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  1. Abstract

    Low‐coverage whole‐genome sequencing (WGS) is increasingly used for the study of evolution and ecology in both model and non‐model organisms; however, effective application of low‐coverage WGS data requires the implementation of probabilistic frameworks to account for the uncertainties in genotype likelihoods.

    Here, we present a probabilistic framework for using genotype likelihoods for standard population assignment applications. Additionally, we derive the Fisher information for allele frequency from genotype likelihoods and use that to describe a novel metric, theeffective sample size, which figures heavily in assignment accuracy. We make these developments available for application through WGSassign, an open‐source software package that is computationally efficient for working with whole‐genome data.

    Using simulated and empirical data sets, we demonstrate the behaviour of our assignment method across a range of population structures, sample sizes and read depths. Through these results, we show that WGSassign can provide highly accurate assignment, even for samples with low average read depths (<0.01X) and among weakly differentiated populations.

    Our simulation results highlight the importance of equalizing the effective sample sizes among source populations in order to achieve accurate population assignment with low‐coverage WGS data. We further provide study design recommendations for population assignment studies and discuss the broad utility of effective sample size for studies using low‐coverage WGS data.

     
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  2. Abstract

    Identifying genetic conservation units (CUs) in threatened species is critical for the preservation of adaptive capacity and evolutionary potential in the face of climate change. However, delineating CUs in highly mobile species remains a challenge due to high rates of gene flow and genetic signatures of isolation by distance. Even when CUs are delineated in highly mobile species, the CUs often lack key biological information about what populations have the most conservation need to guide management decisions. Here we implement a framework for CU identification in the Canada Warbler (Cardellina canadensis), a migratory bird species of conservation concern, and then integrate demographic modelling and genomic offset to guide conservation decisions. We find that patterns of whole genome genetic variation in this highly mobile species are primarily driven by putative adaptive variation. Identification of CUs across the breeding range revealed that Canada Warblers fall into two evolutionarily significant units (ESU), and three putative adaptive units (AUs) in the South, East, and Northwest. Quantification of genomic offset, a metric of genetic changes necessary to maintain current gene–environment relationships, revealed significant spatial variation in climate vulnerability, with the Northwestern AU being identified as the most vulnerable to future climate change. Alternatively, quantification of past population trends within each AU revealed the steepest population declines have occurred within the Eastern AU. Overall, we illustrate that genomics‐informed CUs provide a strong foundation for identifying current and future regional threats that can be used to inform management strategies for a highly mobile species in a rapidly changing world.

     
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  3. Abstract

    Migration is driven by a combination of environmental and genetic factors, but many questions remain about those drivers. Potential interactions between genetic and environmental variants associated with different migratory phenotypes are rarely the focus of study. We pair low coverage whole genome resequencing with a de novo genome assembly to examine population structure, inbreeding, and the environmental factors associated with genetic differentiation between migratory and resident breeding phenotypes in a species of conservation concern, the western burrowing owl (Athene cunicularia hypugaea). Our analyses reveal a dichotomy in gene flow depending on whether the population is resident or migratory, with the former being genetically structured and the latter exhibiting no signs of structure. Among resident populations, we observed significantly higher genetic differentiation, significant isolation‐by‐distance, and significantly elevated inbreeding. Among migratory breeding groups, on the other hand, we observed lower genetic differentiation, no isolation‐by‐distance, and substantially lower inbreeding. Using genotype–environment association analysis, we find significant evidence for relationships between migratory phenotypes (i.e., migrant versus resident) and environmental variation associated with cold temperatures during the winter and barren, open habitats. In the regions of the genome most differentiated between migrants and residents, we find significant enrichment for genes associated with the metabolism of fats. This may be linked to the increased pressure on migrants to process and store fats more efficiently in preparation for and during migration. Our results provide a significant contribution toward understanding the evolution of migratory behavior and vital insight into ongoing conservation and management efforts for the western burrowing owl.

     
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  4. Abstract

    Conservation units (CUs) are an essential tool for maximizing evolutionary potential and prioritizing areas across a species’ range for protection when implementing conservation and management measures. However, current workflows for identifying CUs on the basis of neutral and adaptive genomic variation largely ignore information contained in patterns of isolation by distance (IBD), frequently the primary signal of population structure in highly mobile taxa, such as birds, bats, and marine organisms with pelagic larval stages. While individuals located on either end of a species’ distribution may exhibit clear genetic, phenotypic, and ecological differences, IBD produces subtle changes in allele frequencies across space, making it difficult to draw clear boundaries for conservation purposes in the absence of discrete population structure. Here, we highlight potential pitfalls that arise when applying common methods for delineating CUs to continuously distributed organisms and review existing methods for detecting subtle breakpoints in patterns of IBD that can indicate barriers to gene flow in highly mobile taxa. In addition, we propose a new framework for identifying CUs in all organisms, including those characterized by continuous genomic differentiation, and suggest several possible ways to harness the information contained in patterns of IBD to guide conservation and management decisions.

     
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  5. Abstract

    Understanding the geographic linkages among populations across the annual cycle is an essential component for understanding the ecology and evolution of migratory species and for facilitating their effective conservation. While genetic markers have been widely applied to describe migratory connections, the rapid development of new sequencing methods, such as low‐coverage whole genome sequencing (lcWGS), provides new opportunities for improved estimates of migratory connectivity. Here, we use lcWGS to identify fine‐scale population structure in a widespread songbird, the American Redstart (Setophaga ruticilla), and accurately assign individuals to genetically distinct breeding populations. Assignment of individuals from the nonbreeding range reveals population‐specific patterns of varying migratory connectivity. By combining migratory connectivity results with demographic analysis of population abundance and trends, we consider full annual cycle conservation strategies for preserving numbers of individuals and genetic diversity. Notably, we highlight the importance of the Northern Temperate‐Greater Antilles migratory population as containing the largest proportion of individuals in the species. Finally, we highlight valuable considerations for other population assignment studies aimed at using lcWGS. Our results have broad implications for improving our understanding of the ecology and evolution of migratory species through conservation genomics approaches.

     
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  6. Abstract

    The ability of animals to sync the timing and location of molting (the replacement of hair, skin, exoskeletons or feathers) with peaks in resource availability has important implications for their ecology and evolution. In migratory birds, the timing and location of pre-migratory feather molting, a period when feathers are shed and replaced with newer, more aerodynamic feathers, can vary within and between species. While hypotheses to explain the evolution of intraspecific variation in the timing and location of molt have been proposed, little is known about the genetic basis of this trait or the specific environmental drivers that may result in natural selection for distinct molting phenotypes. Here we take advantage of intraspecific variation in the timing and location of molt in the iconic songbird, the Painted Bunting (Passerina ciris) to investigate the genetic and ecological drivers of distinct molting phenotypes. Specifically, we use genome-wide genetic sequencing in combination with stable isotope analysis to determine population genetic structure and molting phenotype across thirteen breeding sites. We then use genome-wide association analysis (GWAS) to identify a suite of genes associated with molting and pair this with gene-environment association analysis (GEA) to investigate potential environmental drivers of genetic variation in this trait. Associations between genetic variation in molt-linked genes and the environment are further tested via targeted SNP genotyping in 25 additional breeding populations across the range. Together, our integrative analysis suggests that molting is in part regulated by genes linked to feather development and structure (GLI2andCSPG4) and that genetic variation in these genes is associated with seasonal variation in precipitation and aridity. Overall, this work provides important insights into the genetic basis and potential selective forces behind phenotypic variation in what is arguably one of the most important fitness-linked traits in a migratory bird.

     
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  7. Abstract

    Global loss of biodiversity has placed new urgency on the need to understand factors regulating species response to rapid environmental change. While specialists are often less resilient to rapid environmental change than generalists, species‐level analyses may obscure the extent of specialization when locally adapted populations vary in climate tolerances. Until recently, quantification of the degree of climate specialization in migratory birds below the species level was hindered by a lack of genomic and tracking information, but recent technological advances have helped to overcome these barriers. Here we take a genome‐wide genetic approach to mapping population‐specific migratory routes and quantifying niche breadth within genetically distinct populations of a migratory bird, the willow flycatcher (Empidonax traillii), which exhibits variation in the severity of population declines across its breeding range. While our sample size is restricted to the number of genetically distinct populations within the species, our results support the idea that locally adapted populations of the willow flycatcher with narrow climatic niches across seasons are already federally listed as endangered or in steep decline, while populations with broader climatic niches have remained stable in recent decades. Overall, this work highlights the value of quantifying niche breadth within genetically distinct groups across time and space when attempting to understand the factors that facilitate or constrain the response of locally adapted populations to rapid environmental change.

     
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  8. Abstract

    Understanding how risk factors affect populations across their annual cycle is a major challenge for conserving migratory birds. For example, disease outbreaks may happen on the breeding grounds, the wintering grounds, or during migration and are expected to accelerate under climate change. The ability to identify the geographic origins of impacted individuals, especially outside of breeding areas, might make it possible to predict demographic trends and inform conservation decision‐making. However, such an effort is made more challenging by the degraded state of carcasses and resulting low quality of DNA available. Here, we describe a rapid and low‐cost approach for identifying the origins of birds sampled across their annual cycle that is robust even when DNA quality is poor. We illustrate the approach in the common loon (Gavia immer), an iconic migratory aquatic bird that is under increasing threat on both its breeding and wintering areas. Using 300 samples collected from across the breeding range, we develop a panel of 158 single‐nucleotide polymorphisms (SNP) loci with divergent allele frequencies across six genetic subpopulations. We use this SNP panel to identify the breeding grounds for 142 live nonbreeding individuals and carcasses. For example, genetic assignment of loons sampled during botulism outbreaks in parts of the Great Lakes provides evidence for the significant role the lakes play as migratory stopover areas for loons that breed across wide swaths of Canada, and highlights the vulnerability of a large segment of the breeding population to botulism outbreaks that are occurring in the Great Lakes with increasing frequency. Our results illustrate that the use of SNP panels to identify breeding origins of carcasses collected during the nonbreeding season can improve our understanding of the population‐specific impacts of mortality from disease and anthropogenic stressors, ultimately allowing more effective management.

     
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  9. Seasonal migration is a dynamic natural phenomenon that allows organisms to exploit favourable habitats across the annual cycle. While the morphological, physiological and behavioural changes associated with migratory behaviour are well characterized, the genetic basis of migration and its link to endogenous biological time-keeping pathways are poorly understood. Historically, genome-wide research has focused on genes of large effect, whereas many genes of small effect may work together to regulate complex traits like migratory behaviour. Here, we explicitly relax stringent outlier detection thresholds and, as a result, discover how multiple biological time-keeping genes are important to migratory timing in an iconic raptor species, the American kestrel ( Falco sparverius ). To validate the role of candidate loci in migratory timing, we genotyped kestrels captured across autumn migration and found significant associations between migratory timing and genetic variation in metabolic and light-input pathway genes that modulate biological clocks ( top1, phlpp1, cpne4 and peak1) . Further, we demonstrate that migrating individuals originated from a single panmictic source population, suggesting the existence of distinct early and late migratory genotypes (i.e. chronotypes). Overall, our results provide empirical support for the existence of a within-population-level polymorphism in genes underlying migratory timing in a diurnally migrating raptor. 
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