Robert K Wayne

Princeton University, Princeton, New Jersey, United States

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Publications (244)1262.91 Total impact

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    ABSTRACT: In an era of ever-increasing amounts of whole genome sequence data for individuals and populations, the utility of traditional single nucleotide polymorphisms (SNPs) array-based genome scans is uncertain. We previously performed a SNP array-based genome scan to identify candidate genes under selection in six distinct gray wolf (Canis lupus) ecotypes. Using this information, we designed a targeted capture array for 1040 genes, including all exons and flanking regions, as well as 5000 1 kb non-genic neutral regions and resequenced these regions in 107 wolves. Selection tests revealed striking patterns of variation within candidate genes relative to non-candidate regions and identified potentially functional variants related to local adaptation. We found 27% and 47% of candidate genes from the previous SNP array study had functional changes that were outliers in SweeD and Bayenv analyses, respectively. This result verifies the use of genome wide SNP surveys to tag genes that contain functional variants between populations. We highlight non-synonymous variants in APOB, LIPG, and USH2A that occur in functional domains of these proteins, and that demonstrate high correlation with precipitation seasonality and vegetation. We find Arctic and High Arctic wolf ecotypes have higher numbers of genes under selection, which highlight their conservation value and heightened threat due to climate change. This study demonstrates that combining genome wide genotyping arrays with large scale resequencing and environmental data provides a powerful approach to discern candidate functional variants in natural populations. This article is protected by copyright. All rights reserved.
    Molecular Ecology 11/2015; DOI:10.1111/mec.13467 · 6.49 Impact Factor

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    ABSTRACT: Previous genetic studies of the highly mobile gray wolf (Canis lupus) found population structure that coincides with habitat and phenotype differences. We hypothesized that these ecologically distinct populations (ecotypes) should exhibit signatures of selection in genes related to morphology, coat color, and metabolism. To test these predictions, we quantified population structure related to habitat using a genotyping array to assess variation in 42,036 SNPs in 111 North American gray wolves. Using these SNP data and individual-level measurements of 12 environmental variables, we identified six ecotypes: West Forest, Boreal Forest, Arctic, High Arctic, British Columbia, and Atlantic Forest. Next, we explored signals of selection across these wolf ecotypes through the use of three complementary methods to detect selection: FST /haplotype homozygosity bivariate percentile, BayeScan, and environmentally correlated directional selection with Bayenv. Across all methods, we found consistent signals of selection on genes related to morphology, coat coloration, metabolism, as predicted, as well as vision and hearing. In several high-ranking candidate genes, including LEPR, TYR, and SLC14A2, we found variation in allele frequencies that follow environmental changes in temperature and precipitation, a result that is consistent with local adaptation rather than genetic drift. Our findings show that local adaptation can occur despite gene flow in a highly mobile species and can be detected through a moderately dense genomic scan. These patterns of local adaptation revealed by SNP genotyping likely reflect high fidelity to natal habitats of dispersing wolves, strong ecological divergence among habitats, and moderate levels of linkage in the wolf genome. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    Molecular Ecology 09/2015; DOI:10.1111/mec.13364 · 6.49 Impact Factor
  • R.K. Wayne · Z. Fan · A.H. Freedman ·

    Journal of Veterinary Behavior Clinical Applications and Research 09/2015; 10(5):440. DOI:10.1016/j.jveb.2015.07.010 · 0.96 Impact Factor
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    ABSTRACT: Canine transmissible venereal tumor (CTVT) is a parasitic cancer clone that has propagated for thousands of years via sexual transfer of malignant cells. Little is understood about the mechanisms that converted an ancient tumor into the world's oldest known continuously propagating somatic cell lineage. We created the largest existing catalog of canine genome-wide variation and compared it against two CTVT genome sequences, thereby separating alleles derived from the founder's genome from somatic drivers of clonal transmissibility. We show that CTVT has undergone continuous adaptation to its transmissible allograft niche, with overlapping mutations at every step of immunosurveillance, particularly self-antigen presentation and apoptosis. We also identified chronologically early somatic mutations in oncogenesis- and immune-related genes that may represent key initiators of clonal transmissibility. Thus, we provide the first insights into the specific genomic aberrations that underlie CTVT's dogged perseverance in canids around the world. Published by Cold Spring Harbor Laboratory Press.
    Genome Research 07/2015; DOI:10.1101/gr.190314.115 · 14.63 Impact Factor
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    ABSTRACT: The golden jackal of Africa (Canis aureus) has long been considered a conspecific of jackals distributed throughout Eurasia, with the nearest source populations in the Middle East. However, two recent reports found that mitochondrial haplotypes of some African golden jackals aligned more closely to gray wolves (Canis lupus) [1, 2], which is surprising given the absence of gray wolves in Africa and the phenotypic divergence between the two species. Moreover, these results imply the existence of a previously unrecognized phylogenetically distinct species despite a long history of taxonomic work on African canids. To test the distinct-species hypothesis and understand the evolutionary history that would account for this puzzling result, we analyzed extensive genomic data including mitochondrial genome sequences, sequences from 20 autosomal loci (17 introns and 3 exon segments), microsatellite loci, X- and Y-linked zinc-finger protein gene (ZFX and ZFY) sequences, and whole-genome nuclear sequences in African and Eurasian golden jackals and gray wolves. Our results provide consistent and robust evidence that populations of golden jackals from Africa and Eurasia represent distinct monophyletic lineages separated for more than one million years, sufficient to merit formal recognition as different species: C. anthus (African golden wolf) and C. aureus (Eurasian golden jackal). Using morphologic data, we demonstrate a striking morphologic similarity between East African and Eurasian golden jackals, suggesting parallelism, which may have misled taxonomists and likely reflects uniquely intense interspecific competition in the East African carnivore guild. Our study shows how ecology can confound taxonomy if interspecific competition constrains size diversification. Copyright © 2015 Elsevier Ltd. All rights reserved.
    Current biology: CB 07/2015; 25(16). DOI:10.1016/j.cub.2015.06.060 · 9.57 Impact Factor
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    The Journal of heredity 05/2015; 106(4). DOI:10.1093/jhered/esv028 · 2.09 Impact Factor
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    ABSTRACT: Landscape complexity provides opportunities for local adaptation and creates population genetic structure at limited geographic scales. We determined if fine-scale genetic structure was evident in a population of ringtails (Bassariscus astutus) inhabiting the Guadalupe Mountains, a small, isolated, and ecologically diverse mountain range in the southwest United States. We hypothesized that ringtails would exhibit either a genetic pattern of isolation by distance (IBD), because their small body size would most likely limit dispersal distances, or a pattern of isolation by resistance (IBR), because the topographical complexity of the mountain range would result in complex dispersal patterns. To investigate for the presence of fine-scale genetic structure in this population, we genotyped 153 ringtails at 15 microsatellite loci and described genetic structure using 2 Bayesian clustering techniques. Six genetic clusters were identified revealing complex spatial genetic structure within a localized geographic area. We used partial Mantel tests to test for a correlation between genetic distance and geographic distance or resistance distance but found no evidence for a genetic pattern related to IBD or IBR. We subsequently tested for an association between genetic structure and isolation by environment (IBE) using a discriminant function analysis and classified a high proportion of individuals (> 91%) to their observed genetic cluster based exclusively on landscape features. We also used a nonparametric, multivariate analysis of variance to further explore the role of land-cover type and found that plant association explained 26% of the genetic variation. These results suggest that IBE influences the genetic structure of ringtails at local geographic scales, a finding that deserves consideration in conservation planning.
    Journal of Mammalogy 04/2015; 96(2):257-268. DOI:10.1093/jmammal/gyv050 · 1.84 Impact Factor
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    ABSTRACT: One of the hallmarks of eusociality is that workers forego their own reproduction to assist their mother in raising siblings. This seemingly altruistic behaviour may benefit workers if gains in indirect fitness from rearing siblings outweigh the loss of direct fitness. If worker presence is advantageous to mothers, however, eusociality may evolve without net benefits to workers. Indirect fitness benefits are often cited as evidence for the importance of inclusive fitness in eusociality, but have rarely been measured in natural populations. We compared inclusive fitness of alternative social strategies in the tropical sweat bee, Megalopta genalis, for which eusociality is optional. Our results show that workers have significantly lower inclusive fitness than females that found their own nests. In mathematical simulations based on M. genalis field data, eusociality cannot evolve with reduced intra-nest relatedness. The simulated distribution of alternative social strategies matched observed distributions of M. genalis social strategies when helping behaviour was simulated as the result of maternal manipulation, but not as worker altruism. Thus, eusociality in M. genalis is best explained through kin selection, but the underlying mechanism is likely maternal manipulation. © 2015 The Author(s) Published by the Royal Society. All rights reserved.
    Proceedings of the Royal Society B: Biological Sciences 03/2015; 282(1803). DOI:10.1098/rspb.2014.2886 · 5.05 Impact Factor
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    ABSTRACT: Anticoagulant rodenticides (ARs) are increasingly recognized as a threat to nontarget wildlife. High exposure to ARs has been documented globally in nontarget predatory species and linked to the high prevalence of an ectoparasitic disease, notoedric mange. In southern California, mange associated with AR exposure has been the proximate cause of a bobcat (Lynx rufus) population decline. We measured AR exposure in bobcats from two areas in southern California, examining seasonal, demographic and spatial risk factors across landscapes including natural and urbanized areas. The long-term study included bobcats sampled over a 16-year period (1997-2012) and a wide geographic area. We sampled blood (N = 206) and liver (N = 172) to examine exposure ante- and post-mortem. We detected high exposure prevalence (89 %, liver; 39 %, blood) and for individuals with paired liver and blood data (N = 64), 92 % were exposed. Moreover, the animals with the most complete sampling were exposed most frequently to three or more compounds. Toxicant exposure was associated with commercial, residential, and agricultural development. Bobcats of both sexes and age classes were found to be at high risk of exposure, and we documented fetal transfer of multiple ARs. We found a strong association between certain levels of exposure (ppm), and between multiple AR exposure events, and notoedric mange. AR exposure was prevalent throughout both regions sampled and throughout the 16-year time period in the long-term study. ARs pose a substantial threat to bobcats, and likely other mammalian and avian predators, living at the urban-wildland interface.
    Ecotoxicology 02/2015; 24(4). DOI:10.1007/s10646-015-1429-5 · 2.71 Impact Factor
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    ABSTRACT: The Genome 10K Project was established in 2009 by a consortium of biologists and genome scientists determined to facilitate the sequencing and analysis of the complete genomes of 10,000 vertebrate species. Since then the number of selected and initiated species has risen from ∼26 to 277 sequenced or ongoing with funding, an approximately tenfold increase in five years. Here we summarize the advances and commitments that have occurred by mid-2014 and outline the achievements and present challenges of reaching the 10,000-species goal. We summarize the status of known vertebrate genome projects, recommend standards for pronouncing a genome as sequenced or completed, and provide our present and future vision of the landscape of Genome 10K. The endeavor is ambitious, bold, expensive, and uncertain, but together the Genome 10K Consortium of Scientists and the worldwide genomics community are moving toward their goal of delivering to the coming generation the gift of genome empowerment for many vertebrate species.
  • Karen Kapheim · Peter Nonacs · A. R. Smith · Robert K. Wayne · William Wcislo ·
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    ABSTRACT: One of the key features of eusociality is the seemingly altruistic behavior of workers who forego their own reproduction to assist their mother in raising siblings. This behavior may be adaptive if gains in indirect fitness from rearing siblings outweigh the loss of direct fitness. If the presence of workers is sufficiently advantageous to mothers, however, worker fitness may not be the primary driver of eusocial evolution. This distinction is important, because indirect fitness benefits are often cited as prima facie evidence for the importance of kin selection in eusociality, but suitably large indirect fitness gains have rarely been demonstrated in natural populations. Here we compare the inclusive fitness of alternative social strategies in the tropical sweat bee, Megalopta genalis, for which eusocial nesting is optional. We show that inclusive fitness is similar among reproductive females with and without workers, but workers in eusocial nests have significantly lower inclusive fitness than would have been expected if they departed to found their own nests. In support for the role of kin selection in eusocial evolution, mathematical simulations based on M. genalis field data found eusociality cannot evolve with reduced intra-nest relatedness. In addition, the simulated distribution of alternative social strategies matched observed distributions of M. genalis social strategies when simulated as a maternal trait (i.e., manipulation), but not when helping behavior was coded as a worker trait (i.e., altruism). Thus, eusociality in M. genalis is best explained through kin selection, but the mechanism being selected is likely maternal manipulation.
    Entomological Society of America Annual Meeting 2014; 11/2014
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    ABSTRACT: Urbanization profoundly impacts animal populations by causing isolation, increased susceptibility to disease, and exposure to toxicants. Genetic effects include reduced effective population size, increased population substructure, and decreased adaptive potential. We investigated the influence that urbanization and a disease epizootic had on the population genetics of bobcats (Lynx rufus) distributed across a highly fragmented urban landscape. We genotyped more than 300 bobcats, sampled from 1996-2012, for variation at nine neutral and seven immune gene-linked microsatellite loci. We found that two freeways are significant barriers to gene flow. Further, a 3-year disease epizootic, associated with secondary anticoagulant rodenticide exposure, caused a population bottleneck that led to significant genetic differentiation between pre- and post-disease populations that was greater than that between populations separated by major freeways for > 60 years. However, balancing selection acted on immune-linked loci during the epizootic, maintaining variation at functional regions. Conservation assessments need to assay loci that are potentially under selection in order to better preserve the adaptive potential of populations at the urban-wildland interface. Further, inter-connected regions that contain appropriate habitat for wildlife will be critical to the long-term viability of animal populations in urban landscapes.This article is protected by copyright. All rights reserved.
    Evolutionary Applications 10/2014; 8(1). DOI:10.1111/eva.12226 · 3.90 Impact Factor
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    ABSTRACT: Large carnivores can be particularly sensitive to the effects of habitat fragmentation on genetic diversity [1, 2]. The Santa Monica Mountains (SMMs), a large natural area within Greater Los Angeles, is completely isolated by urban development and the 101 freeway to the north. Yet the SMMs support a population of mountain lions (Puma concolor), a very rare example of a large carnivore persisting within the boundaries of a megacity. GPS locations of radio-collared lions indicate that freeways are a near-absolute barrier to movement. We genotyped 42 lions using 54 microsatellite loci and found that genetic diversity in SMM lions, prior to 2009, was lower than that for any population in North America except in southern Florida, where inbreeding depression led to reproductive failure [3-5]. We document multiple instances of father-daughter inbreeding and high levels of intraspecific strife, including the unexpected behavior of a male killing two of his offspring and a mate and his son killing two of his brothers. Overall, no individuals from the SMMs have successfully dispersed. Gene flow is critical for this population, and we show that a single male immigrated in 2009, successfully mated, and substantially enhanced genetic diversity. Our results imply that individual behaviors, most likely caused by limited area and reduced opportunities to disperse, may dominate the fate of small, isolated populations of large carnivores. Consequently, comprehensive behavioral monitoring can suggest novel solutions for the persistence of small populations, such as the transfer of individuals across dispersal barriers.
    Current Biology 08/2014; 24(17). DOI:10.1016/j.cub.2014.07.029 · 9.57 Impact Factor
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    ABSTRACT: The Tibetan grey wolf (Canis lupus chanco) occupies habitats on the Qinghai-Tibet Plateau, a high altitude (>3000 m) environment where low oxygen tension exerts unique selection pressure on individuals to adapt to hypoxic conditions. To identify genes involved in hypoxia adaptation, we generated complete genome sequences of nine Chinese wolves from high and low altitude populations at an average coverage of 25× coverage. We found that, beginning about 55,000 years ago, the highland Tibetan grey wolf suffered a more substantial population decline than lowland wolves. Positively selected hypoxia-related genes in highland wolves are enriched in the HIF signaling pathway (P = 1.57E-6), ATP binding (P = 5.62E-5), and response to an oxygen-containing compound (P≤5.30E-4). Of these positively selected hypoxia-related genes, three genes (EPAS1, ANGPT1, and RYR2) had at least one specific fixed non-synonymous SNP in highland wolves based on the nine genome data. Our re-sequencing studies on a large panel of individuals showed a frequency difference greater than 58% between highland and lowland wolves for these specific fixed non-synonymous SNPs and a high degree of LD surrounding the three genes, which imply strong selection. Past studies have shown that EPAS1 and ANGPT1 are important in the response to hypoxic stress, and RYR2 is involved in heart function. These three genes also exhibited significant signals of natural selection in high altitude human populations, which suggest similar evolutionary constraints on natural selection in wolves and humans of the Qinghai-Tibet Plateau.
    PLoS Genetics 07/2014; 10(7):e1004466. DOI:10.1371/journal.pgen.1004466 · 7.53 Impact Factor
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    ABSTRACT: Background Although a variety of genetic changes have been implicated in causing phenotypic differences among dogs, the role of copy number variants (CNVs) and their impact on phenotypic variation is still poorly understood. Further, very limited knowledge exists on structural variation in the gray wolf, the ancestor of the dog, or other closely related wild canids. Documenting CNVs variation in wild canids is essential to identify ancestral states and variation that may have appeared after domestication. Results In this work, we genotyped 1,611 dog CNVs in 23 wolf-like canids (4 purebred dogs, one dingo, 15 gray wolves, one red wolf, one coyote and one golden jackal) to identify CNVs that may have arisen after domestication. We have found an increase in GC-rich regions close to the breakpoints and around 1 kb away from them suggesting that some common motifs might be associated with the formation of CNVs. Among the CNV regions that showed the largest differentiation between dogs and wild canids we found 12 genes, nine of which are related to two known functions associated with dog domestication; growth (PDE4D, CRTC3 and NEB) and neurological function (PDE4D, EML5, ZNF500, SLC6A11, ELAVL2, RGS7 and CTSB). Conclusions Our results provide insight into the evolution of structural variation in canines, where recombination is not regulated by PRDM9 due to the inactivation of this gene. We also identified genes within the most differentiated CNV regions between dogs and wolves, which could reflect selection during the domestication process. Electronic supplementary material The online version of this article (doi:10.1186/1471-2164-15-465) contains supplementary material, which is available to authorized users.
    BMC Genomics 06/2014; 15(1):465. DOI:10.1186/1471-2164-15-465 · 3.99 Impact Factor
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    ABSTRACT: Although native to the southeastern United States, the red swamp crayfish (Procambarus clarkii) has become established worldwide through accidental and intentional actions by humans. In the Santa Monica Mountains of southern California, the presence of the omnivorous crayfish is associated with the absence or reduced abundance of native amphibians. The original source of P. clarkii in southern California is unknown; however genetic analysis can be used to determine sources of invasion. We sequenced 16S rRNA subunit and cytochrome oxidase I (COI) mitochondrial genes to trace the origins of P. clarkii in the Santa Monica Mountains. The resulting haplotype network of the combined COI and 16S rRNA subunit genes showed 19 distinct haplotypes and suggested multiple introductions of crayfish to the Santa Monica Mountains from possible source locations in Texas, Florida and Louisiana. Identifying original sources and mechanisms of introduction can slow and prevent further expansion of P. clarkii.
    Aquatic Invasions 04/2014; 9(2):211-219. DOI:10.3391/ai.2014.9.2.10 · 1.61 Impact Factor
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    ABSTRACT: To identify genetic changes underlying dog domestication and reconstruct their early evolutionary history, we generated high-quality genome sequences from three gray wolves, one from each of the three putative centers of dog domestication, two basal dog lineages (Basenji and Dingo) and a golden jackal as an outgroup. Analysis of these sequences supports a demographic model in which dogs and wolves diverged through a dynamic process involving population bottlenecks in both lineages and post-divergence gene flow. In dogs, the domestication bottleneck involved at least a 16-fold reduction in population size, a much more severe bottleneck than estimated previously. A sharp bottleneck in wolves occurred soon after their divergence from dogs, implying that the pool of diversity from which dogs arose was substantially larger than represented by modern wolf populations. We narrow the plausible range for the date of initial dog domestication to an interval spanning 11-16 thousand years ago, predating the rise of agriculture. In light of this finding, we expand upon previous work regarding the increase in copy number of the amylase gene (AMY2B) in dogs, which is believed to have aided digestion of starch in agricultural refuse. We find standing variation for amylase copy number variation in wolves and little or no copy number increase in the Dingo and Husky lineages. In conjunction with the estimated timing of dog origins, these results provide additional support to archaeological finds, suggesting the earliest dogs arose alongside hunter-gathers rather than agriculturists. Regarding the geographic origin of dogs, we find that, surprisingly, none of the extant wolf lineages from putative domestication centers is more closely related to dogs, and, instead, the sampled wolves form a sister monophyletic clade. This result, in combination with dog-wolf admixture during the process of domestication, suggests that a re-evaluation of past hypotheses regarding dog origins is necessary.
    PLoS Genetics 01/2014; 10(1):e1004016. DOI:10.1371/journal.pgen.1004016 · 7.53 Impact Factor
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    ABSTRACT: Genomic resources developed for domesticated species provide powerful tools for studying the evolutionary history of their wild relatives. Here we use 61K single-nucleotide polymorphisms (SNPs) evenly spaced throughout the canine nuclear genome to analyse evolutionary relationships among the three largest European populations of grey wolves in comparison with other populations worldwide, and investigate genome-wide effects of demographic bottlenecks and signatures of selection. European wolves have a discontinuous range, with large and connected populations in Eastern Europe and relatively smaller, isolated populations in Italy and the Iberian Peninsula. Our results suggest a continuous decline in wolf numbers in Europe since the Late Pleistocene, and long-term isolation and bottlenecks in the Italian and Iberian populations following their divergence from the Eastern European population. The Italian and Iberian populations have low genetic variability and high linkage disequilibrium, but relatively few autozygous segments across the genome. This last characteristic clearly distinguishes them from populations that underwent recent drastic demographic declines or founder events, and implies long-term bottlenecks in these two populations. Although genetic drift due to spatial isolation and bottlenecks seems to be a major evolutionary force diversifying the European populations, we detected 35 loci that are putatively under diversifying selection. Two of these loci flank the canine platelet-derived growth factor gene, which affects bone growth and may influence differences in body size between wolf populations. This study demonstrates the power of population genomics for identifying genetic signals of demographic bottlenecks and detecting signatures of directional selection in bottlenecked populations, despite their low background variability.Heredity advance online publication, 18 December 2013; doi:10.1038/hdy.2013.122.
    Heredity 12/2013; 112(4). DOI:10.1038/hdy.2013.122 · 3.81 Impact Factor
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    ABSTRACT: The geographic and temporal origins of the domestic dog remain controversial, as genetic data suggest a domestication process in East Asia beginning 15,000 years ago, whereas the oldest doglike fossils are found in Europe and Siberia and date to >30,000 years ago. We analyzed the mitochondrial genomes of 18 prehistoric canids from Eurasia and the New World, along with a comprehensive panel of modern dogs and wolves. The mitochondrial genomes of all modern dogs are phylogenetically most closely related to either ancient or modern canids of Europe. Molecular dating suggests an onset of domestication there 18,800 to 32,100 years ago. These findings imply that domestic dogs are the culmination of a process that initiated with European hunter-gatherers and the canids with whom they interacted.
    Science 11/2013; 342(6160):871-874. DOI:10.1126/science.1243650 · 33.61 Impact Factor

Publication Stats

17k Citations
1,262.91 Total Impact Points


  • 2015
    • Princeton University
      • Department of Ecology and Evolutionary Biology
      Princeton, New Jersey, United States
  • 1991-2015
    • University of California, Los Angeles
      • Department of Ecology and Evolutionary Biology
      Los Ángeles, California, United States
    • NCI-Frederick
      Фредерик, Maryland, United States
  • 2009-2010
    • Cornell University
      • Department of Biological Statistics and Computational Biology
      Ithaca, New York, United States
  • 1992-2009
    • Zoological Society of London
      • Institute of Zoology
      Londinium, England, United Kingdom
  • 1986-2009
    • Johns Hopkins University
      • Department of Earth and Planetary Sciences
      Baltimore, Maryland, United States
  • 2006
    • National Human Genome Research Institute
      Maryland, United States
  • 2004
    • University of Oxford
      Oxford, England, United Kingdom
  • 2003
    • University of Virginia
      Charlottesville, Virginia, United States
  • 2001
    • Sonoma State University
      • Department of Biology
      Rohnert Park, CA, United States
    • Stockholm University
      • Archaeological Research Laboratory
      Tukholma, Stockholm, Sweden
  • 1999
    • Indiana University Bloomington
      • Department of Biology
      Bloomington, IN, United States
  • 1994
    • University of California, Davis
      • Department of Pathology, Microbiology and Immunology (VM)
      Davis, CA, United States
  • 1986-1987
    • National Cancer Institute (USA)
      • Laboratory of Human Carcinogenesis
      베서스다, Maryland, United States