Academic Appointments


Administrative Appointments


  • Faculty Director, Jasper Ridge Biological Preserve (2016 - 2023)

Professional Education


  • 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
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 species. 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, and increasingly important to understand the impacts of the Anthropocene.

Projects


  • Defining the Anthropocene, Stanford University (1/2018 - Present)

    Jasper Ridge has an extraordinary record of sediments representing the past century and more. These sediments are being queried for chemical, physical and biotic evidence of humanity's impact on the environment.

    Location

    Jasper Ridge Biological Preserve

  • The Insect Apocalypse, Stanford University

    Location

    Jasper Ridge Biological Preserve

  • Food webs from feces, soil, and cameras

    Location

    Jasper Ridge Biological Preserve

  • Reverse spillover: Animals are impacted by human-shed microbes

    Location

    Jasper Ridge Biological Preserve

  • Wild and captive tiger genomic diversity

    Location

    stanford university

2023-24 Courses


Stanford Advisees


Graduate and Fellowship Programs


  • Biology (School of Humanities and Sciences) (Phd Program)

All Publications


  • Impressive pan-genomic diversity of E. coli from a wild animal community near urban development reflects human impacts. iScience Lagerstrom, K. M., Scales, N. C., Hadly, E. A. 2024; 27 (3): 109072

    Abstract

    Human and domesticated animal waste infiltrates global freshwater, terrestrial, and marine environments, widely disseminating fecal microbes, antibiotics, and other chemical pollutants. Emerging evidence suggests that guts of wild animals are being invaded by our microbes, including Escherichia coli, which face anthropogenic selective pressures to gain antimicrobial resistance (AMR) and increase virulence. However, wild animal sources remain starkly under-represented among genomic sequence repositories. We sequenced whole genomes of 145 E. coli isolates from 55 wild and 13 domestic animal fecal samples, averaging 2 (ranging 1-7) isolates per sample, on a preserve imbedded in a human-dominated landscape in California Bay Area, USA, to assess AMR, virulence, and pan-genomic diversity. With single nucleotide polymorphism analyses we predict potential transmission routes. We illustrate the usefulness of E. coli to aid our understanding of and ability to surveil the emergence of zoonotic pathogens created by the mixing of human and wild bacteria in the environment.

    View details for DOI 10.1016/j.isci.2024.109072

    View details for PubMedID 38375235

    View details for PubMedCentralID PMC10875580

  • Multiple invasion routes have led to the pervasive introduction of earthworms in North America. Nature ecology & evolution Mathieu, J., Reynolds, J. W., Fragoso, C., Hadly, E. 2024

    Abstract

    Soil-dwelling organisms play a key role in ecosystem functioning and the delivery of ecosystem services. As a consequence, soil taxa such as earthworms are iconic in good land management practices. However, their introduction in places where species did not co-evolve with them can trigger catastrophic changes. This issue has been largely ignored so far in nature management policies because of the positive image of soil taxa and the lack of knowledge of the magnitude of soil fauna introductions outside their native range. Here we address this gap with a large spatio-temporal database of introduced alien earthworms. We show that 70 alien earthworm species have colonized the North American continent. They have larger geographical ranges than native species and novel ecological functions, representing a serious threat to the biodiversity and functioning of native ecosystems. The probably continuous introduction of alien earthworms, from a variety of sources and introduction pathways, into many distant and often empty niches, contrasts with the classical patterns of invasions in most aboveground taxa. This suggests that earthworms, and probably other soil organisms, constitute a major but overlooked pool of invasive species that are not adequately managed by existing control and mitigation strategies.

    View details for DOI 10.1038/s41559-023-02310-7

    View details for PubMedID 38332024

    View details for PubMedCentralID 5376159

  • Exploring climate-induced sex-based differences in aquatic and terrestrial ecosystems to mitigate biodiversity loss. Nature communications Gissi, E., Schiebinger, L., Hadly, E. A., Crowder, L. B., Santoleri, R., Micheli, F. 2023; 14 (1): 4787

    View details for DOI 10.1038/s41467-023-40316-8

    View details for PubMedID 37587108

    View details for PubMedCentralID 5326506

  • Should We Bring Species Back From Extinction NATION Hysolli, E., Hadly, E. A., Sivas, D. A. 2023; 316 (12): 13-14
  • Under-Appreciated Phylogroup Diversity of Escherichia coli within and between Animals at the Urban-Wildland Interface. Applied and environmental microbiology Lagerstrom, K. M., Hadly, E. A. 2023: e0014223

    Abstract

    Wild animals have been implicated as reservoirs and even "melting pots" of pathogenic and antimicrobial-resistant bacteria of concern to human health. Though Escherichia coli is common among vertebrate guts and plays a role in the propagation of such genetic information, few studies have explored its diversity beyond humans nor the ecological factors that influence its diversity and distribution in wild animals. We characterized an average of 20 E. coli isolates per scat sample (n = 84) from a community of 14 wild and 3 domestic species. The phylogeny of E. coli comprises 8 phylogroups that are differentially associated with pathogenicity and antibiotic resistance, and we uncovered all of them in one small biological preserve surrounded by intense human activity. Challenging previous assumptions that a single isolate is representative of within-host phylogroup diversity, 57% of individual animals sampled carried multiple phylogroups simultaneously. Host species' phylogroup richness saturated at different levels across species and encapsulated vast within-sample and within-species variation, indicating that distribution patterns are influenced both by isolation source and laboratory sampling depth. Using ecological methods that ensure statistical relevance, we identify trends in phylogroup prevalence associated with host and environmental factors. The vast genetic diversity and broad distribution of E. coli in wildlife populations has implications for biodiversity conservation, agriculture, and public health, as well as for gauging unknown risks at the urban-wildland interface. We propose critical directions for future studies of the "wild side" of E. coli that will expand our understanding of its ecology and evolution beyond the human environment. IMPORTANCE To our knowledge, neither the phylogroup diversity of E. coli within individual wild animals nor that within an interacting multispecies community have previously been assessed. In doing so, we uncovered the globally known phylogroup diversity from an animal community on a preserve imbedded in a human-dominated landscape. We revealed that the phylogroup composition in domestic animals differed greatly from that in their wild counterparts, implying potential human impacts on the domestic animal gut. Significantly, many wild individuals hosted multiple phylogroups simultaneously, indicating the potential for strain-mixing and zoonotic spillback, especially as human encroachment into wildlands increases in the Anthropocene. We reason that due to extensive anthropogenic environmental contamination, wildlife is increasingly exposed to our waste, including E. coli and antibiotics. The gaps in the ecological and evolutionary understanding of E. coli thus necessitate a significant uptick in research to better understand human impacts on wildlife and the risk for zoonotic pathogen emergence.

    View details for DOI 10.1128/aem.00142-23

    View details for PubMedID 37191541

  • Witnessing history: comparison of a century of sedimentary and written records in a California protected area. Regional environmental change Scott Anderson, R., Allison Stegner, M., La Selle, S., Sherrod, B., Barnosky, A. D., Hadly, E. A. 2023; 23 (2): 65

    Abstract

    We use a combination of proxy records from a high-resolution analysis of sediments from Searsville Lake and adjacent Upper Lake Marsh and historical records to document over one and a half centuries of vegetation and socio-ecological change-relating to logging, agricultural land use change, dam construction, chemical applications, recreation, and other drivers-on the San Francisco Peninsula. A relatively open vegetation with minimal oak (Quercus) and coast redwood (Sequoia sempervirens) in the late 1850s reflects widespread logging and grazing during the nineteenth century. Forest and woodland expansion occurred in the early twentieth century, with forests composed of coast redwood and oak, among other taxa, as both logging and grazing declined. Invasive species include those associated with pasturage (Rume x, Plantago), landscape disturbance (Urtica, Amaranthaceae), planting for wood production and wind barriers (Eucalyptus), and agriculture. Agricultural species, including wheat, rye, and corn, were more common in the early twentieth century than subsequently. Wetland and aquatic pollen and fungal spores document a complex hydrological history, often associated with fluctuating water levels, application of algaecides, raising of Searsville Dam, and construction of a levee. By pairing the paleoecological and historical records of both lakes, we have been able to reconstruct the previously undocumented impacts of socio-ecological influences on this drainage, all of which overprinted known climate changes. Recognizing the ecological manifestations of these impacts puts into perspective the extent to which people have interacted with and transformed the environment in the transition into the Anthropocene.The online version contains supplementary material available at 10.1007/s10113-023-02056-9.

    View details for DOI 10.1007/s10113-023-02056-9

    View details for PubMedID 37125024

    View details for PubMedCentralID PMC10116087

  • The Searsville Lake Site (California, USA) as a candidate Global boundary Stratotype Section and Point for the Anthropocene series. The anthropocene review Stegner, M. A., Hadly, E. A., Barnosky, A. D., La Selle, S., Sherrod, B., Anderson, R. S., Redondo, S. A., Viteri, M. C., Weaver, K. L., Cundy, A. B., Gaca, P., Rose, N. L., Yang, H., Roberts, S. L., Hajdas, I., Black, B. A., Spanbauer, T. L. 2023; 10 (1): 116-145

    Abstract

    Cores from Searsville Lake within Stanford University's Jasper Ridge Biological Preserve, California, USA, are examined to identify a potential GSSP for the Anthropocene: core JRBP2018-VC01B (944.5 cm-long) and tightly correlated JRBP2018-VC01A (852.5 cm-long). Spanning from 1900 CE ± 3 years to 2018 CE, a secure chronology resolved to the sub-annual level allows detailed exploration of the Holocene-Anthropocene transition. We identify the primary GSSP marker as first appearance of 239,240Pu (372-374 cm) in JRBP2018-VC01B and designate the GSSP depth as the distinct boundary between wet and dry season at 366 cm (6 cm above the first sample containing 239,240Pu) and corresponding to October-December 1948 CE. This is consistent with a lag of 1-2 years between ejection of 239,240Pu into the atmosphere and deposition. Auxiliary markers include: first appearance of 137Cs in 1958; late 20th-century decreases in δ15N; late 20th-century elevation in SCPs, Hg, Pb, and other heavy metals; and changes in abundance and presence of ostracod, algae, rotifer and protozoan microfossils. Fossil pollen document anthropogenic landscape changes related to logging and agriculture. As part of a major university, the Searsville site has long been used for research and education, serves users locally to internationally, and is protected yet accessible for future studies and communication about the Anthropocene.The Global boundary Stratotype Section and Point (GSSP) for the proposed Anthropocene Series/Epoch is suggested to lie in sediments accumulated over the last ~120 years in Searsville Lake, Woodside, California, USA. The site fulfills all of the ideal criteria for defining and placing a GSSP. In addition, the Searsville site is particularly appropriate to mark the onset of the Anthropocene, because it was anthropogenic activities-the damming of a watershed-that created a geologic record that now preserves the very signals that can be used to recognize the Anthropocene worldwide.

    View details for DOI 10.1177/20530196221144098

    View details for PubMedID 37213212

    View details for PubMedCentralID PMC10193828

  • Bothersome burrowers: Tracking the impact of Botta's pocket gopher (Thomomys bottae) bioturbation on a late-Holocene site JOURNAL OF ARCHAEOLOGICAL SCIENCE-REPORTS Viteri, M. C., Stegner, M., Hadly, E. A. 2023; 48
  • The Searsville Lake Site (California, USA) as a candidate Global Boundary Stratotype Section and Point for the Anthropocene Series ANTHROPOCENE REVIEW Stegner, M., Hadly, E. A., Barnosky, A. D., La Selle, S., Sherrod, B., Anderson, R., Redondo, S. A., Viteri, M. C., Weaver, K. L., Cundy, A. B., Gaca, P., Rose, N. L., Yang, H., Roberts, S. L., Hajdas, I., Black, B. A., Spanbauer, T. L. 2023
  • Genome Report: Chromosome-level draft assemblies of the snow leopard, African leopard, and tiger (Panthera uncia, Panthera pardus pardus, and Panthera tigris). G3 (Bethesda, Md.) Armstrong, E. E., Campana, M. G., Solari, K. A., Morgan, S. R., Ryder, O. A., Naude, V. N., Samelius, G., Sharma, K., Hadly, E. A., Petrov, D. A. 2022

    Abstract

    The big cats (genus Panthera) represent some of the most popular and charismatic species on the planet. Although some reference genomes are available for this clade, few are at the chromosome level, inhibiting high-resolution genomic studies. We assembled genomes from three members of the genus, the tiger (Panthera tigris), the snow leopard (Panthera uncia), and the African leopard (Panthera pardus pardus), at chromosome or near-chromosome level. We used a combination of short- and long-read technologies, as well as proximity ligation data from Hi-C technology, to achieve high continuity and contiguity for each individual. We hope these genomes will aid in further evolutionary and conservation research of this iconic group of mammals.

    View details for DOI 10.1093/g3journal/jkac277

    View details for PubMedID 36250809

  • From coral reefs to Joshua trees: What ecological interactions teach us about the adaptive capacity of biodiversity in the Anthropocene. Philosophical transactions of the Royal Society of London. Series B, Biological sciences Lagerstrom, K. M., Vance, S., Cornwell, B. H., Ruffley, M., Bellagio, T., Exposito-Alonso, M., Palumbi, S. R., Hadly, E. A. 2022; 377 (1857): 20210389

    Abstract

    The pervasive loss of biodiversity in the Anthropocene necessitates rapid assessments of ecosystems to understand how they will respond to anthropogenic environmental change. Many studies have sought to describe the adaptive capacity (AC) of individual species, a measure that encompasses a species' ability to respond and adapt to change. Only those adaptive mechanisms that can be used over the next few decades (e.g. via novel interactions, behavioural changes, hybridization, migration, etc.) are relevant to the timescale set by the rapid changes of the Anthropocene. The impacts of species loss cascade through ecosystems, yet few studies integrate the capacity of ecological networks to adapt to change with the ACs of its species. Here, we discuss three ecosystems and how their ecological networks impact the AC of species and vice versa. A more holistic perspective that considers the AC of species with respect to their ecological interactions and functions will provide more predictive power and a deeper understanding of what factors are most important to a species' survival. We contend that the AC of a species, combined with its role in ecosystem function and stability, must guide decisions in assigning 'risk' and triaging biodiversity loss in the Anthropocene. This article is part of the theme issue 'Ecological complexity and the biosphere: the next 30 years'.

    View details for DOI 10.1098/rstb.2021.0389

    View details for PubMedID 35757872

  • Spatiotemporal impacts of the Anthropocene on small mammal communities, and the role of small biological preserves in maintaining biodiversity FRONTIERS IN ECOLOGY AND EVOLUTION Viteri, M. C., Hadly, E. A. 2022; 10
  • Planetary-scale change to the biosphere signalled by global species translocations can be used to identify the Anthropocene PALAEONTOLOGY Williams, M., Leinfelder, R., Barnosky, A. D., Head, M. J., McCarthy, F. G., Cearreta, A., Himson, S., Holmes, R., Waters, C. N., Zalasiewicz, J., Turner, S., McGann, M., Hadly, E. A., Stegner, M., Pilkington, P., Kaiser, J., Berrio, J., Wilkinson, I. P., Zinke, J., Delong, K. L. 2022; 65 (4)

    View details for DOI 10.1111/pala.12618

    View details for Web of Science ID 000844707500001

  • Stable isotopes reveal seasonal dietary responses to agroforestry in a venomous mammal, the Hispaniolan solenodon (Solenodon paradoxus). Ecology and evolution Mychajliw, A. M., Almonte, J. N., Martinez, P. A., Hadly, E. A. 2022; 12 (3): e8761

    Abstract

    While trends in tropical deforestation are alarming, conservation biologists are increasingly recognizing the potential for species survival in human-modified landscapes. Identifying the factors underlying such persistence, however, requires basic ecological knowledge of a species' resource use. Here, we generate such data to guide conservation of an understudied venomous mammal, the Hispaniolan solenodon (Solenodon paradoxus), that occupies a mosaic landscape of agriculture and forest fragments in the western Dominican Republic. Using feces collected in both wet and dry seasons, we found significant differences in the stable isotope values of carbon (delta13C) between pasture (-24.63±2.31, Las Mercedes) and agroforestry (-28.07±2.10, Mencia). Solenodon populations in agricultural areas occupied wider isotopic niche spaces, which may be explained by more diverse resource within these patches or individuals combining resources across habitats. We detected elevated delta15N values in the dry season of pasture areas (8.22±2.30) as compared to the wet season (5.26±2.44) and overall narrower isotopic niche widths in the dry season, suggestive of the impacts of aridity on foraging behavior. Our work highlights the importance of considering a more nuanced view of variations in 'modified' or "agricultural" landscapes as compared with strictly protected national parks. We suggest that seasonal differences in foraging should be considered as they intersect with landscape modification by landowners for maintaining resources for focal consumers. This work adds to a growing body of literature highlighting that fecal stable isotopes are a non-invasive and cost-effective monitoring tool that is particularly well-suited for cryptic small mammal species, ensuring actionable and evidenced-based conservation practices in the tropic's rapidly changing landscapes.

    View details for DOI 10.1002/ece3.8761

    View details for PubMedID 35356572

  • Muskrats as a bellwether of a drying delta. Communications biology Ward, E. M., Solari, K. A., Varudkar, A., Gorelick, S. M., Hadly, E. A. 2021; 4 (1): 750

    Abstract

    Wetlands worldwide are under threat from anthropogenic impacts. In large protected North American areas such as Yellowstone and Wood Buffalo National Parks, aquatic habitats are disappearing and wetland-dependent fauna are in decline1-3. Here we investigate population dynamics of an indicator species in Canada's Peace-Athabasca Delta ("the delta"), a World Heritage Site. Based on population surveys, habitat mapping and genetic data from 288 muskrats, we use agent-based modeling and genetic analyses to explain population expansion and decline of the semi-aquatic muskrat (Ondatra zibethicus). Simulations quantify a large population (~500,000 individuals) following flood-induced habitat gains, with decreased size (~10,000 individuals) during drying. Genetic analyses show extremely low long-term effective population size (Ne: 60-127), supporting a legacy of population bottlenecks. Our simulations indicate that the muskrat population in the delta is a metapopulation with individuals migrating preferentially along riparian pathways. Related individuals found over 40km apart imply dispersal distances far greater than their typical home range (130m). Rapid metapopulation recovery is achieved via riparian corridor migration and passive flood-transport of individuals. Source-sink dynamics show wetland loss impacts on the muskrat metapopulation's spatial extent. Dramatic landscape change is underway, devastating local fauna, including this generalist species even in a protected ecosystem.

    View details for DOI 10.1038/s42003-021-02288-7

    View details for PubMedID 34168255

  • The under-investigated wild side of Escherichia coli: genetic diversity, pathogenicity and antimicrobial resistance in wild animals. Proceedings. Biological sciences Lagerstrom, K. M., Hadly, E. A. 2021; 288 (1948): 20210399

    Abstract

    A striking paucity of information exists on Escherichia coli in wild animals despite evidence that they harbour pathogenic and antimicrobial-resistant E. coli in their gut microbiomes and may even serve as melting pots for novel genetic combinations potentially harmful to human health. Wild animals have been implicated as the source of pathogenic E. coli outbreaks in agricultural production, but a lack of knowledge surrounding the genetics of E. coli in wild animals complicates source tracking and thus contamination curtailment efforts. As human populations continue to expand and invade wild areas, the potential for harmful microorganisms to transfer between humans and wildlife increases. Here, we conducted a literature review of the small body of work on E. coli in wild animals. We highlight the geographic and host taxonomic coverage to date, and in each, identify significant gaps. We summarize the current understanding of E. coli in wild animals, including its genetic diversity, host and geographic distribution, and transmission pathways within and between wild animal and human populations. The knowledge gaps we identify call for greater research efforts to understand the existence of E. coli in wild animals, especially in light of the potentially strong implications for global public health.

    View details for DOI 10.1098/rspb.2021.0399

    View details for PubMedID 33849316

  • Recent evolutionary history of tigers highlights contrasting roles of genetic drift and selection. Molecular biology and evolution Armstrong, E. E., Khan, A. n., Taylor, R. W., Gouy, A. n., Greenbaum, G. n., Thiéry, A. n., Kang, J. T., Redondo, S. A., Prost, S. n., Barsh, G. n., Kaelin, C. n., Phalke, S. n., Chugani, A. n., Gilbert, M. n., Miquelle, D. n., Zachariah, A. n., Borthakur, U. n., Reddy, A. n., Louis, E. n., Ryder, O. A., Jhala, Y. V., Petrov, D. n., Excoffier, L. n., Hadly, E. n., Ramakrishnan, U. n. 2021

    Abstract

    Species conservation can be improved by knowledge of evolutionary and genetic history. Tigers are among the most charismatic of endangered species and garner significant conservation attention. However, their evolutionary history and genomic variation remains poorly known, especially for Indian tigers. With 70% of the worlds wild tigers living in India, such knowledge is critical. We re-sequenced 65 individual tiger genomes representing most extant subspecies with a specific focus on tigers from India. As suggested by earlier studies, we found strong genetic differentiation between the putative tiger subspecies. Despite high total genomic diversity in India, individual tigers host longer runs of homozygosity, potentially suggesting recent inbreeding or founding events, possibly due to small and fragmented protected areas. We suggest the impacts of ongoing connectivity loss on inbreeding and persistence of Indian tigers be closely monitored. Surprisingly, demographic models suggest recent divergence (within the last 20,000 years) between subspecies, and strong population bottlenecks. Amur tiger genomes revealed the strongest signals of selection related to metabolic adaptation to cold, while Sumatran tigers show evidence of weak selection for genes involved in body size regulation. We recommend detailed investigation of local adaptation in Amur and Sumatran tigers prior to initiating genetic rescue.

    View details for DOI 10.1093/molbev/msab032

    View details for PubMedID 33592092

  • Assessing the reliability of raptor pellets in recording local small mammal diversity Quaternary Research Viteri, M. 2021

    View details for DOI 10.1017/qua.2021.59

  • Molecular Ecological Network Analyses: An Effective Conservation Tool for the Assessment of Biodiversity, Trophic Interactions, and Community Structure FRONTIERS IN ECOLOGY AND EVOLUTION Meyer, J. M., Leempoel, K., Losapio, G., Hadly, E. A. 2020; 8
  • A comparison of eDNA to camera trapping for assessment of terrestrial mammal diversity. Proceedings. Biological sciences Leempoel, K., Hebert, T., Hadly, E. A. 2020; 287 (1918): 20192353

    Abstract

    Before environmental DNA (eDNA) can establish itself as a robust tool for biodiversity monitoring, comparison with existing approaches is necessary, yet is lacking for terrestrial mammals. Moreover, much is unknown regarding the nature, spread and persistence of DNA shed by animals into terrestrial environments, or the optimal experimental design for understanding these potential biases. To address some of these challenges, we compared the detection of terrestrial mammals using eDNA analysis of soil samples against confirmed species observations from a long-term (approx. 9-year) camera-trapping study. At the same time, we considered multiple experimental parameters, including two sampling designs, two DNA extraction kits and two metabarcodes of different sizes. All mammals regularly recorded with cameras were detected in eDNA. In addition, eDNA reported many unrecorded small mammals whose presence in the study area is otherwise documented. A long metabarcode (220 bp) offering a high taxonomic resolution, achieved a similar efficiency as a shorter one (70 bp) and a phosphate buffer-based extraction gave similar results as a total DNA extraction method, for a fraction of the price. Our results support that eDNA-based monitoring should become a valuable part of ecosystem surveys, yet mitochondrial reference databases need to be enriched first.

    View details for DOI 10.1098/rspb.2019.2353

    View details for PubMedID 31937227

  • Long live the king: chromosome-level assembly of the lion (Panthera leo) using linked-read, Hi-C, and long-read data. BMC biology Armstrong, E. E., Taylor, R. W., Miller, D. E., Kaelin, C. B., Barsh, G. S., Hadly, E. A., Petrov, D. 2020; 18 (1): 3

    Abstract

    BACKGROUND: The lion (Panthera leo) is one of the most popular and iconic feline species on the planet, yet in spite of its popularity, the last century has seen massive declines for lion populations worldwide. Genomic resources for endangered species represent an important way forward for the field of conservation, enabling high-resolution studies of demography, disease, and population dynamics. Here, we present a chromosome-level assembly from a captive African lion from the Exotic Feline Rescue Center (Center Point, IN) as a resource for current and subsequent genetic work of the sole social species of the Panthera clade.RESULTS: Our assembly is composed of 10x Genomics Chromium data, Dovetail Hi-C, and Oxford Nanopore long-read data. Synteny is highly conserved between the lion, other Panthera genomes, and the domestic cat. We find variability in the length of runs of homozygosity across lion genomes, indicating contrasting histories of recent and possibly intense inbreeding and bottleneck events. Demographic analyses reveal similar ancient histories across all individuals during the Pleistocene except the Asiatic lion, which shows a more rapid decline in population size. We show a substantial influence on the reference genome choice in the inference of demographic history and heterozygosity.CONCLUSIONS: We demonstrate that the choice of reference genome is important when comparing heterozygosity estimates across species and those inferred from different references should not be compared to each other. In addition, estimates of heterozygosity or the amount or length of runs of homozygosity should not be taken as reflective of a species, as these can differ substantially among individuals. This high-quality genome will greatly aid in the continuing research and conservation efforts for the lion, which is rapidly moving towards becoming a species in danger of extinction.

    View details for DOI 10.1186/s12915-019-0734-5

    View details for PubMedID 31915011

  • Experimental study of hypoxia-induced changes in gene expression in an Asian pika, Ochotona dauurica. PloS one Solari, K. A., Hadly, E. A. 2020; 15 (10): e0240435

    Abstract

    Acclimation to environmental changes driven by alterations in gene expression will serve as an important response for some species facing rapid Anthropogenic climate change. Pikas, genus Ochotona, are particularly vulnerable to climate change and current trends suggest that only the highest, coldest elevations within their ranges may remain suitable habitat for these species. In this study we aimed to assess the role of changes in gene expression in potentially facilitating elevational movements in pikas by measuring gene expression in the only known captive pika population, Ochotona dauurica, in response to hypoxic conditions. Using a controlled experiment, we exposed four male pikas to oxygen concentrations characteristic of sea-level, 2,000 m, and 4,000 m for 5 days each. Using blood samples collected after each treatment, we used RNAseq to determine if candidate pathways were undergoing significant changes in gene expression at different levels of oxygen (~100%, ~77%, and ~61% of sea-level oxygen concentrations). Gene set enrichment analyses showed that gene sets associated with the oxidative phosphorylation pathway and electron transport chain were significantly enriched for up-regulated genes in the 4,000 m samples compared to samples from the same individuals at lower-elevation conditions. Up-regulation of these pathways is consistent with known mechanisms of oxygen compensation. Our results suggest that these pikas have the acclimation capacity to tolerate oxygen concentrations characteristic of any elevation within their species range and that gene expression can be changed in a matter of days to accommodate drastically different oxygen concentrations. Thus, rapid and radical elevational movements that may be required of some pika species to avoid warmer temperatures in the Anthropocene will likely not be limited by hypoxic stress.

    View details for DOI 10.1371/journal.pone.0240435

    View details for PubMedID 33044983

  • Empowering conservation practice with efficient and economical genotyping from poor quality samples METHODS IN ECOLOGY AND EVOLUTION Natesh, M., Taylor, R. W., Truelove, N. K., Hadly, E. A., Palumbi, S. R., Petrov, D. A., Ramakrishnan, U. 2019; 10 (6): 853–59
  • Empowering conservation practice with efficient and economical genotyping from poor quality samples. Methods in ecology and evolution Natesh, M., Taylor, R. W., Truelove, N. K., Hadly, E. A., Palumbi, S. R., Petrov, D. A., Ramakrishnan, U. 2019; 10 (6): 853-859

    Abstract

    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

  • Gene expression is implicated in the ability of pikas to occupy Himalayan elevational gradient PLOS ONE Solari, K. A., Ramakrishnan, U., Hadly, E. A. 2018; 13 (12)
  • Global fingerprint of humans on the distribution of Bartonella bacteria in mammals. PLoS neglected tropical diseases Frank, H. K., Boyd, S. D., Hadly, E. A. 2018; 12 (11): e0006865

    Abstract

    As humans move and alter habitats, they change the disease risk for themselves, their commensal animals and wildlife. Bartonella bacteria are prevalent in mammals and cause numerous human infections. Understanding how this genus has evolved and switched hosts in the past can reveal how current patterns were established and identify potential mechanisms for future cross-species transmission. We analyzed patterns of Bartonella transmission and likely sources of spillover using the largest collection of Bartonella gltA genotypes assembled, including 67 new genotypes. This pathogenic genus likely originated as an environmental bacterium and insect commensal before infecting mammals. Rodents and domestic animals serve as the reservoirs or at least key proximate host for most Bartonella genotypes in humans. We also find evidence of exchange of Bartonella between phylogenetically distant domestic animals and wildlife, likely due to increased contact. Care should be taken to avoid contact between humans, domestic animals and wildlife to protect the health of all.

    View details for PubMedID 30439961

  • Global fingerprint of humans on the distribution of Bartonella bacteria in mammals PLOS NEGLECTED TROPICAL DISEASES Frank, H. K., Boyd, S. D., Hadly, E. A. 2018; 12 (11)
  • Evolution for extreme living: variation in mitochondrial cytochrome c oxidase genes correlated with elevation in pikas (genus Ochotona) INTEGRATIVE ZOOLOGY Solari, K. A., Hadly, E. A. 2018; 13 (5): 517–35
  • Evolution for extreme living: variation in mitochondrial cytochrome c oxidase genes correlated with elevation in pikas (genus Ochotona). Integrative zoology Solari, K. A., Hadly, E. A. 2018

    Abstract

    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 PubMedID 29851233

  • Making America great again requires acting on scientific knowledge. PLoS biology Hadly, E. A. 2018; 16 (2): e2004337

    View details for PubMedID 29401207

  • Making America great again requires acting on scientific knowledge PLOS BIOLOGY Hadly, E. A. 2018; 16 (2)
  • Rethinking "Native" in the Anthropocene Frontiers in Earth Science Hill, A. P., Hadly, E. A. 2018; 6: 1-4

    View details for DOI 10.3389/feart.2018.00096

  • Gene expression is implicated in the ability of pikas to occupy Himalayan elevational gradient. PloS one Solari, K. A., Ramakrishnan, U., Hadly, E. A. 2018; 13 (12): e0207936

    Abstract

    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 positive selection among sites. However, out of over 10,000 expressed transcripts, 26 were significantly upregulated 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 may play a key role in enabling hypoxia tolerance on this local scale, indicating elevational flexibility that may facilitate successful range shifts in response to climate change.

    View details for PubMedID 30540800

  • Genomic data reveal a loss of diversity in two species of tucotucos (genus Ctenomys) following a volcanic eruption SCIENTIFIC REPORTS Hsu, J. L., Crawford, J., Tammone, M. N., Ramakrishnan, U., Lacey, E. A., Hadly, E. A. 2017; 7
  • Genomic data reveal a loss of diversity in two species of tuco-tucos (genus Ctenomys) following a volcanic eruption. Scientific reports Hsu, J. L., Crawford, J. C., Tammone, M. N., Ramakrishnan, U., Lacey, E. A., Hadly, E. A. 2017; 7 (1): 16227

    Abstract

    Marked reductions in population size can trigger corresponding declines in genetic variation. Understanding the precise genetic consequences of such reductions, however, is often challenging due to the absence of robust pre- and post-reduction datasets. Here, we use heterochronous genomic data from samples obtained before and immediately after the 2011 eruption of the Puyehue-Cordón Caulle volcanic complex in Patagonia to explore the genetic impacts of this event on two parapatric species of rodents, the colonial tuco-tuco (Ctenomys sociabilis) and the Patagonian tuco-tuco (C. haigi). Previous analyses using microsatellites revealed no post-eruption changes in genetic variation in C. haigi, but an unexpected increase in variation in C. sociabilis. To explore this outcome further, we used targeted gene capture to sequence over 2,000 putatively neutral regions for both species. Our data revealed that, contrary to the microsatellite analyses, the eruption was associated with a small but significant decrease in genetic variation in both species. We suggest that genome-level analyses provide greater power than traditional molecular markers to detect the genetic consequences of population size changes, particularly changes that are recent, short-term, or modest in size. Consequently, genomic analyses promise to generate important new insights into the effects of specific environmental events on demography and genetic variation.

    View details for DOI 10.1038/s41598-017-16430-1

    View details for PubMedID 29176629

    View details for PubMedCentralID PMC5701162

  • Frequency shifting reduces but does not eliminate acoustic interference between echolocating bats: A theoretical analysis. The Journal of the Acoustical Society of America Perkins, M. L., Frank, H. K., Pauly, J. M., Hadly, E. A. 2017; 142 (4): 2133

    Abstract

    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

    View details for PubMedID 29092549

  • Rethinking the Origin of Primates by Reconstructing Their Diel Activity Patterns Using Genetics and Morphology SCIENTIFIC REPORTS Wu, Y., Wang, H., Wang, H., Hadly, E. A. 2017; 7: 11837

    Abstract

    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 PubMedID 28928374

  • Rapid increase in genetic diversity in an endemic Patagonian tuco-tuco following a recent volcanic eruption JOURNAL OF MAMMALOGY Hsu, J. L., Kam, S., Tammone, M. N., Lacey, E. A., Hadly, E. A. 2017; 98 (3): 779-792
  • Can protected areas really maintain mammalian diversity? Insights from a nestedness analysis of the Colorado Plateau BIOLOGICAL CONSERVATION Stegner, M., Karp, D. S., Rominger, A. J., Hadly, E. A. 2017; 209: 546–53
  • Invasion of Ancestral Mammals into Dim-light Environments Inferred from Adaptive Evolution of the Phototransduction Genes. Scientific reports Wu, Y., Wang, H., Hadly, E. A. 2017; 7: 46542-?

    Abstract

    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 SCIENCE Barnosky, A. D., Hadly, E. A., Gonzalez, P., Head, J., Polly, P. D., Lawing, A. M., Eronen, J. T., Ackerly, D. D., Alex, K., Biber, E., Blois, J., Brashares, J., Ceballos, G., Davis, E., Dietl, G. P., Dirzo, R., Doremus, H., Fortelius, M., Greene, H. W., Hellmann, J., Hickler, T., Jackson, S. T., Kemp, M., Koch, P. L., Kremen, C., Lindsey, E. L., Looy, C., Marshall, C. R., Mendenhall, C., Mulch, A., Mychajliw, A. M., Nowak, C., Ramakrishnan, U., Schnitzler, J., Das Shrestha, K., Solari, K., Stegner, L., Stegner, M. A., Stenseth, N. C., Wake, M. H., Zhang, Z. 2017; 355 (6325): 594-?

    Abstract

    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 PubMedID 28183912

  • Phylogeny, Traits, and Biodiversity of a Neotropical Bat Assemblage: Close Relatives Show Similar Responses to Local Deforestation. The American naturalist Frank, H. K., Frishkoff, L. O., Mendenhall, C. D., Daily, G. C., Hadly, E. A. 2017; 190 (2): 200–212

    Abstract

    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

  • Corrigendum to "Genetics, morphology and ecology reveal a cryptic pika lineage in the Sikkim Himalaya" [Mol. Phylogenet. Evol. 106 (2017) 55-60]. Molecular phylogenetics and evolution Dahal, N. n., Lissovsky, A. A., Lin, Z. n., Solari, K. n., Hadly, E. A., Zhan, X. n., Ramakrishnan, U. n. 2017; 107: 645

    View details for PubMedID 27888666

  • Frequency shifting reduces but does not eliminate acoustic interference between echolocating bats: A theoretical analysis The Journal of the Acoustical Society of America Perkins, M. L., Frank, H. K., Pauly, J. M., Hadly, E. A. 2017; 142: 2133

    Abstract

    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

  • Genetics, morphology and ecology reveal a cryptic pika lineage in the Sikkim Himalaya. Molecular phylogenetics and evolution Dahal, N., Lissovsky, A. A., Lin, Z., Solari, K., Hadly, E. A., Zhan, X., Ramakrishnan, U. 2017; 106: 55-60

    Abstract

    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

  • Opportunity for some, extinction for others: the fate of tetrapods in the Anthropocene EVOLUTIONARY ECOLOGY RESEARCH Solari, K. A., Frank, H. K., Frishkoff, L. O., Hsu, J. L., Kemp, M. E., Mychajliw, A. M., Hadly, E. A. 2016; 17 (6): 787-813
  • 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 Marcy, A. E., Hadly, E. A., Sherratt, E., Garland, K., Weisbecker, V. 2016; 16

    Abstract

    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

  • Retinal transcriptome sequencing sheds light on the adaptation to nocturnal and diurnal lifestyles in raptors SCIENTIFIC REPORTS Wu, Y., Hadly, E. A., Teng, W., Hao, Y., Liang, W., Liu, Y., Wang, H. 2016; 6

    Abstract

    Owls (Strigiformes) represent a fascinating group of birds that are the ecological night-time counterparts to diurnal raptors (Accipitriformes). The nocturnality of owls, unusual within birds, has favored an exceptional visual system that is highly tuned for hunting at night, yet the molecular basis for this adaptation is lacking. Here, using a comparative evolutionary analysis of 120 vision genes obtained by retinal transcriptome sequencing, we found strong positive selection for low-light vision genes in owls, which contributes to their remarkable nocturnal vision. Not surprisingly, we detected gene loss of the violet/ultraviolet-sensitive opsin (SWS1) in all owls we studied, but two other color vision genes, the red-sensitive LWS and the blue-sensitive SWS2, were found to be under strong positive selection, which may be linked to the spectral tunings of these genes toward maximizing photon absorption in crepuscular conditions. We also detected the only other positively selected genes associated with motion detection in falcons and positively selected genes associated with bright-light vision and eye protection in other diurnal raptors (Accipitriformes). Our results suggest the adaptive evolution of vision genes reflect differentiated activity time and distinct hunting behaviors.

    View details for DOI 10.1038/srep33578

    View details for PubMedID 27645106

  • Climate change and habitat conversion favour the same species ECOLOGY LETTERS Frishkoff, L. O., Karp, D. S., Flanders, J. R., Zook, J., Hadly, E. A., Daily, G. C., M'Gonigle, L. K. 2016; 19 (9): 1081-1090

    Abstract

    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 Kemp, M. E., Hadly, E. A. 2016; 36 (5)
  • Anthropogenic impacts on Costa Rican bat parasitism are sex specific ECOLOGY AND EVOLUTION Frank, H. K., Mendenhall, C. D., Judson, S. D., Daily, G. C., Hadly, E. A. 2016; 6 (14): 4898-4909

    Abstract

    While anthropogenic impacts on parasitism of wildlife are receiving growing attention, whether these impacts vary in a sex-specific manner remains little explored. Differences between the sexes in the effect of parasites, linked to anthropogenic activity, could lead to uneven sex ratios and higher population endangerment. We sampled 1108 individual bats in 18 different sites across an agricultural mosaic landscape in southern Costa Rica to investigate the relationships between anthropogenic impacts (deforestation and reductions in host species richness) and bat fly ectoparasitism of 35 species of Neotropical bats. Although female and male bat assemblages were similar across the deforestation gradient, bat fly assemblages tracked their hosts closely only on female bats. We found that in female hosts, parasite abundance per bat decreased with increasing bat species richness, while in male hosts, parasite abundance increased. We hypothesize the differences in the parasite-disturbance relationship are due to differences in roosting behavior between the sexes. We report a sex-specific parasite-disturbance relationship and argue that sex differences in anthropogenic impacts on wildlife parasitism could impact long-term population health and survival.

    View details for DOI 10.1002/ece3.2245

    View details for Web of Science ID 000380033400022

    View details for PubMedCentralID PMC4979715

  • Anthropogenic impacts on Costa Rican bat parasitism are sex specific. Ecology and evolution Frank, H. K., Mendenhall, C. D., Judson, S. D., Daily, G. C., Hadly, E. A. 2016; 6 (14): 4898-909

    Abstract

    While anthropogenic impacts on parasitism of wildlife are receiving growing attention, whether these impacts vary in a sex-specific manner remains little explored. Differences between the sexes in the effect of parasites, linked to anthropogenic activity, could lead to uneven sex ratios and higher population endangerment. We sampled 1108 individual bats in 18 different sites across an agricultural mosaic landscape in southern Costa Rica to investigate the relationships between anthropogenic impacts (deforestation and reductions in host species richness) and bat fly ectoparasitism of 35 species of Neotropical bats. Although female and male bat assemblages were similar across the deforestation gradient, bat fly assemblages tracked their hosts closely only on female bats. We found that in female hosts, parasite abundance per bat decreased with increasing bat species richness, while in male hosts, parasite abundance increased. We hypothesize the differences in the parasite-disturbance relationship are due to differences in roosting behavior between the sexes. We report a sex-specific parasite-disturbance relationship and argue that sex differences in anthropogenic impacts on wildlife parasitism could impact long-term population health and survival.

    View details for DOI 10.1002/ece3.2245

    View details for PubMedID 27547321

    View details for PubMedCentralID PMC4979715

  • Post-invasion demography of prehistoric humans in South America. Nature Goldberg, A., Mychajliw, A. M., Hadly, E. A. 2016; 532 (7598): 232-235

    Abstract

    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

  • Avoiding collapse: Grand challenges for science and society to solve by 2050 ELEMENTA-SCIENCE OF THE ANTHROPOCENE Barnosky, A. D., Ehrlich, P. R., Hadly, E. A. 2016; 4: 1–9
  • Early Holocene turnover, followed by stability, in a Caribbean lizard assemblage QUATERNARY RESEARCH Kemp, M. E., Hadly, E. A. 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 Barnosky, A. D., Lindsey, E. L., Villavicencio, N. A., Bostelmann, E., Hadly, E. A., Wanket, J., Marshall, C. R. 2016; 113 (4): 856-861

    Abstract

    Loss of megafauna, an aspect of defaunation, can precipitate many ecological changes over short time scales. We examine whether megafauna loss can also explain features of lasting ecological state shifts that occurred as the Pleistocene gave way to the Holocene. We compare ecological impacts of late-Quaternary megafauna extinction in five American regions: southwestern Patagonia, the Pampas, northeastern United States, northwestern United States, and Beringia. We find that major ecological state shifts were consistent with expectations of defaunation in North American sites but not in South American ones. The differential responses highlight two factors necessary for defaunation to trigger lasting ecological state shifts discernable in the fossil record: (i) lost megafauna need to have been effective ecosystem engineers, like proboscideans; and (ii) historical contingencies must have provided the ecosystem with plant species likely to respond to megafaunal loss. These findings help in identifying modern ecosystems that are most at risk for disappearing should current pressures on the ecosystems' large animals continue and highlight the critical role of both individual species ecologies and ecosystem context in predicting the lasting impacts of defaunation currently underway.

    View details for DOI 10.1073/pnas.1505295112

    View details for Web of Science ID 000368617900027

    View details for PubMedCentralID PMC4739530

  • 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 Barnosky, A. D., Lindsey, E. L., Villavicencio, N. A., Bostelmann, E., Hadly, E. A., Wanket, J., Marshall, C. R. 2016; 113 (4): 856-61

    Abstract

    Loss of megafauna, an aspect of defaunation, can precipitate many ecological changes over short time scales. We examine whether megafauna loss can also explain features of lasting ecological state shifts that occurred as the Pleistocene gave way to the Holocene. We compare ecological impacts of late-Quaternary megafauna extinction in five American regions: southwestern Patagonia, the Pampas, northeastern United States, northwestern United States, and Beringia. We find that major ecological state shifts were consistent with expectations of defaunation in North American sites but not in South American ones. The differential responses highlight two factors necessary for defaunation to trigger lasting ecological state shifts discernable in the fossil record: (i) lost megafauna need to have been effective ecosystem engineers, like proboscideans; and (ii) historical contingencies must have provided the ecosystem with plant species likely to respond to megafaunal loss. These findings help in identifying modern ecosystems that are most at risk for disappearing should current pressures on the ecosystems' large animals continue and highlight the critical role of both individual species ecologies and ecosystem context in predicting the lasting impacts of defaunation currently underway.

    View details for DOI 10.1073/pnas.1505295112

    View details for PubMedID 26504219

    View details for PubMedCentralID PMC4739530

  • Palesvertebrate Communities ECOSYSTEMS OF CALIFORNIA Hadly, E. A., Feranec, R. S., Mooney, H., Zavaleta, E. 2016: 155-168
  • Bartonellae are Prevalent and Diverse in Costa Rican Bats and Bat Flies ZOONOSES AND PUBLIC HEALTH Judson, S. D., FRANK, H. K., Hadly, E. A. 2015; 62 (8): 609-617

    View details for DOI 10.1111/zph.12188

    View details for Web of Science ID 000367884000005

  • Using the Anthropocene as a teaching, communication and community engagement opportunity ANTHROPOCENE REVIEW Mychajliw, A. M., Kemp, M. E., Hadly, E. A. 2015; 2 (3): 267-278
  • Thermal niche predicts tolerance to habitat conversion in tropical amphibians and reptiles GLOBAL CHANGE BIOLOGY Frishkoff, L. O., Hadly, E. A., Daily, G. C. 2015; 21 (11): 3901-3916

    Abstract

    Habitat conversion is a major driver of the biodiversity crisis, yet why some species undergo local extinction while others thrive under novel conditions remains unclear. We suggest that focusing on species' niches, rather than traits, may provide the predictive power needed to forecast biodiversity change. We first examine two Neotropical frog congeners with drastically different affinities to deforestation and document how thermal niche explains deforestation tolerance. The more deforestation-tolerant species is associated with warmer macroclimates across Costa Rica, and warmer microclimates within landscapes. Further, in laboratory experiments, the more deforestation-tolerant species has critical thermal limits, and a jumping performance optimum, shifted ~2 °C warmer than those of the more forest-affiliated species, corresponding to the ~3 °C difference in daytime maximum temperature that these species experience between habitats. Crucially, neither species strictly specializes on either habitat - instead habitat use is governed by regional environmental temperature. Both species track temperature along an elevational gradient, and shift their habitat use from cooler forest at lower elevations to warmer deforested pastures upslope. To generalize these conclusions, we expand our analysis to the entire mid-elevational herpetological community of southern Costa Rica. We assess the climatological affinities of 33 amphibian and reptile species, showing that across both taxonomic classes, thermal niche predicts presence in deforested habitat as well as or better than many commonly used traits. These data suggest that warm-adapted species carry a significant survival advantage amidst the synergistic impacts of land-use conversion and climate change.

    View details for DOI 10.1111/gcb.13016

    View details for Web of Science ID 000364777200001

    View details for PubMedID 26148337

  • Extinction biases in Quaternary Caribbean lizards GLOBAL ECOLOGY AND BIOGEOGRAPHY Kemp, M. E., Hadly, E. A. 2015; 24 (11): 1281-1289

    View details for DOI 10.1111/geb.12366

    View details for Web of Science ID 000362796400008

  • Evidence for the peopling of South America: archeological and genetic perspectives Goldberg, A., Mychajliw, A. M., Sztraicher, D., Hadly, E. A. WILEY-BLACKWELL. 2015: 148
  • Loss of avian phylogenetic diversity in neotropical agricultural systems SCIENCE Frishkoff, L. O., Karp, D. S., M'Gonigle, L. K., Mendenhall, C. D., Zook, J., Kremen, C., Hadly, E. A., Daily, G. C. 2014; 345 (6202): 1343-1346

    Abstract

    Habitat conversion is the primary driver of biodiversity loss, yet little is known about how it is restructuring the tree of life by favoring some lineages over others. We combined a complete avian phylogeny with 12 years of Costa Rican bird surveys (118,127 detections across 487 species) sampled in three land uses: forest reserves, diversified agricultural systems, and intensive monocultures. Diversified agricultural systems supported 600 million more years of evolutionary history than intensive monocultures but 300 million fewer years than forests. Compared with species with many extant relatives, evolutionarily distinct species were extirpated at higher rates in both diversified and intensive agricultural systems. Forests are therefore essential for maintaining diversity across the tree of life, but diversified agricultural systems may help buffer against extreme loss of phylogenetic diversity.

    View details for DOI 10.1126/science.1254610

    View details for Web of Science ID 000341483800064

  • Loss of avian phylogenetic diversity in neotropical agricultural systems. Science Frishkoff, L. O., Karp, D. S., M'Gonigle, L. K., Mendenhall, C. D., Zook, J., Kremen, C., Hadly, E. A., Daily, G. C. 2014; 345 (6202): 1343-1346

    Abstract

    Habitat conversion is the primary driver of biodiversity loss, yet little is known about how it is restructuring the tree of life by favoring some lineages over others. We combined a complete avian phylogeny with 12 years of Costa Rican bird surveys (118,127 detections across 487 species) sampled in three land uses: forest reserves, diversified agricultural systems, and intensive monocultures. Diversified agricultural systems supported 600 million more years of evolutionary history than intensive monocultures but 300 million fewer years than forests. Compared with species with many extant relatives, evolutionarily distinct species were extirpated at higher rates in both diversified and intensive agricultural systems. Forests are therefore essential for maintaining diversity across the tree of life, but diversified agricultural systems may help buffer against extreme loss of phylogenetic diversity.

    View details for DOI 10.1126/science.1254610

    View details for PubMedID 25214627

  • Translating science for decision makers to help navigate the Anthropocene ANTHROPOCENE REVIEW Barnosky, A. D., Hadly, E. A., Dirzo, R., Fortelius, M., Stenseth, N. 2014; 1 (2): 160-170
  • Predicting biodiversity change and averting collapse in agricultural landscapes. Nature Mendenhall, C. D., Karp, D. S., Meyer, C. F., Hadly, E. A., Daily, G. C. 2014; 509 (7499): 213-217

    Abstract

    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 Mendenhall, C. D., Karp, D. S., Meyer, C. F., Hadly, E. A., Daily, G. C. 2014; 509 (7499): 213-?

    Abstract

    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 Web of Science ID 000335454300036

    View details for PubMedID 24739971

  • A call for tiger management using "reserves" of genetic diversity. journal of heredity Bay, R. A., Ramakrishnan, U., Hadly, E. A. 2014; 105 (3): 295-302

    Abstract

    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

  • Introducing the Scientific Consensus on Maintaining Humanity's Life Support Systems in the 21 st Century: Information for Policy Makers ANTHROPOCENE REVIEW Barnosky, A. D., Brown, J. H., Daily, G. C., Dirzo, R., Ehrlich, A. H., Ehrlich, P. R., Eronen, J. T., Fortelius, M., Hadly, E. A., Leopold, E. B., Mooney, H. A., Myers, J., Naylor, R. L., Palumbi, S., Stenseth, N., Wake, M. H. 2014; 1 (1): 78–109
  • Problem solving in the Anthropocene ANTHROPOCENE REVIEW Barnosky, A. D., Hadly, E. A. 2014; 1 (1): 76-77
  • Molecular diagnosis of bird-mediated pest consumption in tropical farmland. SpringerPlus Karp, D. S., Judson, S., Daily, G. C., Hadly, E. A. 2014; 3: 630-?

    Abstract

    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

    View details for PubMedCentralID PMC4216319

  • Molecular diagnosis of bird-mediated pest consumption in tropical farmland. SpringerPlus Karp, D. S., Judson, S., Daily, G. C., Hadly, E. A. 2014; 3: 630-?

    Abstract

    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

    View details for PubMedCentralID PMC4216319

  • Forest bolsters bird abundance, pest control and coffee yield ECOLOGY LETTERS Karp, D. S., Mendenhall, C. D., Sandi, R. F., Chaumont, N., Ehrlich, P. R., Hadly, E. A., Daily, G. C. 2013; 16 (11): 1339-1347

    Abstract

    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 Anich, P. S., Hadly, E. A. 2013; 170 (2): 274-286
  • Sustaining ecosystem functions in a changing world: a call for an integrated approach JOURNAL OF APPLIED ECOLOGY Tomimatsu, H., Sasaki, T., Kurokawa, H., Bridle, J. R., Fontaine, C., Kitano, J., Stouffer, D. B., Vellend, M., Bezemer, T., Fukami, T., Hadly, E. A., van der Heijden, M. A., Kawata, M., Kefi, S., Kraft, N. B., McCann, K. S., Mumby, P. J., Nakashizuka, T., Petchey, O. L., Romanuk, T. N., Suding, K. N., Takimoto, G., Urabe, J., Yachi, S. 2013; 50 (5): 1124–30
  • Morphological Adaptations for Digging and Climate-Impacted Soil Properties Define Pocket Gopher (Thomomys spp.) Distributions. PloS one Marcy, A. E., Fendorf, S., Patton, J. L., Hadly, E. A. 2013; 8 (5)

    Abstract

    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 Adams, R. I., Hadly, E. A. 2013; 27 (1): 133-143
  • Approaching a state shift in Earth's biosphere NATURE Barnosky, A. D., Hadly, E. A., Bascompte, J., Berlow, E. L., Brown, J. H., Fortelius, M., Getz, W. M., Harte, J., Hastings, A., Marquet, P. A., Martinez, N. D., Mooers, A., Roopnarine, P., Vermeij, G., Williams, J. W., Gillespie, R., Kitzes, J., Marshall, C., Matzke, N., Mindell, D. P., Revilla, E., Smith, A. B. 2012; 486 (7401): 52-58

    Abstract

    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 PLOS ONE McMenamin, S. K., Hadly, E. A. 2012; 7 (3)

    Abstract

    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

    View details for PubMedCentralID PMC3299687

  • Genetic variation over 10 000 years in Ctenomys: comparative phylochronology provides a temporal perspective on rarity, environmental change and demography MOLECULAR ECOLOGY Chan, Y. L., Hadly, E. A. 2011; 20 (22): 4592-4605

    Abstract

    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 Terry, R. C., Li, C. (., Hadly, E. A. 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 Adams, R. I., Hadly, E. A. 2010; 70 (3): 296-311
  • Small mammal diversity loss in response to late-Pleistocene climatic change NATURE Blois, J. L., McGuire, J. L., Hadly, E. A. 2010; 465 (7299): 771-U5

    Abstract

    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 MOLECULAR ECOLOGY Pinsky, M. L., Newsome, S. D., Dickerson, B. R., Fang, Y., Van Tuinen, M., Kennett, D. J., Ream, R. R., Hadly, E. A. 2010; 19 (12): 2418-2429

    Abstract

    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 Feranec, R. S., Hadly, E. A., Paytan, A. 2010; 217 (1-2): 43-52
  • Developmental dynamics of Ambystoma tigrinum in a changing landscape. BMC ecology McMenamin, S. K., Hadly, E. A. 2010; 10: 10-?

    Abstract

    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

    View details for PubMedCentralID PMC2861013

  • Source-sink dynamics structure a common montane mammal MOLECULAR ECOLOGY O'Keefe, K., Ramakrishnan, U., van Tuinen, M., Hadly, E. A. 2009; 18 (23): 4775-4789

    Abstract

    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 Hadly, E. A., Spaeth, P. A., Li, C. NATL ACAD SCIENCES. 2009: 19707–19714

    Abstract

    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 Web of Science ID 000271907100012

    View details for PubMedID 19897730

    View details for PubMedCentralID PMC2780937

  • Biogeography, changing climates, and niche evolution PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA Wake, D. B., Hadly, E. A., Ackerly, D. D. 2009; 106: 19631-19636

    View details for DOI 10.1073/pnas.0911097106

    View details for Web of Science ID 000271907100001

    View details for PubMedID 19918080

    View details for PubMedCentralID PMC2780939

  • Do complex population histories drive higher estimates of substitution rate in phylogenetic reconstructions? MOLECULAR ECOLOGY Ramakrishnan, U., Hadly, E. A. 2009; 18 (21): 4341-4343

    Abstract

    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 Spaeth, P. A., Van Tuinen, M., CHAN, Y. L., Terca, D., Hadly, E. A. 2009; 90 (3): 571-584
  • Using phylochronology to reveal cryptic population histories: review and synthesis of 29 ancient DNA studies MOLECULAR ECOLOGY Ramakrishnan, U., Hadly, E. A. 2009; 18 (7): 1310-1330

    Abstract

    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 Blois, J. L., Hadly, E. A. 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 Feranec, R. S., Hadly, E. A., Paytan, A. 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 McMenamin, S. K., Hadly, E. A., Wright, C. K. 2008; 105 (44): 16988-16993

    Abstract

    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

    View details for PubMedCentralID PMC2579365

  • Fire and ice: genetic structure of the Uinta ground squirrel (Spermophilus armatus) across the Yellowstone hotspot MOLECULAR ECOLOGY van Tuinen, M., O'Keefe, K., Ramakrishnan, U., Hadly, E. A. 2008; 17 (7): 1776-1788

    Abstract

    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 Riddle, B. R., Dawson, M. N., Hadly, E. A., Hafner, D. J., Hickerson, M. J., Mantooth, S. J., Yoder, A. D. 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 Blois, J. L., Feranec, R. S., Hadly, E. A. 2008; 35 (4): 602-613
  • Determining landscape use of Holocene mammals using strontium isotopes OECOLOGIA Feranec, R. S., Hadly, E. A., Paytan, A. 2007; 153 (4): 943-950

    Abstract

    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 Newsome, S. D., Etnier, M. A., Gifford-Gonzalez, D., Phillips, D. L., van Tuinen, M., Hadly, E. A., Costa, D. P., Kennett, D. J., Guilderson, T. P., Koch, P. L. 2007; 104 (23): 9709-9714

    Abstract

    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 Bruzgul, J. E., Hadly, E. A. 2007; 16 (2): 139-148
  • Radiocarbon dates from the pleistocene fossil deposits of Samwel Cave, Shasta County, California, USA RADIOCARBON Feranec, R. S., Hadly, E. A., Blois, J. L., Barnosky, A. D., Paytan, A. 2007; 49 (1): 117-121
  • Bayesian estimation of the timing and severity of a population bottleneck from ancient DNA PLOS GENETICS Chan, Y. L., Anderson, C. N., Hadly, E. A. 2006; 2 (4): 451-460

    Abstract

    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

    View details for PubMedCentralID PMC1440876

  • Ancient DNA reveals Holocene loss of genetic diversity in a South American rodent BIOLOGY LETTERS Chan, Y. L., Lacey, E. A., Pearson, O. P., Hadly, E. A. 2005; 1 (4): 423-426

    Abstract

    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

    View details for PubMedCentralID PMC1626362

  • Community inertia of quaternary small mammal assemblages in North America PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA McGill, B. J., Hadly, E. A., Maurer, B. A. 2005; 102 (46): 16701-16706

    Abstract

    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

    View details for PubMedCentralID PMC1283796

  • Detecting past population bottlenecks using temporal genetic data MOLECULAR ECOLOGY Ramakrishnan, U., Hadly, E. A., Mountain, J. L. 2005; 14 (10): 2915-2922

    Abstract

    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 BIOINFORMATICS Anderson, C. N., Ramakrishnan, U., CHAN, Y. L., Hadly, E. A. 2005; 21 (8): 1733-1734

    Abstract

    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://www.stanford.edu/group/hadlylab/ssc.htmlsenka@stanford.edu.

    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. BMC ecology Bruzgul, J. E., Long, W., Hadly, E. A. 2005; 5: 7-?

    Abstract

    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 van Tuinen, M., Ramakrishnan, U., Hadley, E. A. 2004; 362 (1825): 2795-2820

    Abstract

    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

  • Similarities in body size distributions of small-bodied flying vertebrates EVOLUTIONARY ECOLOGY RESEARCH Maurer, B. A., Brown, J. H., Dayan, T., Enquist, B. J., Ernest, S. K., Hadly, E. A., Haskell, J. P., Jablonski, D., Jones, K. E., Kaufman, D. M., Lyons, S. K., Niklas, K. J., Porter, W. P., Roy, K., Smith, F. A., Tiffney, B., Willig, M. R. 2004; 6 (6): 783-797
  • Genetic response to climatic change: Insights from ancient DNA and phylochronology PLOS BIOLOGY Hadly, E. A., Ramakrishnan, U., CHAN, Y. L., Van Tuinen, M., O'Keefe, K., Spaeth, P. A., Conroy, C. J. 2004; 2 (10): 1600-1609

    Abstract

    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

    View details for PubMedCentralID PMC515369

  • Error in estimation of rate and time inferred from the early amniote fossil record and avian molecular clocks JOURNAL OF MOLECULAR EVOLUTION van Tuinen, M., Hadly, E. A. 2004; 59 (2): 267-276

    Abstract

    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 AMERICAN NATURALIST Smith, F. A., Brown, J. H., Haskell, J. P., Lyons, S. K., Alroy, J., Charnov, E. L., Dayan, T., Enquist, B. J., Ernest, S. K., Hadly, E. A., Jones, K. E., Kaufman, D. M., Marquet, P. A., Maurer, B. A., Niklas, K. J., Porter, W. P., Tiffney, B., Willig, M. R. 2004; 163 (5): 672-691

    Abstract

    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 van Tuinen, M., Hadly, E. A. 2004; 95 (3): 200-208

    Abstract

    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 Ernest, S. K., Enquist, B. J., Brown, J. H., Charnov, E. L., Gillooly, J. F., Savage, V., White, E. P., Smith, F. A., Hadly, E. A., Haskell, J. P., Lyons, S. K., Maurer, B. A., Niklas, K. J., Tiffney, B. 2003; 6 (11): 990-995
  • The interface of paleontology and mammalogy: Past, present, and future JOURNAL OF MAMMALOGY Hadly, E. A. 2003; 84 (2): 347-353
  • Ancient DNA evidence of prolonged population persistence with negligible genetic diversity in an endemic tuco-tuco (Ctenomys sociabilis) JOURNAL OF MAMMALOGY Hadly, E. A., Van Tuinen, M., Chan, Y., Heiman, K. 2003; 84 (2): 403-417
  • Mammalian response to global warming on varied temporal scales JOURNAL OF MAMMALOGY Barnosky, A. D., Hadly, E. A., Bell, C. J. 2003; 84 (2): 354-368
  • Mapping the origin of faunal assemblages using strontium isotopes PALEOBIOLOGY Porder, S., Paytan, A., Hadly, E. A. 2003; 29 (2): 197-204
  • PALEOECOLOGY OF SMALL MAMMALS FROM WATERFALL LOCALITY, YELLOWSTONE NATIONAL PARK, WYOMING Steele, T., Hadly, E. TAYLOR & FRANCIS INC. 2003: 100A-101A
  • BIOGEOGRAPHIC AND GENETIC ORIGINS OF THE GREATER YELLOWSTONE ECOSYSTEM MAMMALIAN FAUNA Spaeth, P., Conroy, C. J., Chan, Y., Hadly, E. A. TAYLOR & FRANCIS INC. 2003: 100A
  • Temperate terrestrial vertebrate faunas in North and South America: Interplay of ecology, evolution, and geography with biodiversity CONSERVATION BIOLOGY Barnosky, A. D., Hadly, E. A., Maurer, B. A., Christie, M. I. 2001; 15 (3): 658-674
  • Spatial and temporal patterns of species diversity in montane mammal communities of western North America EVOLUTIONARY ECOLOGY RESEARCH Hadly, E. A., Maurer, B. A. 2001; 3 (4): 477-486
  • Fidelity of terrestrial vertebrate fossils to a modern ecosystem PALAEOGEOGRAPHY PALAEOCLIMATOLOGY PALAEOECOLOGY Hadly, E. A. 1999; 149 (1-4): 389-409
  • 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 Hadly, E. A., Kohn, M. H., Leonard, J. A., Wayne, R. K. 1998; 95 (12): 6893-6896

    Abstract

    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

    View details for PubMedCentralID PMC22676