A highly contiguous genome assembly for the Yellow Warbler (Setophaga petechia).

The Yellow Warbler (Setophaga petechia) is a small songbird in the wood-warbler family (Parulidae) that exhibits phenotypic and ecological differences across a widespread distribution and is important to California's riparian habitat conservation. Here, we present a high-quality de novo genome assembly of a vouchered female Yellow Warbler from southern California. Using HiFi long-read and Omni-C proximity sequencing technologies, we generated a 1.22 Gb assembly including 687 scaffolds with a contig N50 of 6.80 Mb, scaffold N50 of 21.18 Mb, and a BUSCO completeness score of 96.0%. This highly contiguous genome assembly provides an essential resource for understanding the history of gene flow, divergence, and local adaptation in Yellow Warblers and can inform conservation management of this charismatic bird species.

Genetic and environmental drivers of migratory behavior in western burrowing owls and implications for conservation and management.

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.

Widespread gene flow following range expansion in Anna's Hummingbird.

Anthropogenic changes have altered the historical distributions of many North American taxa. As environments shift, ecological and evolutionary processes can combine in complex ways to either stimulate or inhibit range expansion. Here, we examined the role of evolution in a rapid range expansion whose ecological context has been well-documented, Anna's Hummingbird (Calypte anna). Previous studies have suggested that the C. anna range expansion is the result of an ecological release facilitated by human-mediated environmental changes, where access to new food sources have allowed further filling of the abiotic niche. We examined the role of gene flow and adaptation during range expansion from their native California breeding range, north into Canada and east into New Mexico and Texas, USA. Using low coverage whole genome sequencing we found high genetic diversity, low divergence, and little evidence of selection on the northern and eastern expansion fronts. Additionally, there are no clear barriers to gene flow across the native and expanded range. The lack of selective signals between core and expanded ranges could reflect (i) an absence of novel selection pressure in the expanded range (supporting the ecological release hypothesis), (ii) swamping of adaptive variation due to high gene flow, or (iii) limitations of genome scans for detecting small shifts in allele frequencies across many loci. Nevertheless, our results provide an example where strong selection is not apparent during a rapid, contemporary range shift.

Genomic responses to parallel temperature gradients in the eelgrass Zostera marina in adjacent bays.

The extent of parallel genomic responses to similar selective pressures depends on a complex array of environmental, demographic, and evolutionary forces. Laboratory experiments with replicated selective pressures yield mixed outcomes under controlled conditions and our understanding of genomic parallelism in the wild is limited to a few well-established systems. Here, we examine genomic signals of selection in the eelgrass Zostera marina across temperature gradients in adjacent embayments. Although we find many genomic regions with signals of selection within each bay there is very little overlap in signals of selection at the SNP level, despite most polymorphisms being shared across bays. We do find overlap at the gene level, potentially suggesting multiple mutational pathways to the same phenotype. Using polygenic models we find that some sets of candidate SNPs are able to predict temperature across both bays, suggesting that small but parallel shifts in allele frequencies may be missed by independent genome scans. Together, these results highlight the continuous rather than binary nature of parallel evolution in polygenic traits and the complexity of evolutionary predictability.

Genotype-environment associations across spatial scales reveal the importance of putative adaptive genetic variation in divergence.

Identifying areas of high evolutionary potential is a judicious strategy for developing conservation priorities in the face of environmental change. For wide-ranging species occupying heterogeneous environments, the evolutionary forces that shape distinct populations can vary spatially. Here, we investigate patterns of genomic variation and genotype-environment associations in the hermit thrush (Catharus guttatus), a North American songbird, at broad (across the breeding range) and narrow spatial scales (at a hybrid zone). We begin by building a genoscape or map of genetic variation across the breeding range and find five distinct genetic clusters within the species, with the greatest variation occurring in the western portion of the range. Genotype-environment association analyses indicate higher allelic turnover in the west than in the east, with measures of temperature surfacing as key predictors of putative adaptive genomic variation rangewide. Since broad patterns detected across a species' range represent the aggregate of many locally adapted populations, we investigate whether our broadscale analysis is consistent with a finer scale analysis. We find that top rangewide temperature-associated loci vary in their clinal patterns (e.g., steep clines vs. fixed allele frequencies) across a hybrid zone in British Columbia, suggesting that the environmental predictors and the associated candidate loci identified in the rangewide analysis are of variable importance in this particular region. However, two candidate loci exhibit strong concordance with the temperature gradient in British Columbia, suggesting a potential role for temperature-related barriers to gene flow and/or temperature-driven ecological selection in maintaining putative local adaptation. This study demonstrates how patterns identified at the broad (macrogeographic) scale can be validated by investigating genotype-environment correlations at the local (microgeographic) scale. Furthermore, our results highlight the importance of considering the spatial distribution of putative adaptive variation when assessing population-level sensitivity to climate change and other stressors.

Genomic analysis of distinct bleaching tolerances among cryptic coral species.

Reef-building coral species are experiencing an unprecedented decline owing to increasing frequency and intensity of marine heatwaves and associated bleaching-induced mortality. Closely related species from the Acropora hyacinthus species complex differ in heat tolerance and in their association with heat-tolerant symbionts. We used low-coverage full genome sequencing of 114 colonies monitored across the 2015 bleaching event in American Samoa to determine the genetic differences among four cryptic species (termed HA, HC, HD and HE) that have diverged in these species traits. Cryptic species differed strongly at thousands of single nucleotide polymorphisms across the genome which are enriched for amino acid changes in the bleaching-resistant species HE. In addition, HE also showed two particularly divergent regions with strong signals of differentiation. One approximately 220 kb locus, HES1, contained the majority of fixed differences in HE. A second locus, HES2, was fixed in HE but polymorphic in the other cryptic species. Surprisingly, non-HE individuals with HE-like haplotypes at HES2 were more likely to bleach. At both loci, HE showed particular sequence similarity to a congener, Acropora millepora. Overall, resilience to bleaching during the third global bleaching event was strongly structured by host cryptic species, buoyed by differences in symbiont associations between these species.

A general theory of avian migratory connectivity.

Birds exhibit a remarkable array of seasonal migrations. Despite much research describing migratory behaviour, the underlying forces driving how a species' breeding and wintering populations redistribute each year, that is, migratory connectivity, remain largely unknown. Here, we test the hypothesis that birds migrate in a way that minimises energy expenditure while considering intraspecific competition for energy acquisition, by developing a modelling framework that simulates an optimal redistribution of individuals between breeding and wintering areas. Using 25 species across the Americas, we find that the model accurately predicts empirical migration patterns, and thus offers a general explanation for migratory connectivity based on first ecological and energetic principles. Our model provides a strong basis for exploring additional processes underlying the ecology and evolution of migration, but also a framework for predicting how migration impacts local adaptation across seasons and how environmental change may affect population dynamics in migratory species.

Linking climate niches across seasons to assess population vulnerability in a migratory bird.

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.

Persistent panmixia despite extreme habitat loss and population decline in the threatened tricolored blackbird (Agelaius tricolor).

Habitat loss and alteration has driven many species into decline, often to the point of requiring protection and intervention to avert extinction. Genomic data provide the opportunity to inform conservation and recovery efforts with details about vital evolutionary processes with a resolution far beyond that of traditional genetic approaches. The tricolored blackbird (Agelaius tricolor) has suffered severe losses during the previous century largely due to anthropogenic impacts on their habitat. Using a dataset composed of a whole genome paired with reduced representation libraries (RAD-Seq) from samples collected across the species' range, we find evidence for panmixia using multiple methods, including PCA (no geographic clustering), admixture analyses (ADMIXTURE and TESS conclude K = 1), and comparisons of genetic differentiation (average FST = 0.029). Demographic modeling approaches recovered an ancient decline that had a strong impact on genetic diversity but did not detect any effect from the known recent decline. We also did not detect any evidence for selection, and hence adaptive variation, at any site, either geographic or genomic. These results indicate that species continues to have high vagility across its range despite population decline and habitat loss and should be managed as a single unit.

Genetic variation reveals individual-level climate tracking across the annual cycle of a migratory bird.

For migratory species, seasonal movements complicate local climate adaptation, as it is unclear whether individuals track climate niches across the annual cycle. In the migratory songbird yellow warbler (Setophaga petechia), we find a correlation between individual-level wintering and breeding precipitation, but not temperature. Birds wintering in the driest regions of the Neotropics breed in the driest regions of North America. Individuals from drier regions also possess distinct morphologies and population responses to varying rainfall. We find a positive association between bill size and breeding season precipitation which, given documented climate-associated genomic variation, might reflect adaptation to local precipitation regimes. Relative abundance in the breeding range is linked to interannual fluctuations in precipitation, but the directionality of this response varies across geography. Together, our results suggest that variation in climate optima may exist across the breeding range of yellow warblers and provide a mechanism for selection across the annual cycle.

Parallel introgression and selection on introduced alleles in a native species.

As humans cause the redistribution of species ranges, hybridization between previously allopatric species is on the rise. Such hybridization can have complex effects on overall fitness of native species as new allelic combinations are tested. Widespread species introductions provide a unique opportunity to study selection on introgressed alleles in independent, replicated populations. We examined selection on alleles that repeatedly introgressed from introduced rainbow trout (Oncorhynchus mykiss) into native westslope cutthroat trout (Oncorhynchus clarkii lewisi) populations in western Canada. We found that the degree of introgression of individual single nucleotide polymorphisms from the invasive species into the native is correlated between independent watersheds. A number of rainbow trout alleles have repeatedly swept to high frequency in native populations, suggesting parallel adaptive advantages. Using simulations, we estimated large selection coefficients up to 0.05 favoring several rainbow trout alleles in the native background. Although previous studies have found reduced hybrid fitness and genome-wide resistance to introgression in westslope cutthroat trout, our results suggest that some introduced genomic regions are strongly favored by selection. Our study demonstrates the utility of replicated introductions as case studies for understanding parallel adaptation and the interactions between selection and introgression across the genome. We suggest that understanding this variation, including consideration of beneficial alleles, can inform management strategies for hybridizing species.

Response to Comment on "Genomic signals of selection predict climate-driven population declines in a migratory bird".

Fitzpatrick et al discuss issues that they had with analyses and interpretation in our recent manuscript on genomic correlates of climate in yellow warblers. We provide evidence that our findings would not change with different analysis and maintain that our study represents a promising direction for integrating the potential for climate adaptation as one of many tools in conservation management.

Ecological genomics predicts climate vulnerability in an endangered southwestern songbird.

Few regions have been more severely impacted by climate change in the USA than the Desert Southwest. Here, we use ecological genomics to assess the potential for adaptation to rising global temperatures in a widespread songbird, the willow flycatcher (Empidonax traillii), and find the endangered desert southwestern subspecies (E. t. extimus) most vulnerable to future climate change. Highly significant correlations between present abundance and estimates of genomic vulnerability - the mismatch between current and predicted future genotype-environment relationships - indicate small, fragmented populations of the southwestern willow flycatcher will have to adapt most to keep pace with climate change. Links between climate-associated genotypes and genes important to thermal tolerance in birds provide a potential mechanism for adaptation to temperature extremes. Our results demonstrate that the incorporation of genotype-environment relationships into landscape-scale models of climate vulnerability can facilitate more precise predictions of climate impacts and help guide conservation in threatened and endangered groups.

Genomic signals of selection predict climate-driven population declines in a migratory bird.

The ongoing loss of biodiversity caused by rapid climatic shifts requires accurate models for predicting species' responses. Despite evidence that evolutionary adaptation could mitigate climate change impacts, evolution is rarely integrated into predictive models. Integrating population genomics and environmental data, we identified genomic variation associated with climate across the breeding range of the migratory songbird, yellow warbler (Setophaga petechia). Populations requiring the greatest shifts in allele frequencies to keep pace with future climate change have experienced the largest population declines, suggesting that failure to adapt may have already negatively affected populations. Broadly, our study suggests that the integration of genomic adaptation can increase the accuracy of future species distribution models and ultimately guide more effective mitigation efforts.

Polygenic evolution drives species divergence and climate adaptation in corals.

Closely related species often show substantial differences in ecological traits that allow them to occupy different environmental niches. For few of these systems is it clear what the genomic basis of adaptation is and whether a few loci of major effect or many genome-wide differences drive species divergence. Four cryptic species of the tabletop coral Acropora hyacinthus are broadly sympatric in American Samoa; here we show that two common species have differences in key environmental traits such as microhabitat distributions and thermal stress tolerance. We compared gene expression patterns and genetic polymorphism between these two species using RNA-Seq. The vast majority of polymorphisms are shared between species, but the two species show widespread differences in allele frequencies and gene expression, and tend to host different symbiont types. We find that changes in gene expression are related to changes in the frequencies of many gene regulatory variants, but that many of these differences are consistent with the action of genetic drift. However, we observe greater genetic divergence between species in amino acid replacement polymorphisms compared to synonymous variants. These findings suggest that polygenic evolution plays a major role in driving species differences in ecology and resilience to climate change.

Genomic models predict successful coral adaptation if future ocean warming rates are reduced.

Population genomic surveys suggest that climate-associated genetic variation occurs widely across species, but whether it is sufficient to allow population persistence via evolutionary adaptation has seldom been quantified. To ask whether rapid adaptation in reef-building corals can keep pace with future ocean warming, we measured genetic variation at predicted warm-adapted loci and simulated future evolution and persistence in a high-latitude population of corals from Rarotonga, Cook Islands. Alleles associated with thermal tolerance were present but at low frequencies in this cooler, southerly locality. Simulations based on predicted ocean warming in Rarotonga showed rapid evolution of heat tolerance resulting in population persistence under mild warming scenarios consistent with low CO2 emission plans, RCP2.6 and RCP4.5. Under more severe scenarios, RCP6.0 and RCP8.5, adaptation was not rapid enough to prevent extinction. Population adaptation was faster for models based on smaller numbers of additive loci that determine thermal tolerance and for higher population growth rates. Finally, accelerated migration via transplantation of thermally tolerant individuals (1 to 5%/year) sped adaptation. These results show that cool-water corals can adapt to warmer oceans but only under mild scenarios resulting from international emissions controls. Incorporation of genomic data into models of species response to climate change offers a promising method for estimating future adaptive processes.

Genetic Coupling of Female Mate Choice with Polygenic Ecological Divergence Facilitates Stickleback Speciation.

Ecological speciation with gene flow is widespread in nature [1], but it presents a conundrum: how are associations between traits under divergent natural selection and traits that contribute to assortative mating maintained? Theoretical models suggest that genetic mechanisms inhibiting free recombination between loci underlying these two types of traits (hereafter, "genetic coupling") can facilitate speciation [2-4]. Here, we perform a direct test for genetic coupling by mapping both divergent traits and female mate choice in a classic model of ecological speciation: sympatric benthic and limnetic threespine stickleback (Gasterosteus aculeatus). By measuring mate choice in F2 hybrid females, we allowed for recombination between loci underlying assortative mating and those under divergent ecological selection. In semi-natural mating arenas in which females had access to both benthic and limnetic males, we found that F2 females mated with males similar to themselves in body size and shape. In addition, we found two quantitative trait loci (QTLs) associated with female mate choice that also predicted female morphology along the benthic-limnetic trait axis. Furthermore, a polygenic genetic model that explains adaptation to contrasting benthic and limnetic feeding niches [5] also predicted F2 female mate choice. Together, these results provide empirical evidence that genetic coupling of assortative mating with traits under divergent ecological selection helps maintain species in the face of gene flow, despite a polygenic basis for adaptation to divergent environments.

Transcriptome predictors of coral survival and growth in a highly variable environment.

Concern over rapid environmental shifts associated with climate change has led to a search for molecular markers of environmental tolerance. Climate-associated gene expression profiles exist for a number of systems, but have rarely been tied to fitness outcomes, especially in nonmodel organisms. We reciprocally transplanted corals between two backreef locations with more and less variable temperature regimes to disentangle effects of recent and native environment on survival and growth. Coral growth over 12 months was largely determined by local environment. Survival, however, was impacted by native environment; corals from the more variable environment had 22% higher survivorship. By contrast, corals native to the less variable environment had more variable survival. This might represent a "selective sieve" where poor survivors are filtered from the more stressful environment. We also find a potential fitness trade-off-corals with high survival under stressful conditions grew less in the more benign environment. Transcriptome samples taken a year before transplantation were used to examine gene expression patterns that predicted transplant survival and growth. Two separate clusters of coexpressed genes were predictive of survival in the two locations. Genes from these clusters are candidate biomarkers for predicting persistence of corals under future climate change scenarios.

Predicting Responses to Contemporary Environmental Change Using Evolutionary Response Architectures.

Rapid environmental change currently presents a major threat to global biodiversity and ecosystem functions, and understanding impacts on individual populations is critical to creating reliable predictions and mitigation plans. One emerging tool for this goal is high-throughput sequencing technology, which can now be used to scan the genome for signs of environmental selection in any species and any system. This explosion of data provides a powerful new window into the molecular mechanisms of adaptation, and although there has been some success in using genomic data to predict responses to selection in fields such as agriculture, thus far genomic data are rarely integrated into predictive frameworks of future adaptation in natural populations. Here, we review both theoretical and empirical studies of adaptation to rapid environmental change, focusing on areas where genomic data are poised to contribute to our ability to estimate species and population persistence and adaptation. We advocate for the need to study and model evolutionary response architectures, which integrate spatial information, fitness estimates, and plasticity with genetic architecture. Understanding how these factors contribute to adaptive responses is essential in efforts to predict the responses of species and ecosystems to future environmental change.