Senior Associate Vice Provost of Undergraduate Education, VPUE (2013 - Present)
Ph.D., Univ. California, Berkeley, Integrative Biology (1995)
M.S., Northern Arizona University, Quaternary Studies (1990)
B.A., Univ. Colorado, Boulder, Anthropology (1981)
Current Research and Scholarly Interests
ELIZABETH A. HADLY
PROFESSOR, DEPARTMENT OF BIOLOGY AND DEPARTMENT OF GEOLOGICAL SCIENCES, BY COURTESY
Professor Hadly uses a combined field and laboratory approach to examine how ecological perturbations link or decouple levels of biological organization, because understanding the links among ecosystems, species, populations and genes is central to understanding how organisms exist, evolve and become extinct. She addresses problems in organismal biology from both evolutionary and ecological perspectives, primarily using extant mammals. One of the unique aspects of her overall approach is the focus on the decadal to millennial time scale, a scale that is little studied, although it is a scale that is integral to understanding links between ecology and evolution.
Living on the roof of the world: mechanisms underlying hypo tolerance in pikas, Stanford University (2012 - Present)
This research investigates the mechanisms underlying species tolerance of extreme environments, focusing on pika (genus Ochotona). There are 30 pika species, each occupying a unique elevational range between 0 - 6400 m with the highest concentration of species diversity in the Himalayas and Tibetan Plateau region. Limited oxygen at high elevation critically stresses aerobic metabolism; however, little is known about how pikas are capable of tolerating the extreme hypoxia of their high-elevation habitat. Additionally, climate change is causing many pika populations to shift their ranges even higher in elevation.
- Uma Ramakrishnan, Visiting Associate Professor, Biology, National Center for Biological Sciences, Bangalore, India
Tracing zoonotic disease risks and immunological adaptations in bats, humans and human commensals across the Central American countryside, Stanford University (1/1/2015 - Present)
Bats have been identified as the reservoirs for a number of emerging infectious diseases but most of these pathogens have coevolved with their hosts for long periods of time without causing issue. We are seeking to understand the potential sources, sinks and pathways of zoonotic infection in a countryside landscape that is home to one of the most diverse bat faunas in the world by examining bats and livestock as well as surveying human behavior.
Evolution, Extinction, and Conservation of Caribbean Mammals, Stanford University (2013 - Present)
We take an interdisciplinary approach to reconstruct recent extinctions in the Caribbean across the past 15,000 years, and leverage these data towards guiding conservation planning in the region under a changing climate and growing human population. Techniques include genomics, stable isotopes, radiocarbon dating, and morphometrics.
- Juan Almonte, Curator, Museo Nacional de Historia Natural, Santo Domingo
Ecological and evolutionary aspects of the bat-infection relationship, Stanford University (February 2012 - Present)
Costa Rica is home to one of the richest, most ecologically diverse bat faunas in the world and is also subject to widespread habitat conversion like many developing nations. We seek to understand how bat ecology and deforestation affect infections in bats as well as how ecologically diverse bats may have evolved to deal with their infections.
Gene Expression, not local adaptation, sufficient for pikas to occupy vast Himalayan elevational gradient, Stanford Uniniversity
Species are shifting their ranges due to climate change, many moving to cooler and higher locations. However, with elevation increase comes oxygen decline, potentially limiting a species’ ability to track its environment depending on what mechanisms it has available to compensate for hypoxic stress. Pikas (Family Ochotonidae), cold-specialist small mammal species, are already undergoing elevational range shifts. We collected RNA samples from one population of Ochotona roylei in the western Himalaya at three sites – 3,600, 4,000, and 5,000 meters – and found no evidence of significant population genetic structure, nor any loci under positive selection between sites. However, out of over 10,000 expressed transcripts, 26 were significantly up-regulated at the 5,000 m site and were significantly enriched for pathways consistent with physiological compensation for limited oxygen. These results suggest that differences in gene expression alone may enable hypoxia tolerance on this local scale, indicating elevational flexibility that may facilitate successful range shifts in response to climate change.
Low-coverage Genome Sequencing of Black Rhinoceros to Inform Conservation Management, Stanford University (January 1, 2015 - Present)
Anthropogenic pressures (e.g. poaching) have tremendously reduced the black rhinoceros (Diceros bicornis) distribution and population size. While conservation efforts have been effective, doubling the population size over 20 years from a low of 2,400 individuals, the species remains critically endangered and populations must be actively protected from poaching. We are sequencing hundreds of low coverage genomes from one of the largest collections of rhino tissue samples collected to date in Africa to 1) determine parentage for offspring and evaluate the effect of management actions (e.g. dehornings, translocations) on reproductive success and breeding patterns and 2) determine relevant genetic characteristics of each population. Our results will be directly applicable to the genetic and demographic management of free-ranging populations and especially to the planning of rhino re-introduction projects.
- Conservation and Population Genomics
BIO 386 (Aut, Spr)
- I, Scientist: Diversity Improves the Scientific Practice
BIO 52, CSRE 52H (Aut)
Independent Studies (12)
- Advanced Research Laboratory in Experimental Biology
BIO 199 (Aut, Win, Spr, Sum)
- Directed Individual Study in Earth Systems
EARTHSYS 297 (Aut, Win, Spr, Sum)
- 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, Win, Spr, Sum)
- Honors Program in Earth Systems
EARTHSYS 199 (Aut, Win, Spr, Sum)
- Out-of-Department Advanced Research Laboratory in Experimental Biology
BIO 199X (Sum)
- Out-of-Department Directed Reading
BIO 198X (Sum)
- Out-of-Department Graduate Research
BIO 300X (Sum)
- Teaching of Biology
BIO 290 (Aut, Win, Spr)
- Advanced Research Laboratory in Experimental Biology
Prior Year Courses
- Conservation and Population Genomics
BIO 386 (Spr)
- Conservation and Population Genomics
Graduate and Fellowship Programs
Biology (School of Humanities and Sciences) (Phd Program)
Evolution for extreme living: variation in mitochondrial cytochrome c oxidase genes correlated with elevation in pikas (genus Ochotona).
The genus Ochotona (pikas) is a clade of cold-tolerant lagomorphs that includes many high-elevation species. Pikas offer a unique opportunity to study adaptations and potential limitations of an ecologically important mammal to high-elevation hypoxia. We analyzed the evolution of three mitochondrial genes encoding the catalytic core of cytochrome c oxidase (COX) in 10 pika species occupying elevations from sea level to 5,000 meters. COX is an enzyme highly reliant on oxygen and essential for cell function. One amino acid property, the equilibrium constant (ionization of COOH), was found to be under selection in the overall protein complex. We observed a strong relationship between the net value change in this property and the elevation each species occupies, with higher-elevation species having potentially more efficient proteins. We also found evidence of selection in low-elevation species for potentially less efficient COX, perhaps trading efficiency for heat production in the absence of hypoxia. Our results suggest that different pika species may have evolved elevation-specific COX proteins, specialization that may indicate limitations in their ability to shift their elevational ranges in response to future climate change. This article is protected by copyright. All rights reserved.
View details for DOI 10.1111/1749-4877.12332
View details for PubMedID 29851233
- Making America great again requires acting on scientific knowledge. PLoS biology 2018; 16 (2): e2004337
Rethinking "Native" in the Anthropocene
Frontiers in Earth Science
2018; 6: 1-4
View details for DOI 10.3389/feart.2018.00096
- Genomic data reveal a loss of diversity in two species of tucotucos (genus Ctenomys) following a volcanic eruption SCIENTIFIC REPORTS 2017; 7
Rethinking the Origin of Primates by Reconstructing Their Diel Activity Patterns Using Genetics and Morphology
2017; 7: 11837
Phylogenetic inference typically invokes nocturnality as ancestral in primates; however, some recent studies posit that diurnality is. Here, through adaptive evolutionary analyses of phototransduction genes by using a variety of approaches (restricted branch/branch-site models and unrestricted branch-site-based models (BS-REL, BUSTED and RELAX)), our results consistently showed that ancestral primates were subjected to enhanced positive selection for bright-light vision and relatively weak selection for dim-light vision. These results suggest that ancestral primates were mainly diurnal with some crepuscularity and support diurnality as plesiomorphic from Euarchontoglires. Our analyses show relaxed selection on motion detection in ancestral primates, suggesting that ancestral primates decreased their emphasis on mobile prey (e.g., insects). However, within primates, the results show that ancestral Haplorrhini were likely nocturnal, suggesting that evolution of the retinal fovea occurred within ancestral primates rather than within haplorrhines as was previously hypothesized. Our findings offer a reassessment of the visual adaptation of ancestral primates. The evolution of the retinal fovea, trichromatic vision and orbital convergence in ancestral primates may have helped them to efficiently discriminate, target, and obtain edible fruits and/or leaves from a green foliage background instead of relying on mobile insect prey.
View details for DOI 10.1038/s41598-017-12090-3
View details for Web of Science ID 000411165100014
View details for PubMedID 28928374
View details for PubMedCentralID PMC5605515
Invasion of Ancestral Mammals into Dim-light Environments Inferred from Adaptive Evolution of the Phototransduction Genes.
2017; 7: 46542-?
Nocturnality is a key evolutionary innovation of mammals that enables mammals to occupy relatively empty nocturnal niches. Invasion of ancestral mammals into nocturnality has long been inferred from the phylogenetic relationships of crown Mammalia, which is primarily nocturnal, and crown Reptilia, which is primarily diurnal, although molecular evidence for this is lacking. Here we used phylogenetic analyses of the vision genes involved in the phototransduction pathway to predict the diel activity patterns of ancestral mammals and reptiles. Our results demonstrated that the common ancestor of the extant Mammalia was dominated by positive selection for dim-light vision, supporting the predominate nocturnality of the ancestral mammals. Further analyses showed that the nocturnality of the ancestral mammals was probably derived from the predominate diurnality of the ancestral amniotes, which featured strong positive selection for bright-light vision. Like the ancestral amniotes, the common ancestor of the extant reptiles and various taxa in Squamata, one of the main competitors of the temporal niches of the ancestral mammals, were found to be predominate diurnality as well. Despite this relatively apparent temporal niche partitioning between ancestral mammals and the relevant reptiles, our results suggested partial overlap of their temporal niches during crepuscular periods.
View details for DOI 10.1038/srep46542
View details for PubMedID 28425474
Merging paleobiology with conservation biology to guide the future of terrestrial ecosystems
2017; 355 (6325): 594-?
Conservation of species and ecosystems is increasingly difficult because anthropogenic impacts are pervasive and accelerating. Under this rapid global change, maximizing conservation success requires a paradigm shift from maintaining ecosystems in idealized past states toward facilitating their adaptive and functional capacities, even as species ebb and flow individually. Developing effective strategies under this new paradigm will require deeper understanding of the long-term dynamics that govern ecosystem persistence and reconciliation of conflicts among approaches to conserving historical versus novel ecosystems. Integrating emerging information from conservation biology, paleobiology, and the Earth sciences is an important step forward on the path to success. Maintaining nature in all its aspects will also entail immediately addressing the overarching threats of growing human population, overconsumption, pollution, and climate change.
View details for DOI 10.1126/science.aah4787
View details for Web of Science ID 000393636700038
View details for PubMedID 28183912
Genetics, morphology and ecology reveal a cryptic pika lineage in the Sikkim Himalaya.
Molecular phylogenetics and evolution
2017; 106: 55-60
Asian pika species are morphologically ∼similar and have overlapping ranges. This leads to uncertainty and species misidentification in the field. Phylogenetic analyses of such misidentified samples leads to taxonomic ambiguity. The ecology of many pika species remains understudied, particularly in the Himalaya, where sympatric species could be separated by elevation and/or substrate. We sampled, measured, and acquired genetic data from pikas in the Sikkim Himalaya. Our analyses revealed a cryptic lineage, Ochotona sikimaria, previously reported as a subspecies of O. thibetana. The results support the elevation of this lineage to the species level, as it is genetically divergent from O. thibetana, as well as sister species, O. cansus (endemic to central China) and O. curzoniae (endemic to the Tibetan plateau). The Sikkim lineage diverged from its sister species' about 1.7-0.8myrago, coincident with uplift events in the Himalaya. Our results add to the recent spate of cryptic diversity identified from the eastern Himalaya and highlight the need for further study within the Ochotonidae.
View details for DOI 10.1016/j.ympev.2016.09.015
View details for PubMedID 27640954
Phylogeny, Traits, and Biodiversity of a Neotropical Bat Assemblage: Close Relatives Show Similar Responses to Local Deforestation.
The American naturalist
2017; 190 (2): 200–212
If species' evolutionary pasts predetermine their responses to evolutionarily novel stressors, then phylogeny could predict species survival in an increasingly human-dominated world. To understand the role of phylogenetic relatedness in structuring responses to rapid environmental change, we focused on assemblages of Neotropical bats, an ecologically diverse and functionally important group. We examined how taxonomic and phylogenetic diversity shift between tropical forest and farmland. We then explored the importance of evolutionary history by ascertaining whether close relatives share similar responses to environmental change and which species traits might mediate these trends. We analyzed a 5-year data set (5,011 captures) from 18 sites in a countryside landscape in southern Costa Rica using statistical models that account and correct for imperfect detection of species across sites, spatial autocorrelation, and consideration of spatial scale. Taxonomic and phylogenetic diversity decreased with deforestation, and assemblages became more phylogenetically clustered. Species' responses to deforestation were strongly phylogenetically correlated. Body mass and absolute wing loading explained a substantial portion of species variation in species' habitat preferences, likely related to these traits' influence on maneuverability in cluttered forest environments. Our findings highlight the role that evolutionary history plays in determining which species will survive human impacts and the need to consider diversity metrics, evolutionary history, and traits together when making predictions about species persistence for conservation or ecosystem functioning.
View details for DOI 10.1086/692534
View details for PubMedID 28731793
Frequency shifting reduces but does not eliminate acoustic interference between echolocating bats: A theoretical analysis
The Journal of the Acoustical Society of America
2017; 142: 2133
Bats have been observed to shift the frequency of their echolocation calls in the presence of other echolocating bats, ostensibly as a way to reduce acoustic interference. Few studies, however, have examined the theoretical efficacy of such jamming avoidance responses. The present study uses the wideband ambiguity function to analyze the effects of acoustic interference from conspecifics and congeneric heterospecifics on the target acquisition ability of Myotis californicus and Myotis yumanensis, specifically whether unilateral or bilateral frequency shifts reduce the effects of such interference. Model results suggest that in conspecific interactions, M. yumanensis recovers its target acquisition ability more completely and with less absolute frequency shift than does M. californicus, but that alternative methods of jamming avoidance may be easier to implement. The optimal strategy for reducing heterospecific interference is for M. californicus to downshift its call and M. yumanensis to upshift its call, which exaggerates a preexisting difference in mean frequency between the calls of the two species. Further empirical research would elucidate whether these species do in practice actively employ frequency shifting or other means for jamming avoidance, as well as illuminate the role of acoustic interference in niche partitioning.
View details for DOI 10.1121/1.5006928
Opportunity for some, extinction for others: the fate of tetrapods in the Anthropocene
EVOLUTIONARY ECOLOGY RESEARCH
2016; 17 (6): 787-813
View details for Web of Science ID 000392724100006
Getting a head in hard soils: Convergent skull evolution and divergent allometric patterns explain shape variation in a highly diverse genus of pocket gophers (Thomomys)
BMC EVOLUTIONARY BIOLOGY
High morphological diversity can occur in closely related animals when selection favors morphologies that are subject to intrinsic biological constraints. A good example is subterranean rodents of the genus Thomomys, one of the most taxonomically and morphologically diverse mammalian genera. Highly procumbent, tooth-digging rodent skull shapes are often geometric consequences of increased body size. Indeed, larger-bodied Thomomys species tend to inhabit harder soils. We used geometric morphometric analyses to investigate the interplay between soil hardness (the main extrinsic selection pressure on fossorial mammals) and allometry (i.e. shape change due to size change; generally considered the main intrinsic factor) on crania and humeri in this fast-evolving mammalian clade.Larger Thomomys species/subspecies tend to have more procumbent cranial shapes with some exceptions, including a small-bodied species inhabiting hard soils. Counter to earlier suggestions, cranial shape within Thomomys does not follow a genus-wide allometric pattern as even regional subpopulations differ in allometric slopes. In contrast, humeral shape varies less with body size and with soil hardness. Soft-soil taxa have larger humeral muscle attachment sites but retain an orthodont (non-procumbent) cranial morphology. In intermediate soils, two pairs of sister taxa diverge through differential modifications on either the humerus or the cranium. In the hardest soils, both humeral and cranial morphology are derived through large muscle attachment sites and a high degree of procumbency.Our results show that conflict between morphological function and intrinsic allometric patterning can quickly and differentially alter the rodent skeleton, especially the skull. In addition, we found a new case of convergent evolution of incisor procumbency among large-, medium-, and small-sized species inhabiting hard soils. This occurs through different combinations of allometric and non-allometric changes, contributing to shape diversity within the genus. The strong influence of allometry on cranial shape appears to confirm suggestions that developmental change underlies mammalian cranial shape divergences, but this requires confirmation from ontogenetic studies. Our findings illustrate how a variety of intrinsic processes, resulting in species-level convergence, could sustain a genus-level range across a variety of extrinsic environments. This might represent a mechanism for observations of genus-level niche conservation despite species extinctions in mammals.
View details for DOI 10.1186/s12862-016-0782-1
View details for Web of Science ID 000386025400005
View details for PubMedID 27724858
View details for PubMedCentralID PMC5057207
Climate change and habitat conversion favour the same species
2016; 19 (9): 1081-1090
Land-use change and climate change are driving a global biodiversity crisis. Yet, how species' responses to climate change are correlated with their responses to land-use change is poorly understood. Here, we assess the linkages between climate and land-use change on birds in Neotropical forest and agriculture. Across > 300 species, we show that affiliation with drier climates is associated with an ability to persist in and colonise agriculture. Further, species shift their habitat use along a precipitation gradient: species prefer forest in drier regions, but use agriculture more in wetter zones. Finally, forest-dependent species that avoid agriculture are most likely to experience decreases in habitable range size if current drying trends in the Neotropics continue as predicted. This linkage suggests a synergy between the primary drivers of biodiversity loss. Because they favour the same species, climate and land-use change will likely homogenise biodiversity more severely than otherwise anticipated.
View details for DOI 10.1111/ele.12645
View details for Web of Science ID 000382542500008
View details for PubMedID 27396714
- Rocking Earth's biodiversity cradle: challenges, advances, and prospects for conservation paleontology in the tropics JOURNAL OF VERTEBRATE PALEONTOLOGY 2016; 36 (5)
- Anthropogenic impacts on Costa Rican bat parasitism are sex specific ECOLOGY AND EVOLUTION 2016; 6 (14): 4898-4909
Post-invasion demography of prehistoric humans in South America.
2016; 532 (7598): 232-235
As the last habitable continent colonized by humans, the site of multiple domestication hotspots, and the location of the largest Pleistocene megafaunal extinction, South America is central to human prehistory. Yet remarkably little is known about human population dynamics during colonization, subsequent expansions, and domestication. Here we reconstruct the spatiotemporal patterns of human population growth in South America using a newly aggregated database of 1,147 archaeological sites and 5,464 calibrated radiocarbon dates spanning fourteen thousand to two thousand years ago (ka). We demonstrate that, rather than a steady exponential expansion, the demographic history of South Americans is characterized by two distinct phases. First, humans spread rapidly throughout the continent, but remained at low population sizes for 8,000 years, including a 4,000-year period of 'boom-and-bust' oscillations with no net growth. Supplementation of hunting with domesticated crops and animals had a minimal impact on population carrying capacity. Only with widespread sedentism, beginning ~5 ka, did a second demographic phase begin, with evidence for exponential population growth in cultural hotspots, characteristic of the Neolithic transition worldwide. The unique extent of humanity's ability to modify its environment to markedly increase carrying capacity in South America is therefore an unexpectedly recent phenomenon.
View details for DOI 10.1038/nature17176
View details for PubMedID 27049941
- Early Holocene turnover, followed by stability, in a Caribbean lizard assemblage QUATERNARY RESEARCH 2016; 85 (2): 255-261
- Variable impact of late-Quaternary megafaunal extinction in causing ecological state shifts in North and South America PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 2016; 113 (4): 856-861
- Bartonellae are Prevalent and Diverse in Costa Rican Bats and Bat Flies ZOONOSES AND PUBLIC HEALTH 2015; 62 (8): 609-617
- Extinction biases in Quaternary Caribbean lizards GLOBAL ECOLOGY AND BIOGEOGRAPHY 2015; 24 (11): 1281-1289
- Thermal niche predicts tolerance to habitat conversion in tropical amphibians and reptiles GLOBAL CHANGE BIOLOGY 2015; 21 (11): 3901-3916
- Loss of avian phylogenetic diversity in neotropical agricultural systems SCIENCE 2014; 345 (6202): 1343-1346
Predicting biodiversity change and averting collapse in agricultural landscapes.
2014; 509 (7499): 213-217
The equilibrium theory of island biogeography is the basis for estimating extinction rates and a pillar of conservation science. The default strategy for conserving biodiversity is the designation of nature reserves, treated as islands in an inhospitable sea of human activity. Despite the profound influence of islands on conservation theory and practice, their mainland analogues, forest fragments in human-dominated landscapes, consistently defy expected biodiversity patterns based on island biogeography theory. Countryside biogeography is an alternative framework, which recognizes that the fate of the world's wildlife will be decided largely by the hospitality of agricultural or countryside ecosystems. Here we directly test these biogeographic theories by comparing a Neotropical countryside ecosystem with a nearby island ecosystem, and show that each supports similar bat biodiversity in fundamentally different ways. The island ecosystem conforms to island biogeographic predictions of bat species loss, in which the water matrix is not habitat. In contrast, the countryside ecosystem has high species richness and evenness across forest reserves and smaller forest fragments. Relative to forest reserves and fragments, deforested countryside habitat supports a less species-rich, yet equally even, bat assemblage. Moreover, the bat assemblage associated with deforested habitat is compositionally novel because of predictable changes in abundances by many species using human-made habitat. Finally, we perform a global meta-analysis of bat biogeographic studies, spanning more than 700 species. It generalizes our findings, showing that separate biogeographic theories for countryside and island ecosystems are necessary. A theory of countryside biogeography is essential to conservation strategy in the agricultural ecosystems that comprise roughly half of the global land surface and are likely to increase even further.
View details for DOI 10.1038/nature13139
View details for PubMedID 24739971
- Predicting biodiversity change and averting collapse in agricultural landscapes NATURE 2014; 509 (7499): 213-?
A call for tiger management using "reserves" of genetic diversity.
journal of heredity
2014; 105 (3): 295-302
Tigers (Panthera tigris), like many large carnivores, are threatened by anthropogenic impacts, primarily habitat loss and poaching. Current conservation plans for tigers focus on population expansion, with the goal of doubling census size in the next 10 years. Previous studies have shown that because the demographic decline was recent, tiger populations still retain a large amount of genetic diversity. Although maintaining this diversity is extremely important to avoid deleterious effects of inbreeding, management plans have yet to consider predictive genetic models. We used coalescent simulations based on previously sequenced mitochondrial fragments (n = 125) from 5 of 6 extant subspecies to predict the population growth needed to maintain current genetic diversity over the next 150 years. We found that the level of gene flow between populations has a large effect on the local population growth necessary to maintain genetic diversity, without which tigers may face decreases in fitness. In the absence of gene flow, we demonstrate that maintaining genetic diversity is impossible based on known demographic parameters for the species. Thus, managing for the genetic diversity of the species should be prioritized over the riskier preservation of distinct subspecies. These predictive simulations provide unique management insights, hitherto not possible using existing analytical methods.
View details for DOI 10.1093/jhered/est086
View details for PubMedID 24336928
Molecular diagnosis of bird-mediated pest consumption in tropical farmland.
2014; 3: 630-?
Biodiversity loss will likely have surprising and dramatic consequences for human wellbeing. Identifying species that benefit society represents a critical first step towards predicting the consequences of biodiversity loss. Though natural predators prevent billions of dollars in agricultural pest damage annually, characterizing which predators consume pests has proven challenging. Emerging molecular techniques may illuminate these interactions. In the countryside of Costa Rica, we identified avian predators of coffee's most damaging insect pest, the coffee berry borer beetle (Coleoptera:Scolytidae Hypothenemus hampeii), by assaying 1430 fecal samples of 108 bird species for borer DNA. While feeding trials confirmed the efficacy of our approach, detection rates were low. Nevertheless, we identified six species that consume the borer. These species had narrow diet breadths, thin bills, and short wings; traits shared with borer predators in other systems. Borer predators were not threatened; therefore, safeguarding pest control necessitates managing species beyond those at risk of regional extinction by maintaining populations in farmland habitats. Generally, our results demonstrate potential for pairing molecular methods with ecological analyses to yield novel insights into species interactions.
View details for DOI 10.1186/2193-1801-3-630
View details for PubMedID 25392800
- Molecular diagnosis of bird-mediated pest consumption in tropical farmland. SpringerPlus 2014; 3: 630-?
Forest bolsters bird abundance, pest control and coffee yield
2013; 16 (11): 1339-1347
Efforts to maximise crop yields are fuelling agricultural intensification, exacerbating the biodiversity crisis. Low-intensity agricultural practices, however, may not sacrifice yields if they support biodiversity-driven ecosystem services. We quantified the value native predators provide to farmers by consuming coffee's most damaging insect pest, the coffee berry borer beetle (Hypothenemus hampei). Our experiments in Costa Rica showed birds reduced infestation by ~ 50%, bats played a marginal role, and farmland forest cover increased pest removal. We identified borer-consuming bird species by assaying faeces for borer DNA and found higher borer-predator abundances on more forested plantations. Our coarse estimate is that forest patches doubled pest control over 230 km2 by providing habitat for ~ 55 000 borer-consuming birds. These pest-control services prevented US$75-US$310 ha-year(-1) in damage, a benefit per plantation on par with the average annual income of a Costa Rican citizen. Retaining forest and accounting for pest control demonstrates a win-win for biodiversity and coffee farmers.
View details for DOI 10.1111/ele.12173
View details for Web of Science ID 000325976500002
View details for PubMedID 23981013
- Asymmetrical Competition between Microtus montanus and Microtus longicaudus in the Greater Yellowstone Ecosystem AMERICAN MIDLAND NATURALIST 2013; 170 (2): 274-286
Morphological Adaptations for Digging and Climate-Impacted Soil Properties Define Pocket Gopher (Thomomys spp.) Distributions.
2013; 8 (5)
Species ranges are mediated by physiology, environmental factors, and competition with other organisms. The allopatric distribution of five species of northern Californian pocket gophers (Thomomys spp.) is hypothesized to result from competitive exclusion. The five species in this environmentally heterogeneous region separate into two subgenera, Thomomys or Megascapheus, which have divergent digging styles. While all pocket gophers dig with their claws, the tooth-digging adaptations of subgenus Megascapheus allow access to harder soils and climate-protected depths. In a Northern Californian locality, replacement of subgenus Thomomys with subgenus Megascapheus occurred gradually during the Pleistocene-Holocene transition. Concurrent climate change over this transition suggests that environmental factors - in addition to soil - define pocket gopher distributional limits. Here we show 1) that all pocket gophers occupy the subset of less energetically costly soils and 2) that subgenera sort by percent soil clay, bulk density, and shrink-swell capacity (a mineralogical attribute). While clay and bulk density (without major perturbations) stay constant over decades to millennia, low precipitation and high temperatures can cause shrink-swell clays to crack and harden within days. The strong yet underappreciated interaction between soil and moisture on the distribution of vertebrates is rarely considered when projecting species responses to climatic change. Furthermore, increased precipitation alters the weathering processes that create shrink-swell minerals. Two projected outcomes of ongoing climate change-higher temperatures and precipitation-will dramatically impact hardness of soil with shrink-swell minerals. Current climate models do not include factors controlling soil hardness, despite its impact on all organisms that depend on a stable soil structure.
View details for DOI 10.1371/journal.pone.0064935
View details for PubMedID 23717675
View details for PubMedCentralID PMC3663803
- Genetic diversity within vertebrate species is greater at lower latitudes EVOLUTIONARY ECOLOGY 2013; 27 (1): 133-143
Approaching a state shift in Earth's biosphere
2012; 486 (7401): 52-58
Localized ecological systems are known to shift abruptly and irreversibly from one state to another when they are forced across critical thresholds. Here we review evidence that the global ecosystem as a whole can react in the same way and is approaching a planetary-scale critical transition as a result of human influence. The plausibility of a planetary-scale 'tipping point' highlights the need to improve biological forecasting by detecting early warning signs of critical transitions on global as well as local scales, and by detecting feedbacks that promote such transitions. It is also necessary to address root causes of how humans are forcing biological changes.
View details for DOI 10.1038/nature11018
View details for Web of Science ID 000304854000026
View details for PubMedID 22678279
Ancient DNA Assessment of Tiger Salamander Population in Yellowstone National Park
2012; 7 (3)
Recent data indicates that blotched tiger salamanders (Ambystoma tigrinum melanostictum) in northern regions of Yellowstone National Park are declining due to climate-related habitat changes. In this study, we used ancient and modern mitochondrial haplotype diversity to model the effective size of this amphibian population through recent geological time and to assess past responses to climatic changes in the region. Using subfossils collected from a cave in northern Yellowstone, we analyzed >700 base pairs of mitochondrial sequence from 16 samples ranging in age from 100 to 3300 years old and found that all shared an identical haplotype. Although mitochondrial diversity was extremely low within the living population, we still were able to detect geographic subdivision within the local area. Using serial coalescent modelling with Bayesian priors from both modern and ancient genetic data we simulated a range of probable population sizes and mutation rates through time. Our simulations suggest that regional mitochondrial diversity has remained relatively constant even through climatic fluctuations of recent millennia.
View details for DOI 10.1371/journal.pone.0032763
View details for Web of Science ID 000302381500040
View details for PubMedID 22427878
Genetic variation over 10 000 years in Ctenomys: comparative phylochronology provides a temporal perspective on rarity, environmental change and demography
2011; 20 (22): 4592-4605
An understanding of how ecological traits influence past species response to environmental change can aid our future predictions of species persistence. We used ancient DNA and serial coalescent modelling in a hypothesis-testing framework to reveal differences in temporal genetic variation over 10,000 years for two species of subterranean rodents that currently differ in rarity (abundance, range size and habitat specificity) and mating system, but that reside in the same volcanically active region. Comparative phylochronologic analyses indicated little genetic change and suggest genetic stability in the solitary widespread Ctenomys haigi over thousands of years. In contrast, we found a pattern of haplotypic turnover in the rare and currently endangered Ctenomys sociabilis. Serial coalescent modelling indicated that the best-fit models of microevolutionary change included gene flow between isolated populations for this species. Although C. haigi and C. sociabilis are congeners that share many life history traits, they have behavioural, habitat-preference and population-size differences that may have resulted in contrasting patterns of temporal variation during periods of environmental change.
View details for DOI 10.1111/j.1365-294X.2011.05295.x
View details for Web of Science ID 000297414200003
View details for PubMedID 22008209
- Predicting small-mammal responses to climatic warming: autecology, geographic range, and the Holocene fossil record GLOBAL CHANGE BIOLOGY 2011; 17 (10): 3019-3034
HIGH LEVELS OF GENE FLOW IN THE CALIFORNIA VOLE (MICROTUS CALIFORNICUS) ARE CONSISTENT ACROSS SPATIAL SCALES
WESTERN NORTH AMERICAN NATURALIST
2010; 70 (3): 296-311
View details for Web of Science ID 000284435700003
Small mammal diversity loss in response to late-Pleistocene climatic change
2010; 465 (7299): 771-U5
Communities have been shaped in numerous ways by past climatic change; this process continues today. At the end of the Pleistocene epoch about 11,700 years ago, North American communities were substantially altered by the interplay of two events. The climate shifted from the cold, arid Last Glacial Maximum to the warm, mesic Holocene interglacial, causing many mammal species to shift their geographic distributions substantially. Populations were further stressed as humans arrived on the continent. The resulting megafaunal extinction event, in which 70 of the roughly 220 largest mammals in North America (32%) became extinct, has received much attention. However, responses of small mammals to events at the end of the Pleistocene have been much less studied, despite the sensitivity of these animals to current and future environmental change. Here we examine community changes in small mammals in northern California during the last 'natural' global warming event at the Pleistocene-Holocene transition and show that even though no small mammals in the local community became extinct, species losses and gains, combined with changes in abundance, caused declines in both the evenness and richness of communities. Modern mammalian communities are thus depauperate not only as a result of megafaunal extinctions at the end of the Pleistocene but also because of diversity loss among small mammals. Our results suggest that across future landscapes there will be some unanticipated effects of global change on diversity: restructuring of small mammal communities, significant loss of richness, and perhaps the rising dominance of native 'weedy' species.
View details for DOI 10.1038/nature09077
View details for Web of Science ID 000278551800043
View details for PubMedID 20495547
Dispersal provided resilience to range collapse in a marine mammal: insights from the past to inform conservation biology
2010; 19 (12): 2418-2429
Population loss is often a harbinger of species extinction, but few opportunities exist to follow a species' demography and genetics through both time and space while this occurs. Previous research has shown that the northern fur seal (Callorhinus ursinus) was extirpated from most of its range over the past 200-800 years and that some of the extirpated populations had unique life history strategies. In this study, widespread availability of subfossils in the eastern Pacific allowed us to examine temporal changes in spatial genetic structure during massive population range contraction and partial recovery. We sequenced the mitochondrial control region from 40 ancient and 365 modern samples and analyzed them through extensive simulations within a serial Approximate Bayesian Computation framework. These analyses suggest that the species maintained a high abundance, probably in subarctic refugia, that dispersal rates are likely 85% per generation into new breeding colonies, and that population structure was not higher in the past. Despite substantial loss of breeding range, this species' high dispersal rates and refugia appear to have prevented a loss of genetic diversity. High dispersal rates also suggest that previous evidence for divergent life history strategies in ancient populations likely resulted from behavioral plasticity. Our results support the proposal that panmictic, or nearly panmictic, species with large ranges will be more resilient to future disturbance and environmental change. When appropriately verified, evidence of low population structure can be powerful information for conservation decision-making.
View details for DOI 10.1111/j.1365-294X.2010.04671.x
View details for Web of Science ID 000278624000006
View details for PubMedID 20497323
- Isotopes reveal limited effects of middle Pleistocene climate change on the ecology of mid-sized mammals QUATERNARY INTERNATIONAL 2010; 217 (1-2): 43-52
Developmental dynamics of Ambystoma tigrinum in a changing landscape.
2010; 10: 10-?
Loss of pond habitat is catastrophic to aquatic larval amphibians, but even reduction in the amount of time a breeding site holds water (hydroperiod) can influence amphibian development and limit reproductive success. Using the landscape variation of a glacial valley in the Greater Yellowstone Ecosystem as the context for a natural experiment, we examined variation in growth pattern and life history of the salamander Ambystoma tigrinum melanostictum and determined how these developmental characteristics varied with hydroperiod over several summers.In ponds that dried early in the season, maximum larval size was reduced relative to the sizes achieved in permanent ponds. Ephemeral ponds were associated with early metamorphosis at small body sizes, while permanent ponds facilitated longer larval periods and later metamorphosis. Paedomorphosis resulted from indefinite metamorphic postponement, and was identified only in the most permanent environments. Patterns of growth and allometry were similar between ponds with different hydroperiods, but considerable life history variation was derived from modulating the timing of and size at metamorphosis. Considering maximum rates of growth and inferring the minimum size at metamorphosis across 25 ponds over the course of three years, we calculated that hydroperiods longer than three months are necessary to support these populations through metamorphosis and/or reproductive maturity.Landscape heterogeneity fosters life history variation in this natural population. Modulation of the complex ambystomatid life cycle allows this species to survive in unpredictable environments, but current trends towards rapid pond drying will promote metamorphosis at smaller sizes and could eliminate the paedomorphic phenotype from this region. Metamorphosis at small size is has been linked to altered fitness traits, including reduced survival and fecundity. Thus, widespread environmental truncation of larval periods may lead to decreased population persistence. We found that the hydroperiods of many ponds in this region are now shorter than the developmental period required for larvae to reach the minimum size for metamorphosis; these locations serve as reproductive sinks that may be detrimental for persistence of the species in the region.
View details for DOI 10.1186/1472-6785-10-10
View details for PubMedID 20361876
Source-sink dynamics structure a common montane mammal
2009; 18 (23): 4775-4789
Assessing the relative role of evolutionary processes on genetic diversity is critical for understanding species response to climatic change. However, many processes, independent of climate, can lead to the same genetic pattern. Because effective population size and gene flow are affected directly by abundance and dispersal, population ecology has the potential to profoundly influence patterns of genetic variation over microevolutionary timescales. Here, we use aDNA data and simulations to explore the influence of population ecology and Holocene climate change on genetic diversity of the Uinta ground squirrel (Spermophilus armatus). We examined phylochronology from three modern and two ancient populations spanning the climate transitions of the last 3000 years. Population genetic analyses based on summary statistics suggest that changes in genetic diversity and structure coincided with the Medieval Warm Period (MWP), c. 1000 years ago. Serial coalescent simulations allowed us to move beyond correlation with climate to statistically compare the likelihoods of alternative population histories given the observed data. The data best fit source-sink models that include large, mid-elevation populations that exchange many migrants and small populations at the elevational extremes. While the MWP is likely to have reduced genetic diversity, our model-testing approach revealed that MWP-driven changes in genetic structure were not better supported for the range of models explored. Our results point to the importance of species ecology in understanding responses to climate, and showcase the use of ancient genetic data and simulation-based inference for unraveling the relative roles of microevolutionary processes.
View details for DOI 10.1111/j.1365-294X.2009.04382.x
View details for Web of Science ID 000271904400004
View details for PubMedID 19863718
Niche conservatism above the species level
Arthur M Sackler Colloquium of the National-Academy-of-Sciences on Biogeography, Changing Climates and Niche Evolution
NATL ACAD SCIENCES. 2009: 19707–19714
Traits that enable species to persist in ecological environments are often maintained over time, a phenomenon known as niche conservatism. Here we argue that ecological niches function at levels above species, notably at the level of genus for mammals, and that niche conservatism is also evident above the species level. Using the proxy of geographic range size, we explore changes in the realized niche of North American mammalian genera and families across the major climatic transition represented by the last glacial-interglacial transition. We calculate the mean and variance of range size for extant mammalian genera and families, rank them by range size, and estimate the change in range size and rank during the late Pleistocene and late Holocene. We demonstrate that range size at the genus and family levels was surprisingly constant over this period despite range shifts and extinctions of species within the clades. We suggest that underlying controls on niche conservatism may be different at these higher taxonomic levels than at the species level. Niche conservatism at higher levels seems primarily controlled by intrinsic life history traits, whereas niche conservatism at the species level may reflect underlying environmental controls. These results highlight the critical importance of conserving the biodiversity of mammals at the genus level and of maintaining an adequate species pool within genera.
View details for DOI 10.1073/pnas.0901648106
View details for Web of Science ID 000271907100012
View details for PubMedID 19897730
- Biogeography, changing climates, and niche evolution PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 2009; 106: 19631-19636
Do complex population histories drive higher estimates of substitution rate in phylogenetic reconstructions?
2009; 18 (21): 4341-4343
Our curiosity about biodiversity compels us to reconstruct the evolutionary past of species. Molecular evolutionary theory now allows parameterization of mathematically sophisticated and detailed models of DNA evolution, which have resulted in a wealth of phylogenetic histories. But reconstructing how species and population histories have played out is critically dependent on the assumptions we make, such as the clock-like accumulation of genetic differences over time and the rate of accumulation of such differences. An important stumbling block in the reconstruction of evolutionary history has been the discordance in estimates of substitution rate between phylogenetic and pedigree-based studies. Ancient genetic data recovered directly from the past are intermediate in time scale between phylogenetics-based and pedigree-based calibrations of substitution rate. Recent analyses of such ancient genetic data suggest that substitution rates are closer to the higher, pedigree-based estimates. In this issue, Navascués & Emerson (2009) model genetic data from contemporary and ancient populations that deviate from a simple demographic history (including changes in population size and structure) using serial coalescent simulations. Furthermore, they show that when these data are used for calibration, we are likely to arrive at upwardly biased estimates of mutation rate.
View details for DOI 10.1111/j.1365-294X.2009.04334.x
View details for Web of Science ID 000270829700001
View details for PubMedID 19845859
PHYLOGEOGRAPHY OF MICROTUS LONGICAUDUS IN THE TECTONICALLY AND GLACIALLY DYNAMIC CENTRAL ROCKY MOUNTAINS
JOURNAL OF MAMMALOGY
2009; 90 (3): 571-584
View details for Web of Science ID 000266952900004
Using phylochronology to reveal cryptic population histories: review and synthesis of 29 ancient DNA studies
2009; 18 (7): 1310-1330
The evolutionary history of a population involves changes in size, movements and selection pressures through time. Reconstruction of population history based on modern genetic data tends to be averaged over time or to be biased by generally reflecting only recent or extreme events, leaving many population historic processes undetected. Temporal genetic data present opportunities to reveal more complex population histories and provide important insights into what processes have influenced modern genetic diversity. Here we provide a synopsis of methods available for the analysis of ancient genetic data. We review 29 ancient DNA studies, summarizing the analytical methods and general conclusions for each study. Using the serial coalescent and a model-testing approach, we then re-analyse data from two species represented by these data sets in a common interpretive framework. Our analyses show that phylochronologic data can reveal more about population history than modern data alone, thus revealing 'cryptic' population processes, and enable us to determine whether simple or complex models best explain the data. Our re-analyses point to the need for novel methods that consider gene flow, multiple populations and population size in reconstruction of population history. We conclude that population genetic samples over large temporal and geographical scales, when analysed using more complex models and the serial coalescent, are critical to understand past population dynamics and provide important tools for reconstructing the evolutionary process.
View details for DOI 10.1111/j.1365-294X.2009.04092.x
View details for Web of Science ID 000264373900002
View details for PubMedID 19281471
- Mammalian Response to Cenozoic Climatic Change ANNUAL REVIEW OF EARTH AND PLANETARY SCIENCES 2009; 37: 181-208
- Stable isotopes reveal seasonal competition for resources between late Pleistocene bison (Bison) and horse (Equus) from Rancho La Brea, southern California PALAEOGEOGRAPHY PALAEOCLIMATOLOGY PALAEOECOLOGY 2009; 271 (1-2): 153-160
Climatic change and wetland desiccation cause amphibian decline in Yellowstone National Park
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
2008; 105 (44): 16988-16993
Amphibians are a bellwether for environmental degradation, even in natural ecosystems such as Yellowstone National Park in the western United States, where species have been actively protected longer than anywhere else on Earth. We document that recent climatic warming and resultant wetland desiccation are causing severe declines in 4 once-common amphibian species native to Yellowstone. Climate monitoring over 6 decades, remote sensing, and repeated surveys of 49 ponds indicate that decreasing annual precipitation and increasing temperatures during the warmest months of the year have significantly altered the landscape and the local biological communities. Drought is now more common and more severe than at any time in the past century. Compared with 16 years ago, the number of permanently dry ponds in northern Yellowstone has increased 4-fold. Of the ponds that remain, the proportion supporting amphibians has declined significantly, as has the number of species found in each location. Our results indicate that climatic warming already has disrupted one of the best-protected ecosystems on our planet and that current assessments of species' vulnerability do not adequately consider such impacts.
View details for DOI 10.1073/pnas.0809090105
View details for Web of Science ID 000260913800036
View details for PubMedID 18955700
Fire and ice: genetic structure of the Uinta ground squirrel (Spermophilus armatus) across the Yellowstone hotspot
2008; 17 (7): 1776-1788
The range of the Uinta ground squirrel, Spermophilus armatus, is centred over one of the most tectonically active regions today, the Yellowstone hotspot. We document the role of Quaternary tectonic and climatic history on the genetic structure of this species by screening museum and extant individuals throughout its range. Phylogeographic, divergence time, and demographic analyses of partial mitochondrial cytochrome b and control region DNA sequences yield insight into the cadence of evolution across three spatiotemporal scales: (i) a relatively deep intraspecific divergence of S. armatus into three lineages coincident with the last major volcanic eruption in the region and maintained by the Snake River Plain; (ii) demographic expansion in two lineages corresponding to the time of last deglaciation of the region; and (iii) a recent (< 50 years) local extinction of the third lineage coincident with climatic change and conversion of habitat for agricultural purposes in eastern Idaho. Beyond these inferences, our study highlights the unique value of museum material to phylogeography, and shows that small mammal recolonization of previously glaciated montane 'islands' differs from northward postglacial expansion observed in areas previously covered by continental ice sheets. Montane 'islands' may harbour high genetic diversity because of admixture and recurrent expansion/extinction.
View details for DOI 10.1111/j.1365-294X.2008.03671.x
View details for Web of Science ID 000254384700014
View details for PubMedID 18284571
- The role of molecular genetics in sculpting the future of integrative biogeography PROGRESS IN PHYSICAL GEOGRAPHY 2008; 32 (2): 173-202
- Environmental influences on spatial and temporal patterns of body-size variation in California ground squirrels (Spermophilus beecheyi) JOURNAL OF BIOGEOGRAPHY 2008; 35 (4): 602-613
Determining landscape use of Holocene mammals using strontium isotopes
2007; 153 (4): 943-950
The use of the landscape by animals is predicted to be a function of their body size. However, empirical data relating these two variables from an array of body sizes within a single mammalian community are scarce. We tested this prediction by assessing landscape use of mammals by analyzing strontium (Sr) isotope signatures found in mammalian hard tissues representing a 3,000-year record. We examined: (1) the Sr-determined landscape area of small (approximately 100 g), medium (approximately 1,500 g) and large (approximately 100,000 g) mammals, and; (2) whether the area used by these mammals varied during periods of environmental change. Strontium isotope values were obtained from 46 specimens from the Holocene paleontological deposits of Lamar Cave and Waterfall Locality in Wyoming, USA, as well as from 13 modern ungulate specimens from the same area. Our data indicate that medium- and large-sized species use larger percentages of the landscape than do species of small body size. The isotope values for specimens from each of the paleontological sites are similar across all stratigraphic levels, suggesting no change in home range over the last 3,000 years, even though climate is known to have fluctuated at these sites over this time period. Further, our study verifies that the fossil localities represent the local community. Where bedrock geology is appropriate, the use of strontium isotope analyses provides a valuable tool for discerning landscape use by vertebrate communities, an important though generally difficult aspect of an ancient species niche to identify.
View details for DOI 10.1007/s00442-007-0779-y
View details for Web of Science ID 000249407000015
View details for PubMedID 17593400
The shifting baseline of northern fur seal ecology in the northeast Pacific Ocean
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
2007; 104 (23): 9709-9714
Historical data provide a baseline against which to judge the significance of recent ecological shifts and guide conservation strategies, especially for species decimated by pre-20th century harvesting. Northern fur seals (NFS; Callorhinus ursinus) are a common pinniped species in archaeological sites from southern California to the Aleutian Islands, yet today they breed almost exclusively on offshore islands at high latitudes. Harvest profiles from archaeological sites contain many unweaned pups, confirming the presence of temperate-latitude breeding colonies in California, the Pacific Northwest, and the eastern Aleutian Islands. Isotopic results suggest that prehistoric NFS fed offshore across their entire range, that California populations were distinct from populations to the north, and that populations breeding at temperate latitudes in the past used a different reproductive strategy than modern populations. The extinction of temperate-latitude breeding populations was asynchronous geographically. In southern California, the Pacific Northwest, and the eastern Aleutians, NFS remained abundant in the archaeological record up to the historical period approximately 200 years B.P.; thus their regional collapse is plausibly attributed to historical hunting or some other anthropogenic ecosystem disturbance. In contrast, NFS populations in central and northern California collapsed at approximately 800 years B.P., long before European contact. The relative roles of human hunting versus climatic factors in explaining this ecological shift are unclear, as more paleoclimate information is needed from the coastal zone.
View details for DOI 10.1073/pnas.0610986104
View details for Web of Science ID 000247114100031
View details for PubMedID 17526720
- Non-random patterns in the Yellowstone ecosystem: inferences from mammalian body size, order and biogeographical affinity GLOBAL ECOLOGY AND BIOGEOGRAPHY 2007; 16 (2): 139-148
Radiocarbon dates from the pleistocene fossil deposits of Samwel Cave, Shasta County, California, USA
2007; 49 (1): 117-121
View details for Web of Science ID 000246375900008
Bayesian estimation of the timing and severity of a population bottleneck from ancient DNA
2006; 2 (4): 451-460
In this first application of the approximate Bayesian computation approach using the serial coalescent, we demonstrated the estimation of historical demographic parameters from ancient DNA. We estimated the timing and severity of a population bottleneck in an endemic subterranean rodent, Ctenomys sociabilis, over the last 10,000 y from two cave sites in northern Patagonia, Argentina. Understanding population bottlenecks is important in both conservation and evolutionary biology. Conservation implications include the maintenance of genetic variation, inbreeding, fixation of mildly deleterious alleles, and loss of adaptive potential. Evolutionary processes are impacted because of the influence of small populations in founder effects and speciation. We found a decrease from a female effective population size of 95,231 to less than 300 females at 2,890 y before present: a 99.7% decline. Our study demonstrates the persistence of a species depauperate in genetic diversity for at least 2,000 y and has implications for modes of speciation in the incredibly diverse rodent genus Ctenomys. Our approach shows promise for determining demographic parameters for other species with ancient and historic samples and demonstrates the power of such an approach using ancient DNA.
View details for DOI 10.1371/journal.pgen.0020059
View details for Web of Science ID 000239494500008
View details for PubMedID 16636697
Ancient DNA reveals Holocene loss of genetic diversity in a South American rodent
2005; 1 (4): 423-426
Understanding how animal populations have evolved in response to palaeoenvironmental conditions is essential for predicting the impact of future environmental change on current biodiversity. Analyses of ancient DNA provide a unique opportunity to track population responses to prehistoric environments. We explored the effects of palaeoenvironmental change on the colonial tuco-tuco (Ctenomys sociabilis), a highly endemic species of Patagonian rodent that is currently listed as threatened by the IUCN. By combining surveys of modern genetic variation from throughout this species' current geographic range with analyses of DNA samples from fossil material dating back to 10,000 ybp, we demonstrate a striking decline in genetic diversity that is concordant with environmental events in the study region. Our results highlight the importance of non-anthropogenic factors in loss of diversity, including reductions in smaller mammals such as rodents.
View details for DOI 10.1098/rsbl.2005.0354
View details for Web of Science ID 000233911600012
View details for PubMedID 17148223
Community inertia of quaternary small mammal assemblages in North America
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
2005; 102 (46): 16701-16706
One of the longest running debates in ecology is whether chance or determinism structures biotic communities, and this question is often studied by looking for the presence or absence of community inertia (lack of change) over time or space. Results have been equivocal. We adopted three tactics for a fresh approach: (i) allowing the answer to vary with the geographic, temporal, and taxonomic scale of study, (ii) using appropriate reference points for the amount of inertia in random biological systems, and (iii) using a robust approach for measurement of inertia. We examined fossil assemblages of mammalian communities across almost 1,000,000 years and at sites spanning approximately 3,500 km. We showed that in general there is good evidence for inertia but that the results change in a quantifiable fashion with taxonomic, spatial, and temporal scales. By using neutral theory we place a reference point on the degree of inertia and demonstrate that empirical mammalian communities show greater inertia than neutral communities over time scales >3,000 year. Although our results do not specifically reveal mechanism, they emphasize that deterministic forces are at work in structuring communities over millennia.
View details for DOI 10.1073/pnas.0504225102
View details for Web of Science ID 000233462900033
View details for PubMedID 16260748
Detecting past population bottlenecks using temporal genetic data
2005; 14 (10): 2915-2922
Population bottlenecks wield a powerful influence on the evolution of species and populations by reducing the repertoire of responses available for stochastic environmental events. Although modern contractions of wild populations due to human-related impacts have been documented globally, discerning historic bottlenecks for all but the most recent and severe events remains a serious challenge. Genetic samples dating to different points in time may provide a solution in some cases. We conducted serial coalescent simulations to assess the extent to which temporal genetic data are informative regarding population bottlenecks. These simulations demonstrated that the power to reject a constant population size hypothesis using both ancient and modern genetic data is almost always higher than that based solely on modern data. The difference in power between the modern and temporal DNA approaches depends significantly on effective population size and bottleneck intensity and less significantly on sample size. The temporal approach provides more power in cases of genetic recovery (via migration) from a bottleneck than in cases of demographic recovery (via population growth). Choice of genetic region is critical, as mutation rate heavily influences the extent to which temporal sampling yields novel information regarding the demographic history of populations.
View details for DOI 10.1111/j.1365-294X.2005.02586.x
View details for Web of Science ID 000231223000002
View details for PubMedID 16101762
Serial SimCoal: A population genetics model for data from multiple populations and points in time
2005; 21 (8): 1733-1734
We present Serial SimCoal, a program that models population genetic data from multiple time points, as with ancient DNA data. An extension of SIMCOAL, it also allows simultaneous modeling of complex demographic histories, and migration between multiple populations. Further, we incorporate a statistical package to calculate relevant summary statistics, which, for the first time allows users to investigate the statistical power provided by, conduct hypothesis-testing with, and explore sample size limitations of ancient DNA data.Source code and Windows/Mac executables at http://firstname.lastname@example.org.
View details for DOI 10.1093/bioinformatics/bti154
View details for Web of Science ID 000228401800075
View details for PubMedID 15564305
Temporal response of the tiger salamander (Ambystoma tigrinum) to 3,000 years of climatic variation.
2005; 5: 7-?
Amphibians are sensitive indicators of environmental conditions and show measurable responses, such as changes in phenology, abundance and range limits to local changes in precipitation and temperature regimes. Amphibians offer unique opportunities to study the important ecological and evolutionary implications of responses in life history characteristics to climatic change. We analyzed a late-Holocene fossil record of the Tiger Salamander (Ambystoma tigrinum) for evidence of population-level changes in body size and paedomorphosis to climatic change over the last 3000 years.We found a significant difference in body size index between paedomorphic and metamorphic individuals during the time interval dominated by the Medieval Warm Period. There is a consistent ratio of paedomorphic to metamorphic specimens through the entire 3000 years, demonstrating that not all life history characteristics of the population were significantly altered by changes in climate on this timescale.The fossil record of Ambystoma tigrinum we used spans an ecologically relevant timescale appropriate for understanding population and community response to projected climatic change. The population-level responses we documented are concordant with expectations based on modern environmental studies, and yield insight into population-level patterns across hundreds of generations, especially the independence of different life history characteristics. These conclusions lead us to offer general predictions about the future response of this species based on likely scenarios of climatic warming in the Rocky Mountain region.
View details for PubMedID 16159383
Studying the effect of environmental change on biotic evolution: past genetic contributions, current work and future directions
PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY A-MATHEMATICAL PHYSICAL AND ENGINEERING SCIENCES
2004; 362 (1825): 2795-2820
Evolutionary geneticists currently face a major scientific opportunity when integrating across the rapidly increasing amount of genetic data and existing biological scenarios based on ecology, fossils or climate models. Although genetic data acquisition and analysis have improved tremendously, several limitations remain. Here, we discuss the feedback between history and genetic variation in the face of environmental change with increasing taxonomic and temporal scale, as well as the major challenges that lie ahead. In particular, we focus on recent developments in two promising genetic methods, those of 'phylochronology' and 'molecular clocks'. With the advent of ancient DNA techniques, we can now directly sample the recent past. We illustrate this amazing and largely untapped utility of ancient DNA extracted from accurately dated localities with documented environmental changes. Innovative statistical analyses of these genetic data expose the direct effect of recent environmental change on genetic endurance, or maintenance of genetic variation. The 'molecular clock' (assumption of a linear relationship between genetic distance and evolutionary time) has been used extensively in phylogenetic studies to infer time and correlation between lineage divergence time and concurrent environmental change. Several studies at both population and species scale support a persuasive relationship between particular perturbation events and time of biotic divergence. However, we are still a way from gleaning an overall pattern to this relationship, which is a prerequisite to ultimately understanding the mechanisms by which past environments have shaped the evolutionary trajectory. Current obstacles include as-yet undecided reasons behind the frequent discrepancy between molecular and fossil time estimates, and the frequent lack of consideration of extensive confidence intervals around time estimates. We suggest that use and interpretation of both ancient DNA and molecular clocks is most effective when results are synthesized with palaeontological (fossil) and ecological (life history) information.
View details for DOI 10.1098/rsta.2004.1465
View details for Web of Science ID 000225645200014
View details for PubMedID 15539371
Genetic response to climatic change: Insights from ancient DNA and phylochronology
2004; 2 (10): 1600-1609
Understanding how climatic change impacts biological diversity is critical to conservation. Yet despite demonstrated effects of climatic perturbation on geographic ranges and population persistence, surprisingly little is known of the genetic response of species. Even less is known over ecologically long time scales pertinent to understanding the interplay between microevolution and environmental change. Here, we present a study of population variation by directly tracking genetic change and population size in two geographically widespread mammal species (Microtus montanus and Thomomys talpoides) during late-Holocene climatic change. We use ancient DNA to compare two independent estimates of population size (ecological and genetic) and corroborate our results with gene diversity and serial coalescent simulations. Our data and analyses indicate that, with population size decreasing at times of climatic change, some species will exhibit declining gene diversity as expected from simple population genetic models, whereas others will not. While our results could be consistent with selection, independent lines of evidence implicate differences in gene flow, which depends on the life history strategy of species.
View details for DOI 10.1371/journal.pbio.0020290
View details for Web of Science ID 000224737100016
View details for PubMedID 15361933
Similarities in body size distributions of small-bodied flying vertebrates
EVOLUTIONARY ECOLOGY RESEARCH
2004; 6 (6): 783-797
View details for Web of Science ID 000223973000001
Error in estimation of rate and time inferred from the early amniote fossil record and avian molecular clocks
JOURNAL OF MOLECULAR EVOLUTION
2004; 59 (2): 267-276
The best reconstructions of the history of life will use both molecular time estimates and fossil data. Errors in molecular rate estimation typically are unaccounted for and no attempts have been made to quantify this uncertainty comprehensively. Here, focus is primarily on fossil calibration error because this error is least well understood and nearly universally disregarded. Our quantification of errors in the synapsid-diapsid calibration illustrates that although some error can derive from geological dating of sedimentary rocks, the absence of good stem fossils makes phylogenetic error the most critical. We therefore propose the use of calibration ages that are based on the first undisputed synapsid and diapsid. This approach yields minimum age estimates and standard errors of 306.1 +/- 8.5 MYR for the divergence leading to birds and mammals. Because this upper bound overlaps with the recent use of 310 MYR, we do not support the notion that several metazoan divergence times are significantly overestimated because of serious miscalibration (sensuLee 1999). However, the propagation of relevant errors reduces the statistical significance of the pre-K-T boundary diversification of many bird lineages despite retaining similar point time estimates. Our results demand renewed investigation into suitable loci and fossil calibrations for constructing evolutionary timescales.
View details for DOI 10.1007/s00239-004-2624-9
View details for Web of Science ID 000223424800011
View details for PubMedID 15486700
Similarity of mammalian body size across the taxonomic hierarchy and across space and time
2004; 163 (5): 672-691
Although it is commonly assumed that closely related animals are similar in body size, the degree of similarity has not been examined across the taxonomic hierarchy. Moreover, little is known about the variation or consistency of body size patterns across geographic space or evolutionary time. Here, we draw from a data set of terrestrial, nonvolant mammals to quantify and compare patterns across the body size spectrum, the taxonomic hierarchy, continental space, and evolutionary time. We employ a variety of statistical techniques including "sib-sib" regression, phylogenetic autocorrelation, and nested ANOVA. We find an extremely high resemblance (heritability) of size among congeneric species for mammals over approximately 18 g; the result is consistent across the size spectrum. However, there is no significant relationship among the body sizes of congeneric species for mammals under approximately 18 g. We suspect that life-history and ecological parameters are so tightly constrained by allometry at diminutive size that animals can only adapt to novel ecological conditions by modifying body size. The overall distributions of size for each continental fauna and for the most diverse orders are quantitatively similar for North America, South America, and Africa, despite virtually no overlap in species composition. Differences in ordinal composition appear to account for quantitative differences between continents. For most mammalian orders, body size is highly conserved, although there is extensive overlap at all levels of the taxonomic hierarchy. The body size distribution for terrestrial mammals apparently was established early in the Tertiary, and it has remained remarkably constant over the past 50 Ma and across the major continents. Lineages have diversified in size to exploit environmental opportunities but only within limits set by allometric, ecological, and evolutionary constraints.
View details for Web of Science ID 000221651400005
View details for PubMedID 15122486
Calibration and error in placental molecular clocks: A conservative approach using the cetartiodactyl fossil record
JOURNAL OF HEREDITY
2004; 95 (3): 200-208
The nature of the molecular and fossil record and their limitations must be ascertained in order to gain the most precise and accurate evolutionary timescale using genetic information. Yet the majority of such timescales are based on point estimates using fossils or the molecular clock. Here we document from the primary literature minimum and maximum fossil age estimates of the divergence of whales from artiodactyls, a commonly used anchor point for calibrating both mitogenomic and nucleogenomic placental timescales. We applied these reestimates to the most recently established placental timescale based on mitochondrial rRNA and several nuclear loci, and present an attempt to account for both genetic and fossil uncertainty. Our results indicate that disregard for fossil calibration error may inflate the power of the molecular clock when testing the time of ordinal diversification in context with the K-T boundary. However, the early history of placentals, including their superordinal diversification, remained in the Cretaceous despite a conservative approach. Our conclusions need corroboration across other frequently used fossil anchor points, but also with more genetic partitions on the linear relationship between molecular substitutions and geologic time.
View details for DOI 10.1093/jhered/esh045
View details for Web of Science ID 000222399600003
View details for PubMedID 15220386
- Thermodynamic and metabolic effects on the scaling of production and population energy use ECOLOGY LETTERS 2003; 6 (11): 990-995
The interface of paleontology and mammalogy: Past, present, and future
JOURNAL OF MAMMALOGY
2003; 84 (2): 347-353
View details for Web of Science ID 000183284500001
Ancient DNA evidence of prolonged population persistence with negligible genetic diversity in an endemic tuco-tuco (Ctenomys sociabilis)
JOURNAL OF MAMMALOGY
2003; 84 (2): 403-417
View details for Web of Science ID 000183284500005
Mammalian response to global warming on varied temporal scales
JOURNAL OF MAMMALOGY
2003; 84 (2): 354-368
View details for Web of Science ID 000183284500002
Mapping the origin of faunal assemblages using strontium isotopes
2003; 29 (2): 197-204
View details for Web of Science ID 000183070500005
Temperate terrestrial vertebrate faunas in North and South America: Interplay of ecology, evolution, and geography with biodiversity
2001; 15 (3): 658-674
View details for Web of Science ID 000169226000014
Spatial and temporal patterns of species diversity in montane mammal communities of western North America
EVOLUTIONARY ECOLOGY RESEARCH
2001; 3 (4): 477-486
View details for Web of Science ID 000168501000008
Fidelity of terrestrial vertebrate fossils to a modern ecosystem
PALAEOGEOGRAPHY PALAEOCLIMATOLOGY PALAEOECOLOGY
1999; 149 (1-4): 389-409
View details for Web of Science ID 000081023500028
A genetic record of population isolation in pocket gophers during Holocene climatic change
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
1998; 95 (12): 6893-6896
A long-standing question in Quaternary paleontology is whether climate-induced, population-level phenotypic change is a result of large-scale migration or evolution in isolation. To directly measure genetic variation through time, ancient DNA and morphologic variation was measured over 2,400 years in a Holocene sequence of pocket gophers (Thomomys talpoides) from Lamar Cave, Yellowstone National Park, Wyoming. Ancient specimens and modern samples collected near Lamar Cave share mitochondrial cytochrome b sequences that are absent from adjacent localities, suggesting that the population was isolated for the entire period. In contrast, diastemal length, a morphologic character correlated with body size and nutritional level, changed predictably in response to climatic change. Our results demonstrate that small mammal populations can experience the long-term isolation assumed by many theoretical models of microevolutionary change.
View details for Web of Science ID 000074131900059
View details for PubMedID 9618509