skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Demographic history shapes North American gray wolf genomic diversity and informs species' conservation
Abstract Effective population size estimates are critical information needed for evolutionary predictions and conservation decisions. This is particularly true for species with social factors that restrict access to breeding or experience repeated fluctuations in population size across generations. We investigated the genomic estimates of effective population size along with diversity, subdivision, and inbreeding from 162,109 minimally filtered and 81,595 statistically neutral and unlinked SNPs genotyped in 437 grey wolf samples from North America collected between 1986 and 2021. We found genetic structure across North America, represented by three distinct demographic histories of western, central, and eastern regions of the continent. Further, grey wolves in the northern Rocky Mountains have lower genomic diversity than wolves of the western Great Lakes and have declined over time. Effective population size estimates revealed the historical signatures of continental efforts of predator extermination, despite a quarter century of recovery efforts. We are the first to provide molecular estimates of effective population size across distinct grey wolf populations in North America, which ranged betweenNe ~ 275 and 3050 since early 1980s. We provide data that inform managers regarding the status and importance of effective population size estimates for grey wolf conservation, which are on average 5.2–9.3% of census estimates for this species. We show that while grey wolves fall above minimum effective population sizes needed to avoid extinction due to inbreeding depression in the short term, they are below sizes predicted to be necessary to avoid long‐term risk of extinction.  more » « less
Award ID(s):
1939399
PAR ID:
10563263
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ;
Publisher / Repository:
Molecular Ecology - Wiley
Date Published:
Journal Name:
Molecular Ecology
Volume:
33
Issue:
3
ISSN:
0962-1083
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract The grey wolf (Canis lupus) was the first species to give rise to a domestic population, and they remained widespread throughout the last Ice Age when many other large mammal species went extinct. Little is known, however, about the history and possible extinction of past wolf populations or when and where the wolf progenitors of the present-day dog lineage (Canis familiaris) lived1–8. Here we analysed 72 ancient wolf genomes spanning the last 100,000 years from Europe, Siberia and North America. We found that wolf populations were highly connected throughout the Late Pleistocene, with levels of differentiation an order of magnitude lower than they are today. This population connectivity allowed us to detect natural selection across the time series, including rapid fixation of mutations in the geneIFT8840,000–30,000 years ago. We show that dogs are overall more closely related to ancient wolves from eastern Eurasia than to those from western Eurasia, suggesting a domestication process in the east. However, we also found that dogs in the Near East and Africa derive up to half of their ancestry from a distinct population related to modern southwest Eurasian wolves, reflecting either an independent domestication process or admixture from local wolves. None of the analysed ancient wolf genomes is a direct match for either of these dog ancestries, meaning that the exact progenitor populations remain to be located. 
    more » « less
  2. Nielsen, Rasmus (Ed.)
    Abstract Island ecosystems provide natural laboratories to assess the impacts of isolation on population persistence. However, most studies of persistence have focused on a single species, without comparisons to other organisms they interact with in the ecosystem. The case study of moose and gray wolves on Isle Royale allows for a direct contrast of genetic variation in isolated populations that have experienced dramatically differing population trajectories over the past decade. Whereas the Isle Royale wolf population recently declined nearly to extinction due to severe inbreeding depression, the moose population has thrived and continues to persist, despite having low genetic diversity and being isolated for ∼120 years. Here, we examine the patterns of genomic variation underlying the continued persistence of the Isle Royale moose population. We document high levels of inbreeding in the population, roughly as high as the wolf population at the time of its decline. However, inbreeding in the moose population manifests in the form of intermediate-length runs of homozygosity suggestive of historical inbreeding and purging, contrasting with the long runs of homozygosity observed in the smaller wolf population. Using simulations, we confirm that substantial purging has likely occurred in the moose population. However, we also document notable increases in genetic load, which could eventually threaten population viability over the long term. Overall, our results demonstrate a complex relationship between inbreeding, genetic diversity, and population viability that highlights the use of genomic datasets and computational simulation tools for understanding the factors enabling persistence in isolated populations. 
    more » « less
  3. Abstract Pleistocene diversity was much higher than today, for example there were three distinct wolf morphotypes (dire, gray, Beringian) in North America versus one today (gray). Previous fossil evidence suggested that these three groups overlapped ecologically, but split the landscape geographically. The Natural Trap Cave (NTC) fossil site in Wyoming,USAis an ideally placed late Pleistocene site to study the geographical movement of species from northern to middle North America before, during, and after the last glacial maximum. Until now, it has been unclear what type of wolf was present atNTC. We analyzed morphometrics of three wolf groups (dire, extant North American gray, Alaskan Beringian) to determine which wolves were present atNTCand what this indicates about wolf diversity and migration in Pleistocene North America. Results showNTCwolves group with Alaskan Beringian wolves. This provides the first morphological evidence for Beringian wolves in mid‐continental North America. Their location atNTCand their radiocarbon ages suggest that they followed a temporary channel through the glaciers. Results suggest high levels of competition and diversity in Pleistocene North American wolves. The presence of mid‐continental Beringian morphotypes adds important data for untangling the history of immigration and evolution ofCanisin North America. 
    more » « less
  4. null (Ed.)
    Recent advances in genomics and palaeontology have begun to unravel the complex evolutionary history of the gray wolf, Canis lupus . Still, much of their phenotypic variation across time and space remains to be documented. We examined the limb morphology of the fossil and modern North American gray wolves from the late Quaternary (< ca 70 ka) to better understand their postcranial diversity through time. We found that the late-Pleistocene gray wolves were characterized by short-leggedness on both sides of the Cordilleran–Laurentide ice sheets, and that this trait survived well into the Holocene despite the collapse of Pleistocene megafauna and disappearance of the ‘Beringian wolf' from Alaska. By contrast, extant populations in the Midwestern USA and northwestern North America are distinguished by their elongate limbs with long distal segments, which appear to have evolved during the Holocene possibly in response to a new level or type of prey depletion. One of the consequences of recent extirpation of the Plains ( Canis lupus nubilus ) and Mexican wolves ( C. l. baileyi ) from much of the USA is an unprecedented loss of postcranial diversity through removal of short-legged forms. Conservation of these wolves is thus critical to restoration of the ecophenotypic diversity and evolutionary potential of gray wolves in North America. 
    more » « less
  5. INTRODUCTION The Anthropocene is marked by an accelerated loss of biodiversity, widespread population declines, and a global conservation crisis. Given limited resources for conservation intervention, an approach is needed to identify threatened species from among the thousands lacking adequate information for status assessments. Such prioritization for intervention could come from genome sequence data, as genomes contain information about demography, diversity, fitness, and adaptive potential. However, the relevance of genomic data for identifying at-risk species is uncertain, in part because genetic variation may reflect past events and life histories better than contemporary conservation status. RATIONALE The Zoonomia multispecies alignment presents an opportunity to systematically compare neutral and functional genomic diversity and their relationships to contemporary extinction risk across a large sample of diverse mammalian taxa. We surveyed 240 species spanning from the “Least Concern” to “Critically Endangered” categories, as published in the International Union for Conservation of Nature’s Red List of Threatened Species. Using a single genome for each species, we estimated historical effective population sizes ( N e ) and distributions of genome-wide heterozygosity. To estimate genetic load, we identified substitutions relative to reconstructed ancestral sequences, assuming that mutations at evolutionarily conserved sites and in protein-coding sequences, especially in genes essential for viability in mice, are predominantly deleterious. We examined relationships between the conservation status of species and metrics of heterozygosity, demography, and genetic load and used these data to train and test models to distinguish threatened from nonthreatened species. RESULTS Species with smaller historical N e are more likely to be categorized as at risk of extinction, suggesting that demography, even from periods more than 10,000 years in the past, may be informative of contemporary resilience. Species with smaller historical N e also carry proportionally higher burdens of weakly and moderately deleterious alleles, consistent with theoretical expectations of the long-term accumulation and fixation of genetic load under strong genetic drift. We found weak support for a causative link between fixed drift load and extinction risk; however, other types of genetic load not captured in our data, such as rare, highly deleterious alleles, may also play a role. Although ecological (e.g., physiological, life-history, and behavioral) variables were the best predictors of extinction risk, genomic variables nonrandomly distinguished threatened from nonthreatened species in regression and machine learning models. These results suggest that information encoded within even a single genome can provide a risk assessment in the absence of adequate ecological or population census data. CONCLUSION Our analysis highlights the potential for genomic data to rapidly and inexpensively gauge extinction risk by leveraging relationships between contemporary conservation status and genetic variation shaped by the long-term demographic history of species. As more resequencing data and additional reference genomes become available, estimates of genetic load, estimates of recent demographic history, and accuracy of predictive models will improve. We therefore echo calls for including genomic information in assessments of the conservation status of species. Genomic information can help predict extinction risk in diverse mammalian species. Across 240 mammals, species with smaller historical N e had lower genetic diversity, higher genetic load, and were more likely to be threatened with extinction. Genomic data were used to train models that predict whether a species is threatened, which can be valuable for assessing extinction risk in species lacking ecological or census data. [Animal silhouettes are from PhyloPic] 
    more » « less