved issues in the ecology and evolution of marine populations center on how far planktonic larvae disperse away from their parents. Genetic tools provide a promising way to define the spatial spread of larvae, yet their accurate interpretation depends on the extent to which genetic loci are under selection. Genetic clines, geographic zones in which genetically differentiated populations interbreed, provide opportunities to explicitly and simultaneously quantify the relative roles of selection and dispersal. Here, we review the theory and analysis of genetic clines and apply these techniques to published studies of multilocus clines in the sea. The geographic width of a stable genetic cline is determined by a balance between the homogenizing effects of dispersal and the diversifying effects of selection. For marine researchers, the power of genetic clines is that, if selection and clinal width are quantified, then the average geographic distances that larvae move can be inferred. Measuring selection or dispersal through laboratory or field-based experimentation is possible, though logistically difficult, for pelagically dispersed organisms. Instead, dispersal may be more robustly quantified from the degree of linkage disequilibrium between two or more loci, because linkage disequilibrium integrates selection across multiple life stages and generations. It is also relatively insensitive to whether exogenous or endogenous selection operates. Even without quantifying linkage disequilibrium, the theory of genetic clines indicates that the average dispersal distance of larvae is a fraction (i.e., generally <35%) of the clinal width. Because cline theory is based on several underlying assumptions, including near-equilibrium between selection and migration, the dispersal distances inferred from empirical data should be of the correct order but may not be precise. Even so, such estimates of larval dispersal are valuable, as they can be utilized to design appropriate scales for future investigations and provide some guidance to conservation efforts.
View details for Web of Science ID 000237552400003
View details for PubMedID 16761586
Coral gardens: Paternity and drug testing on the reef
2005; 15 (14): R544-R545
An international team has used molecular genetics and chemical tagging to trace how baby clownfish travel from their mother's nest through the ocean to the anemone they will live on. More than one out of five juveniles came from nests that were only meters away, despite spending over a week drifting in ocean currents. Such surprising fidelity to a small area of the coral reef bodes well for efforts to preserve coral reef diversity with reserves.
View details for Web of Science ID 000230903900011
View details for PubMedID 16051159
Evolutionary animation: How do molecular phylogenies compare to Mayr"s reconstruction of speciation patterns in the sea?
Colloquium on Systematics and the Origin of Species
NATL ACAD SCIENCES. 2005: 6566–6572
Ernst Mayr used the geography of closely related species in various stages of increasing divergence to "animate" the process of geographic, or allopatric, speciation. This approach was applied to a wide set of taxa, and a seminal paper by Mayr used it to explore speciation patterns in tropical sea urchins. Since then, taxonomic information in several of these genera has been augmented by detailed molecular phylogenies. We compare Mayr's animation with the phylogenies of eight sea urchin genera placed by Mayr into four speciation groups. True to Mayr's predictions, early-stage genera have on average lower species divergence and more polytypic species than genera in later stages. For six of these genera, we also have information about the evolution of the gamete recognition protein bindin, which is critical to reproductive isolation. These comparisons show that later-stage genera with many sympatric species tend to be those with rapid bindin evolution. By contrast, early-stage genera with few sympatric species are not necessarily earlier in the divergence process; they happen to be those with slow rates of bindin evolution. These results show that the rate of speciation in sea urchins does not only depend on the steady accumulation of genome divergence over time, but also on the rate of evolution of gamete recognition proteins. The animation method used by Mayr is generally supported by molecular phylogenies. However, the existence of multiple rates in the acquisition of reproductive isolation complicates placement of different genera in an evolutionary series.
View details for Web of Science ID 000229023700009
View details for PubMedID 15851681
View details for PubMedCentralID PMC1131860
- Environmental science - Germ theory for ailing corals NATURE 2005; 434 (7034): 713-715
Ecological science and sustainability for the 21st century
FRONTIERS IN ECOLOGY AND THE ENVIRONMENT
2005; 3 (1): 4-11
View details for Web of Science ID 000226955300002
Conspecific sperm precedence in two species of tropical sea urchins
2005; 59 (1): 97-105
Conspecific sperm precedence occurs when females are exposed to sperm from males of multiple species, but preferentially use sperm of a conspecific. Conspecific sperm precedence and its mechanisms have been documented widely in terrestrial species, in which complex female behaviors or reproductive tract morphologies can allow many opportunities for female choice and sperm competition, however, the opportunity for conspecific sperm precedence in free spawning marine invertebrates has been largely ignored. Two sea urchin species, Echinometra oblonga and E. sp. C, have high levels of interspecific fertilization in no-choice lab crosses, but no natural hybrids have been found. We performed competitive fertilization assays to test for conspecific sperm precedence and found that eggs of both species showed a marked preference for conspecific sperm when fertilized with heterospecific sperm mixtures. Strong rejection of heterospecific sperm would not have been predicted from no-choice assays and helps explain the lack of natural hybrids. We also found significant variation in hybridization success among crosses. Conspecific sperm precedence in free spawning invertebrates shows that the simple surfaces of eggs and sperm provide ample opportunity for egg choice and sperm competition even in the absence of intricate behavior or complex reproductive morphologies.
View details for Web of Science ID 000226737900009
View details for PubMedID 15792230
Testing the utility of internally transcribed spacer sequences in coral phylogenetics
2004; 13 (9): 2763-2772
Reef-building corals often possess high levels of intraindividual and intraspecific ribosomal DNA (rDNA) variation that is largely polyphyletic between closely related species. Polyphyletic rDNA phylogenies coupled with high intraindividual rDNA variation have been taken as evidence of introgressive hybridization in corals. Interpreting the data is problematic because the rDNA cluster evolves in a complex fashion and polyphyletic lineages can be generated by a variety of processes--such as incomplete lineage sorting and slow concerted evolution--in addition to hybridization. Using the genetically characterized Caribbean Acropora hybridization system, we evaluate how well rDNA data perform in revealing patterns of recent introgressive hybridization in contrast to genetic data from four single-copy loci. While the rDNA data are broadly consistent with the unidirectional introgression seen in other loci, we show that the phylogenetic signature of recent introgressive hybridization is obscured in the Caribbean Acropora by ancient shared rDNA lineages that predate the divergence of the species.
View details for DOI 10.1111/j.1365-294X.2004.02265.x
View details for Web of Science ID 000223291200022
View details for PubMedID 15315687
- Fisheries science - Why mothers matter NATURE 2004; 430 (7000): 621-622
Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula
2004; 13 (8): 2143-2156
A long-standing issue in marine biology is identifying spatial scales at which populations of sessile adults are connected by planktonic offspring. We examined the genetic continuity of the acorn barnacle Balanus glandula, an abundant member of rocky intertidal communities of the northeastern Pacific Ocean, and compared these genetic patterns to the nearshore oceanography described by trajectories of surface drifters. Consistent with its broad dispersal potential, barnacle populations are genetically similar at both mitochondrial (cytochrome oxidase I) and nuclear (elongation factor 1-alpha) loci across broad swaths of the species' range. In central California, however, there is a striking genetic cline across 475 km of coastline between northern and southern populations. These patterns indicate that gene flow within central California is far more restricted spatially than among other populations. Possible reasons for the steep cline include the slow secondary introgression of historically separated populations, a balance between diversifying selection and dispersal, or some mix of both. Geographic trajectories of oceanic drifters closely parallel geographical patterns of gene flow. Drifters placed to the north (Oregon; approximately 44 degrees N) and south (Santa Barbara, California; approximately 34 degrees N) of the cline disperse hundreds of kilometers within 40 days, yet over the long-term their trajectories never overlapped. The lack of communication between waters originating in Oregon and southern California probably helps to maintain strong genetic differentiation between these regions. More broadly, the geographical variation in gene flow implies that focusing on species-level averages of gene flow can mask biologically important variance within species which reflects local environmental conditions and historical events.
View details for DOI 10.1111/j.1365-294X.2004.02225.x
View details for Web of Science ID 000222521300004
View details for PubMedID 15245390
Gene expression and feeding ecology: evolution of piscivory in the venomous gastropod genus Conus
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES
2004; 271 (1544): 1165-1174
Differential expression of gene-family members is typically associated with the specific development of certain tissues and organs, but its importance in the ecological adaptation of organisms has rarely been investigated. Several specialized feeding modes have evolved within the predatory marine gastropod genus Conus, including molluscivory and piscivory. Based on phylogenetic investigations of Conus species, it has been concluded that piscivory arose at least twice in this genus. Moreover, molecular analyses of conotoxin mRNA transcripts reveal that piscivores from independent evolutionary lineages express the same subset of four-loop conotoxins, contrary to phylogenetic expectations. These results demonstrate that differential expression of gene-family members can play a key role in adaptive evolution, particularly during shifts to new ecological niches.
View details for DOI 10.1098/rspb.2004.2708
View details for Web of Science ID 000223994100010
View details for PubMedID 15306367
- Ecology for a crowded planet SCIENCE 2004; 304 (5675): 1251-1252
Marine reserves and ocean neighborhoods: The spatial scale of marine populations and their management
ANNUAL REVIEW OF ENVIRONMENT AND RESOURCES
2004; 29: 31-68
View details for Web of Science ID 000225744400003
Marine reserves: the best option for our oceans?
FRONTIERS IN ECOLOGY AND THE ENVIRONMENT
2003; 1 (9): 495-502
View details for Web of Science ID 000221791600017
- Ecological subsidies alter the structure of marine communities PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 2003; 100 (21): 11927-11928
Recent speciation in the Indo-West Pacific: rapid evolution of gamete recognition and sperm morphology in cryptic species of sea urchin
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES
2003; 270 (1526): 1839-1847
The rich species diversity of the marine Indo-West Pacific (IWP) has been explained largely on the basis of historical observation of large-scale diversity gradients. Careful study of divergence among closely related species can reveal important new information about the pace and mechanisms of their formation, and can illuminate the genesis of biogeographic patterns. Young species inhabiting the IWP include urchins of the genus Echinometra, which diverged over the past 1-5 Myr. Here, we report the most recent divergence of two cryptic species of Echinometra inhabiting this region. Mitochondrial cytochrome oxidase 1 (CO1) sequence data show that in Echinometra oblonga, species-level divergence in sperm morphology, gamete recognition proteins and gamete compatibility arose between central and western Pacific populations in the past 250 000 years. Divergence in sperm attachment proteins suggests rapid evolution of the fertilization system. Divergence of sperm morphology may be a common feature of free-spawning animals, and offers opportunities to simultaneously understand genetic divergence, changes in protein expression patterns and morphological evolution in traits directly related to reproductive isolation.
View details for DOI 10.1098/rspb.2003.2395
View details for Web of Science ID 000185206500012
View details for PubMedID 12964987
Climate change, human impacts, and the resilience of coral reefs
2003; 301 (5635): 929-933
The diversity, frequency, and scale of human impacts on coral reefs are increasing to the extent that reefs are threatened globally. Projected increases in carbon dioxide and temperature over the next 50 years exceed the conditions under which coral reefs have flourished over the past half-million years. However, reefs will change rather than disappear entirely, with some species already showing far greater tolerance to climate change and coral bleaching than others. International integration of management strategies that support reef resilience need to be vigorously implemented, and complemented by strong policy decisions to reduce the rate of global warming.
View details for Web of Science ID 000184755900027
View details for PubMedID 12920289
Genome size evolution in pufferfish: A comparative analysis of diodontid and tetraodontid pufferfish genomes
2003; 13 (5): 821-830
Smooth pufferfish of the family Tetraodontidae have the smallest vertebrate genomes yet measured. They have a haploid genome size of approximately 400 million bp (Mb), which is almost eight times smaller than the human genome. Given that spiny pufferfish from the sister family Diodontidae and a fish from the outgroup Molidae have genomes twice as large as smooth puffers, it appears that the genome size of smooth puffers has contracted in the last 50-70 million years since their divergence from the spiny puffers. Here we use renaturation kinetics to compare the repetitive nature of the smooth and spiny puffer genomes. We also estimate the rates of small (<400 bp) insertions and deletions in smooth and spiny puffers using defunct non-LTR retrotransposons. We find a significantly greater abundance of a transposon-like repetitive DNA class in spiny puffers relative to smooth puffers, in addition to nearly identical indel rates. We comment on the role that large insertions may play in the evolution of genome size in these two groups.
View details for DOI 10.1101/gr.841703
View details for Web of Science ID 000182645500008
View details for PubMedID 12727902
Reproductive character displacement and the genetics of gamete recognition in tropical sea urchins
2003; 57 (5): 1049-1060
Reproductive character displacement occurs when sympatric and allopatric populations of a species differ in traits crucial to reproduction, and it is commonly thought of as a signal of selection acting to limit hybridization. Most documented cases of reproductive character displacement involve characters that are poorly understood at the genetic level, and rejecting alternative hypotheses for biogeographic shifts in reproductive traits is often very difficult. In sea urchins, the gamete recognition protein bindin evolves under positive selection when species are broadly sympatric, suggesting character displacement may be operating in this system. We sampled sympatric and allopatric populations of two species in the sea urchin genus Echinometra for variation in bindin and for the mitochondrial cytochrome oxidase I to examine patterns of population differentiation and molecular evolution at a reproductive gene. We found a major shift in bindin alleles between central Pacific (allopatric) and western Pacific (sympatric) populations of E. oblonga. Allopatric populations of E. oblonga are polyphyletic with E. sp. C at bindin, whereas sympatric populations of the two species are reciprocally monophyletic. There is a strong signal of positive selection (P(N)/P(S) = 4.5) in the variable region of the first exon of bindin, which is associated with alleles found in sympatric populations of E. oblonga. These results indicate that there is a strong pattern of reproductive character displacement between E. oblonga and E. sp. C and that the divergence is driven by selection. There is much higher population structure in sympatric populations at the bindin locus than at the neutral mitochondrial locus, but this difference is not seen in allopatric populations. These data suggest a pattern of speciation driven by selection for local gamete coevolution as a result of interactions between sympatric species. Although this pattern is highly suggestive of speciation by reinforcement, further research into hybrid fitness and egg-sperm interactions is required to address this potential mechanism for character displacement.
View details for Web of Science ID 000183500900010
View details for PubMedID 12836822
New wave: high-tech tools to help marine reserve research
FRONTIERS IN ECOLOGY AND THE ENVIRONMENT
2003; 1 (2): 73-79
View details for Web of Science ID 000221789500013
Population genetics, demographic connectivity, and the design of marine reserves
2003; 13 (1): S146-S158
View details for Web of Science ID 000181742700012
Population models for marine reserve design: A retrospective and prospective synthesis
2003; 13 (1): S47-S64
View details for Web of Science ID 000181742700005
- Why gobies are like hobbits SCIENCE 2003; 299 (5603): 51-52
Rapid recovery of genetic populations on Krakatau: diversity of stomatopod temporal and spatial scales of marine larval dispersal
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES
2002; 269 (1500): 1591-1597
Although the recovery of terrestrial communities shattered by the massive eruption of Krakatau in 1883 has been well chronicled, the fate of marine populations has been largely ignored. We examined patterns of genetic diversity in populations of two coral reef-dwelling mantis shrimp, Haptosquilla pulchella and Haptosquilla glyptocercus (Stomatopoda: Protosquillidae), on the islands of Anak Krakatau and Rakata. Genetic surveys of mitochondrial cytochrome oxidase c (subunit 1) in these populations revealed remarkably high levels of haplotypic and nucleotide diversity that were comparable with undisturbed populations throughout the Indo-Pacific. Recolonization and rapid recovery of genetic diversity in the Krakatau populations indicates that larval dispersal from multiple and diverse source populations contributes substantially to the demographics of local populations over intermediate temporal (tens to hundreds of years) and spatial scales (tens to hundreds of kilometres). Natural experiments such as Krakatau provide an excellent mechanism to investigate marine larval dispersal and connectivity. Results from stomatopods indicate that marine reserves should be spaced no more than 50-100 km apart to facilitate ecological connectivity via larval dispersal.
View details for DOI 10.1098/rspb.2002.2026
View details for Web of Science ID 000177508300010
View details for PubMedID 12184829
View details for PubMedCentralID PMC1691063
Hybridization and the evolution of reef coral diversity
2002; 296 (5575): 2023-2025
Hundreds of coral species coexist sympatrically on reefs, reproducing in mass-spawning events where hybridization appears common. In the Caribbean, DNA sequence data from all three sympatric Acropora corals show that mass spawning does not erode species barriers. Species A. cervicornis and A. palmata are distinct at two nuclear loci or share ancestral alleles. Morphotypes historically given the name Acropora prolifera are entirely F(1) hybrids of these two species, showing morphologies that depend on which species provides the egg for hybridization. Although selection limits the evolutionary potential of hybrids, F(1) individuals can reproduce asexually and form long-lived, potentially immortal hybrids with unique morphologies.
View details for Web of Science ID 000176273300052
View details for PubMedID 12065836
Characterization of microsatellite loci for the Argentine ant, Linepithema humile, and their potential for analysis of colony structure in invading Hawaiian populations
MOLECULAR ECOLOGY NOTES
2002; 2 (2): 94-95
View details for Web of Science ID 000176371900004
Sharp genetic breaks among populations of Haptosquilla pulchella (Stomatopoda) indicate limits to larval transport: patterns, causes, and consequences
2002; 11 (4): 659-674
To help stem the precipitous decline of coral reef ecosystems world-wide, conservation efforts are focused on establishing interconnected reserve networks to protect threatened populations. Because many coral reef organisms have a planktonic or pelagic larval dispersal phase, it is critical to understand the patterns of ecological connectivity between reserve populations that result from larval dispersal. We used genetics to infer dispersal patterns among 24 Indo-West Pacific populations of the mantis shrimp, Haptosquilla pulchella. Contrary to predictions of high dispersal facilitated by the strong currents of the Indonesian throughflow, mitochondrial DNA sequences from 393 individuals displayed striking patterns of regional genetic differentiation concordant with ocean basins isolated during periods of lowered sea level. Patterns of genetic structuring indicate that although dispersal within geographical regions with semicontiguous coastlines spanning thousands of kilometres may be common, ecologically meaningful connections can be rare among populations separated by as little as 300 km of open ocean. Strong genetic mosaics in a species with high dispersal potential highlight the utility of genetics for identifying regional patterns of genetic connectivity between marine populations and show that the assumption that ocean currents will provide ecological connectivity among marine populations must be empirically tested in the design of marine reserve networks.
View details for Web of Science ID 000175250300003
View details for PubMedID 11972755
- Origins of diverse feeding ecologies within Conus, a genus of venomous marine gastropods BIOLOGICAL JOURNAL OF THE LINNEAN SOCIETY 2001; 73 (4): 391-409
Predicting nuclear gene coalescence from mitochondrial data: The three-times rule
2001; 55 (5): 859-868
Coalescence theory predicts when genetic drift at nuclear loci will result in fixation of sequence differences to produce monophyletic gene trees. However, the theory is difficult to apply to particular taxa because it hinges on genetically effective population size, which is generally unknown. Neutral theory also predicts that evolution of monophyly will be four times slower in nuclear than in mitochondrial genes primarily because genetic drift is slower at nuclear loci. Variation in mitochondrial DNA (mtDNA) within and between species has been studied extensively, but can these mtDNA data be used to predict coalescence in nuclear loci? Comparison of neutral theories of coalescence of mitochondrial and nuclear loci suggests a simple rule of thumb. The "three-times rule" states that, on average, most nuclear loci will be monophyletic when the branch length leading to the mtDNA sequences of a species is three times longer than the average mtDNA sequence diversity observed within that species. A test using mitochondrial and nuclear intron data from seven species of whales and dolphins suggests general agreement with predictions of the three-times rule. We define the coalescence ratio as the mitochondrial branch length for a species divided by intraspecific mtDNA diversity. We show that species with high coalescence ratios show nuclear monophyly, whereas species with low ratios have polyphyletic nuclear gene trees. As expected, species with intermediate coalescence ratios show a variety of patterns. Especially at very high or low coalescence ratios, the three-times rule predicts nuclear gene patterns that can help detect the action of selection. The three-times rule may be useful as an empirical benchmark for evaluating evolutionary processes occurring at multiple loci.
View details for DOI 10.1554/0014-3820(2001)055[0859:PNGCFM]2.0.CO;2
View details for Web of Science ID 000169403100002
View details for PubMedID 11430646
Evolutionary diversification of multigene families: Allelic selection of toxins in predatory cone snails
MOLECULAR BIOLOGY AND EVOLUTION
2000; 17 (9): 1286-1293
In order to investigate the evolution of conotoxin multigene families among two closely related vermivorous CONUS: species, we sequenced 104 four-loop conotoxin mRNAs from two individuals of CONUS: ebraeus and compared these with sequences already obtained from CONUS: abbreviatus. In contrast to the diversity of conotoxin sequences obtained from C. abbreviatus, only two common sequence variants were recovered from C. ebraeus. Segregation patterns of the variants in these two individuals and restriction digests of four-loop conotoxin amplification products from nine additional individuals suggest that the common variants are alleles from a single locus. These two putative alleles differ at nine positions that occur nonrandomly in the toxin-coding region of the sequences. Moreover, all substitutions are at nonsynonymous sites and are responsible for seven amino acid differences among the predicted amino acid sequences of the alleles. These results imply that conotoxin diversity is driven by strong diversifying selection and some form of frequency-dependent or overdominant selection at conotoxin loci, and they suggest that diverse conotoxin multigene families can originate from duplications at polymorphic loci. Furthermore, none of the sequences recovered from C. ebraeus appeared to be orthologs of loci from C. abbreviatus, and attempts to amplify orthologous sequences with locus-specific primers were unsuccessful among these species. These patterns suggest that venoms of closely related CONUS: species may differ due to the differential expression of conotoxin loci.
View details for Web of Science ID 000089104100002
View details for PubMedID 10958845
- Biogeography - A marine Wallace's line? NATURE 2000; 406 (6797): 692-693
Predicted decline of protected whales based on molecular genetic monitoring of Japanese and Korean markets
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES
2000; 267 (1449): 1191-1199
We present a two-tiered analysis of molecular genetic variation in order to determine the origins of whale' products purchased from retail markets in Japan and the Republic of (South) Korea during 1993-1999. This approach combined phylogenetic analysis of mitochondrial DNA sequences for identification of protected species with a statistical comparison of intraspecific haplotype frequencies for distinguishing regional subpopulations or 'stocks' hunted for scientific research by the Japanese and killed incidentally in coastal fisheries by the Koreans. The phylogenetic identification of 655 products included eight species or subspecies of baleen whales, sperm whales, a pygmy sperm whale, two species of beaked whales, porpoises, killer whales and numerous species of dolphins as well as domestic sheep and horses. Six of the baleen whale species (the fin, sei, common-form and small-form Bryde's, blue or blue/fin hybrid, and humpback) and the sperm whale are protected by international agreements dating back to at least 1989 for all species and 1966 for some species. We compared the haplotype frequencies from the Japanese market sample to those reported from scientific hunting in the western North Pacific stock for products derived from the exploited North Pacific minke whale. The market sample differed significantly from the scientific catch (p < 0.001), showing a greater than expected frequency of haplotypes characteristic of the protected Sea of Japan stock. We used a 'mixed-stock' analysis and maximum-likelihood methods to estimate that 31% (95% confidence interval 19-43%) of the market for this species originated from the Sea of Japan stock. The source of these products was assumed to be undocumented 'incidental takes' from fisheries' by-catch, although we cannot exclude the possibility of illegal hunting or smuggling. The demographic impact of this undocumented exploitation was evaluated using the model of population dynamics adopted by the Scientific Committee of the International Whaling Commission. For the range of exploitation consistent with the market sample, this protected stock was predicted to decline towards extinction over the next few decades. These results confirmed the power of molecular methods in monitoring retail markets and pointed to the inadequacy of the current moratorium for ensuring the recovery of protected species. More importantly, the integration of genetic evidence with a model of population dynamics identified an urgent need for actions to limit undocumented exploitation of a 'protected' stock of whales.
View details for Web of Science ID 000087837100005
View details for PubMedID 10902685
View details for PubMedCentralID PMC1690661
All males are not created equal: Fertility differences depend on gamete recognition polymorphisms in sea urchins
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
1999; 96 (22): 12632-12637
Behaviors, morphologies, and genetic loci directly involved in reproduction have been increasingly shown to be polymorphic within populations. Explaining how such variants are maintained by selection is crucial to understanding the genetic basis of fertility differences, but direct tests of how alleles at reproductive loci affect fertility are rare. In the sea urchin genus Echinometra, the protein bindin mediates sperm attachment to eggs, evolves quickly, and is polymorphic within species. Eggs exposed to experimental sperm mixtures show strong discrimination on the basis of the males' bindin genotype. Different females produce eggs that nonrandomly select sperm from different males, showing that variable egg-sperm interactions determine fertility. Eggs select sperm with a bindin genotype similar to their own, suggesting strong linkage between female choice and male trait loci. These experiments demonstrate that alleles at a single locus can have a strong effect on fertilization and that reproductive loci may retain functional polymorphisms through epistatic interactions between male and female traits. They also suggest that positive selection at gamete recognition loci like bindin involves strong selection within species on mate choice interactions.
View details for Web of Science ID 000083373000079
View details for PubMedID 10535974
View details for PubMedCentralID PMC23023
Population structure of the black tiger prawn, Penaeus monodon, among western Indian Ocean and western Pacific populations
1999; 134 (4): 705-710
View details for Web of Science ID 000082633300012
Developmental shifts and species selection in gastropods
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
1999; 96 (18): 10272-10277
The fossil record of marine gastropods has been used as evidence to support the operation of species selection; namely, that species with limited dispersal differentially increase in numbers because they are more likely to speciate than widely dispersing species. This conclusion is based on a tacit phylogenetic assumption that increases in species with limited dispersal are solely the result of speciation within monophyletic groups with low dispersal. To test this assumption, we reconstructed a phylogeny from nuclear sequence data for 70 species of the marine gastropod genus Conus and used it to map the evolution of developmental mode. All eight species without planktonic life history phases recently and independently evolved this characteristic from ancestors with planktonic larval phases, showing that transitions in developmental mode are common in this group. A simple model of species diversification shows that such shifts can control the relative numbers of species with and without dispersing larval stages, leading to apparent species selection. Such results challenge the conclusion that increases in the number of nonplanktonic species relative to species with planktonic larvae over geologic time is necessarily a result of higher rates of speciation of nonplanktonic lineages and show that demonstration of species selection requires a phylogenetic framework.
View details for Web of Science ID 000082424100062
View details for PubMedID 10468598
View details for PubMedCentralID PMC17878
Molecular genetics of ecological diversification: Duplication and rapid evolution of toxin genes of the venomous gastropod Conus
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
1999; 96 (12): 6820-6823
Predatory snails in the marine gastropod genus Conus stun prey by injecting a complex mixture of peptide neurotoxins. These conotoxins are associated with trophic diversification and block a diverse array of ion channels and neuronal receptors in prey species, but the evolutionary genesis of this functional diversity is unknown. Here we show that conotoxins with little amino acid similarity are in fact products of recently diverged loci that are rapidly evolving by strong positive selection in the vermivorous cone, Conus abbreviatus, and that the rate of conotoxin evolution is higher than that of most other known proteins. Gene duplication and diversifying selection result in the formation of functionally variable conotoxins that are linked to ecological diversification and evolutionary success of this genus.
View details for Web of Science ID 000080842200045
View details for PubMedID 10359796
View details for PubMedCentralID PMC21999
Intraspecific genetic diversity in the marine shrimp Penaeus vannamei: Multiple polymorphic elongation factor-1 alpha loci revealed by intron sequencing
1999; 1 (3): 261-268
View details for Web of Science ID 000081514400006
Speciation and population genetic structure in tropical Pacific Sea urchins
1997; 51 (5): 1506-1517
View details for Web of Science ID A1997YE98000018
Molecular evolution of a portion of the mitochondrial 16S ribosomal gene region in scleractinian corals
JOURNAL OF MOLECULAR EVOLUTION
1997; 45 (4): 397-411
Relationships among families and suborders of scleractinian corals are poorly understood because of difficulties 1) in making inferences about the evolution of the morphological characters used in coral taxonomy and 2) in interpreting their 240-million-year fossil record. Here we describe patterns of molecular evolution in a segment of the mitochondrial (mt) 16S ribosomal gene from taxa of 14 families of corals and the use of this gene segment in a phylogenetic analysis of relationships within the order. We show that sequences obtained from scleractinians are homologous to other metazoan 16S ribosomal sequences and fall into-two distinct clades defined by size of the amplified gene product. Comparisons of sequences from the two clades demonstrate that both sets of sequences are evolving under similar evolutionary constraints: they do not differ in nucleotide composition, numbers of transition and transversion substitutions, spatial patterns of substitutions, or in rates of divergence. The characteristics and patterns observed in these sequences as well as the secondary structures, are similar to those observed in mt 16S ribosomal DNA sequences from other taxa. Phylogenetic analysis of these sequences shows that they are useful for evaluating relationships within the order. The hypothesis generated from this analysis differs from traditional hypotheses for evolutionary relationships among the Scleractinia and suggests that a reevaluation of evolutionary affinities in the order is needed.
View details for Web of Science ID A1997XX82400009
View details for PubMedID 9321419
Evolution of scleractinian corals inferred from molecular systematics
1996; 271 (5249): 640-642
View details for Web of Science ID A1996TT87000043
HIERARCHICAL STRUCTURE OF MITOCHONDRIAL-DNA GENE FLOW AMONG HUMPBACK WHALES MEGAPTERA-NOVAEANGLIAE, WORLDWIDE
1994; 3 (4): 313-327
The genetic structure of humpback whale populations and subpopulation divisions is described by restriction fragment length analysis of the mitochondrial (mt) DNA from samples of 230 whales collected by biopsy darting in 11 seasonal habitats representing six subpopulations, or 'stocks', world-wide. The hierarchical structure of mtDNA haplotype diversity among population subdivisions is described using the analysis of molecular variance (AMOVA) procedure, the analysis of gene identity, and the genealogical relationship of haplotypes as constructed by parsimony analysis and distance clustering. These analyses revealed: (i) significant partitioning of world-wide genetic variation among oceanic populations, among subpopulations or 'stocks' within oceanic populations and among seasonal habitats within stocks; (ii) fixed categorical segregation of haplotypes on the south-eastern Alaska and central California feeding grounds of the North Pacific; (iii) support for the division of the North Pacific population into a central stock which feeds in Alaska and winters in Hawaii, and an eastern or 'American' stock which feeds along the coast of California and winters near Mexico; (iv) evidence of genetic heterogeneity within the Gulf of Maine feeding grounds and among the sampled feeding and breeding grounds of the western North Atlantic; and (v) support for the historical division between the Group IV (Western Australia) and Group V (eastern Australia, New Zealand and Tonga) stocks in the Southern Oceans. Overall, our results demonstrate a striking degree of genetic structure both within and between oceanic populations of humpback whales, despite the nearly unlimited migratory potential of this species. We suggest that the humpback whale is a suitable demographic and genetic model for the management of less tractable species of baleen whales and for the general study of gene flow among long-lived, mobile vertebrates in the marine ecosystem.
View details for Web of Science ID A1994PD87200005
View details for PubMedID 7921358
ABUNDANT MITOCHONDRIAL-DNA VARIATION AND WORLDWIDE POPULATION-STRUCTURE IN HUMPBACK WHALES
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
1993; 90 (17): 8239-8243
Hunting during the last 200 years reduced many populations of mysticete whales to near extinction. To evaluate potential genetic bottlenecks in these exploited populations, we examined mitochondrial DNA control region sequences from 90 individual humpback whales (Megaptera novaeangliae) representing six subpopulations in three ocean basins. Comparisons of relative nucleotide and nucleotype diversity reveal an abundance of genetic variation in all but one of the oceanic subpopulations. Phylogenetic reconstruction of nucleotypes and analysis of maternal gene flow show that current genetic variation is not due to postexploitation migration between oceans but is a relic of past population variability. Calibration of the rate of control region evolution across three families of whales suggests that existing humpback whale lineages are of ancient origin. Preservation of preexploitation variation in humpback whales may be attributed to their long life-span and overlapping generations and to an effective, though perhaps not timely, international prohibition against hunting.
View details for Web of Science ID A1993LV64400069
View details for PubMedID 8367488
View details for PubMedCentralID PMC47324
INFLUENCE OF SEASONAL MIGRATION ON GEOGRAPHIC-DISTRIBUTION OF MITOCHONDRIAL-DNA HAPLOTYPES IN HUMPBACK WHALES
1990; 344 (6263): 238-240
Humpback whales (Megaptera novaeangliae) migrate nearly 10,000 km each year between summer feeding grounds in temperate or near-polar waters and winter breeding grounds in shallow tropical waters. Observations of marked individuals suggest that major oceanic populations of humpback whales are divided into a number of distinct seasonal subpopulations which are not separated by obvious geographic barriers. To test whether these observed patterns of distribution and migration are reflected in the genetic structure of populations, we looked for variation in the mitochondrial DNA of 84 individual humpback whales on different feeding and wintering grounds of the North Pacific and western North Atlantic oceans. On the basis of restriction-fragment analysis, we now report a marked segregation of mitochondrial DNA haplotypes among subpopulations as well as between the two oceans. We interpret this segregation to be the consequence of maternally directed fidelity to migratory destinations.
View details for Web of Science ID A1990CU13800056
View details for PubMedID 1969116
- GRAFT COMPATIBILITY AND CLONAL IDENTITY IN INVERTEBRATES SCIENCE 1985; 229 (4712): 487-488
AGING IN MODULAR ORGANISMS - ECOLOGY OF ZOOID SENESCENCE IN STEGINOPORELLA SP (BRYOZOA, CHEILOSTOMATA)
1983; 164 (2): 267-278
View details for Web of Science ID A1983QM95000010
ECOLOGY OF CRYPTIC CORAL-REEF COMMUNITIES .2. RECOVERY FROM SMALL DISTURBANCE EVENTS BY ENCRUSTING BRYOZOA - THE INFLUENCE OF HOST SPECIES AND LESION SIZE
JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY
1982; 64 (2): 103-115
View details for Web of Science ID A1982PK64100001