skip to main content

Title: Species' attributes predict the relative magnitude of ecological and genetic recovery following mass mortality
Theoretically, species' characteristics should allow estimation of dispersal potential and, in turn, explain levels of population genetic differentiation. However, a mismatch between traits and genetic patterns is often reported for marine species, and interpreted as evidence that life-history traits do not influence dispersal. Here, we couple ecological and genomic methods to test the hypothesis that species with attributes favouring greater dispersal potential—e.g., longer pelagic duration, higher fecundity and larger population size—have greater realized dispersal overall. We used a natural experiment created by a large-scale and multispecies mortality event which created a “clean slate” on which to study recruitment dynamics, thus simplifying a usually complex problem. We surveyed four species of differing dispersal potential to quantify the abundance and distribution of recruits and to genetically assign these recruits to probable parental sources. Species with higher dispersal potential recolonized a broader extent of the impacted range, did so more quickly and recovered more genetic diversity than species with lower dispersal potential. Moreover, populations of taxa with higher dispersal potential exhibited more immigration (71%–92% of recruits) than taxa with lower dispersal potential (17%–44% of recruits). By linking ecological with genomic perspectives, we demonstrate that a suite of interacting life-history and demographic attributes do influence species' realized dispersal and genetic neighbourhoods. To better understand species' resilience and recovery in this time of global change, integrative eco-evolutionary approaches are needed to more rigorously evaluate the effect of dispersal-linked attributes on realized dispersal and population genetic differentiation.  more » « less
Award ID(s):
1737381 1243970
Author(s) / Creator(s):
; ; ; ;
Date Published:
Journal Name:
Molecular Ecology
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. 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
  2. Abstract

    Understanding population genetic structure is key to developing predictions about species susceptibility to environmental change, such as habitat fragmentation and climate change. It has been theorized that life‐history traits may constrain some species in their dispersal and lead to greater signatures of population genetic structure. In this study, we use a quantitative comparative approach to assess if patterns of population genetic structure in bees are driven by three key species‐level life‐history traits: body size, sociality, and diet breadth. Specifically, we reviewed the current literature on bee population genetic structure, as measured by the differentiation indices Nei'sGST,Hedrick'sGST, and Jost'sD. We then used phylogenetic generalised linear models to estimate the correlation between the evolution of these traits and patterns of genetic differentiation. Our analyses revealed a negative and significant effect of body size on genetic structure, regardless of differentiation index utilized. For Hedrick'sGSTand Jost'sD, we also found a significant impact of sociality, where social species exhibited lower levels of differentiation than solitary species. We did not find an effect of diet specialization on population genetic structure. Overall, our results suggest that physical dispersal or other functions related to body size are among the most critical for mediating population structure for bees. We further highlight the importance of standardizing population genetic measures to more easily compare studies and to identify the most susceptible species to landscape and climatic changes.

    more » « less
  3. Abstract

    Central Mexico is characterized by a complex topography that is the result of historic and contemporary tectonic and climatic factors. These events have influenced the evolutionary history of numerous freshwater fishes in the region. Nonetheless, recent studies have shown that life‐history traits and ecological characteristics of species may influence dispersal capabilities and the degree of genetic connectivity.Goodea(Cyprinodontiformes: Goodeidae) is one of the most widely distributed and environmentally tolerant genera of goodeids. In this study, the authors analysed variation in the mitochondrial cytochrome b gene to evaluate the phylogeographic relationships, genetic structure, genetic diversity and demographic history ofGoodeafrom across its distribution range. They found low genetic differentiation and identified shared haplotypes among several regions. Geographic segregation was found in samples southwest and northeast of the Lower Lerma region, with some internal isolated groups showing phylogeographic differentiation and unique haplotypes. The AMOVA best explained genetic structure when grouped by haplogroups rather than when grouped by recognized biogeographic regions. Several regions showed null genetic diversity, raising the possibility of dispersal mediated by humans. Finally, Bayesian Skyline Plot analysis showed a population expansion for the Southwest haplogroup, except for the Armería population and sub‐group II of the Northeast haplogroup. All this suggests a recent colonization ofGoodea atripinnisthroughout some of the biogeographic regions currently inhabited by this species.

    more » « less
  4. Abstract

    Understanding the factors that govern variation in genetic structure across species is key to the study of speciation and population genetics. Genetic structure has been linked to several aspects of life history, such as foraging strategy, habitat association, migration distance, and dispersal ability, all of which might influence dispersal and gene flow. Comparative studies of population genetic data from species with differing life histories provide opportunities to tease apart the role of dispersal in shaping gene flow and population genetic structure. Here, we examine population genetic data from sets of bird species specialized on a series of Amazonian habitat types hypothesized to filter for species with dramatically different dispersal abilities: stable upland forest, dynamic floodplain forest, and highly dynamic riverine islands. Using genome‐wide markers, we show that habitat type has a significant effect on population genetic structure, with species in upland forest, floodplain forest, and riverine islands exhibiting progressively lower levels of structure. Although morphological traits used as proxies for individual‐level dispersal ability did not explain this pattern, population genetic measures of gene flow are elevated in species from more dynamic riverine habitats. Our results suggest that the habitat in which a species occurs drives the degree of population genetic structuring via its impact on long‐term fluctuations in levels of gene flow, with species in highly dynamic habitats having particularly elevated gene flow. These differences in genetic variation across taxa specialized in distinct habitats may lead to disparate responses to environmental change or habitat‐specific diversification dynamics over evolutionary time scales.

    more » « less
  5. Abstract

    Organismal traits such as ecological specialization and migratory behaviour may affect colonization potential, population persistence and degree of isolation, factors that determine the composition and genetic structure of communities. However, studies focusing on community assembly rarely consider these factors jointly. We sequenced 16 nuclear genes and one mitochondrial gene from Caucasian and European populations of 30 forest‐dwelling avian species that represent diverse ecological (specialist–generalist) and behavioural (migratory‐resident) backgrounds. We tested the effects of organismal traits on population divergence and community assembly in the Caucasus forest, a continental mountain island setting. We found that (i) there is no concordance in divergence times between the Caucasus forest bird populations and their European counterparts, (ii) habitat specialists tend to be more divergent than generalists and (iii) residents tend to be more divergent than migrants. Thus, specialists and residents contribute to the high level of endemism of Caucasus forest avifauna more than do generalists and migrants. Patterns of genetic differentiation are better explained by differences in effective population sizes, an often overlooked factor in comparative studies of phylogeography and speciation, than by divergence times or levels of gene flow. Our results suggest that the Caucasus forest avifauna was assembled through time via dispersal and/or multiple vicariant events, rather than originating simultaneously via a single isolation event. Our study is one of the first multilocus, multispecies analyses revealing how ecological and migratory traits impact the evolutionary history of community formation on a continental island.

    more » « less