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Abstract Global change is impacting biodiversity across all habitats on earth. New selection pressures from changing climatic conditions and other anthropogenic activities are creating heterogeneous ecological and evolutionary responses across many species' geographic ranges. Yet we currently lack standardised and reproducible tools to effectively predict the resulting patterns in species vulnerability to declines or range changes.We developed an informatic toolbox that integrates ecological, environmental and genomic data and analyses (environmental dissimilarity, species distribution models, landscape connectivity, neutral and adaptive genetic diversity, genotype‐environment associations and genomic offset) to estimate population vulnerability. In our toolbox, functions and data structures are coded in a standardised way so that it is applicable to any species or geographic region where appropriate data are available, for example individual or population sampling and genomic datasets (e.g. RAD‐seq, ddRAD‐seq, whole genome sequencing data) representing environmental variation across the species geographic range.To demonstrate multi‐species applicability, we apply our toolbox to three georeferenced genomic datasets for co‐occurring East African spiny reed frogs (Afrixalus fornasini, A. delicatusandA. sylvaticus) to predict their population vulnerability, as well as demonstrating that range loss projections based on adaptive variation can be accurately reproduced from a previous study using data for two European bat species (Myotis escaleraiandM. crypticus).Our framework sets the stage for large scale, multi‐species genomic datasets to be leveraged in a novel climate change vulnerability framework to quantify intraspecific differences in genetic diversity, local adaptation, range shifts and population vulnerability based on exposure, sensitivity and landscape barriers.more » « less
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Abstract Patterns of population connectivity shape ecological and evolutionary phenomena from population persistence to local adaptation and can inform conservation strategy. Connectivity patterns emerge from the interaction of individual behavior with a complex and heterogeneous environment. Despite ample observation that dispersal patterns vary through time, the extent to which variation in the physical environment can explain emergent connectivity variation is not clear. Empirical studies of its contribution promise to illuminate a potential source of variability that shapes the dynamics of natural populations. We leveraged simultaneous direct dispersal observations and oceanographic transport simulations of the clownfishAmphiprion clarkiiin the Camotes Sea, Philippines, to assess the contribution of oceanographic variability to emergent variation in connectivity. We found that time‐varying oceanographic simulations on both annual and monsoonal timescales partly explained the observed dispersal patterns, suggesting that temporal variation in oceanographic transport shapes connectivity variation on these timescales. However, interannual variation in observed mean dispersal distance was nearly 10 times the expected variation from biophysical simulations, revealing that additional biotic and abiotic factors contribute to interannual connectivity variation. Simulated dispersal kernels also predicted a smaller scale of dispersal than the observations, supporting the hypothesis that undocumented abiotic factors and behaviors such as swimming and navigation enhance the probability of successful dispersal away from, as opposed to retention near, natal sites. Our findings highlight the potential for coincident observations and biophysical simulations to test dispersal hypotheses and the influence of temporal variability on metapopulation persistence, local adaptation, and other population processes.more » « less
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Abstract Genetic diversity is a fundamental component of biodiversity. Examination of global patterns of genetic diversity can help highlight mechanisms underlying species diversity, though a recurring challenge has been that patterns may vary by molecular marker. Here, we compiled 6862 observations of genetic diversity from 492 species of marine fish and tested among hypotheses for diversity gradients: the founder effect hypothesis, the kinetic energy hypothesis, and the productivity‐diversity hypothesis. We fit generalized linear mixed effect models (GLMMs) and explored the extent to which various macroecological drivers (latitude, longitude, temperature (SST), and chlorophyll‐a concentration) explained variation in genetic diversity. We found that mitochondrial genetic diversity followed geographic gradients similar to those of species diversity, being highest near the Equator, particularly in the Coral Triangle, while nuclear genetic diversity did not follow clear geographic patterns. Despite these differences, all genetic diversity metrics were correlated with chlorophyll‐a concentration, while mitochondrial diversity was also positively associated with SST. Our results provide support for the kinetic energy hypothesis, which predicts that elevated mutation rates at higher temperatures increase mitochondrial but not necessarily nuclear diversity, and the productivity‐diversity hypothesis, which posits that resource‐rich regions support larger populations with greater genetic diversity. Overall, these findings reveal how environmental variables can influence mutation rates and genetic drift in the ocean, caution against using mitochondrial macrogenetic patterns as proxies for whole‐genome diversity, and aid in defining global gradients of genetic diversity.more » « less
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Abstract The demographic history of a population is important for conservation and evolution, but this history is unknown for many populations. Methods that use genomic data have been developed to infer demography, but they can be challenging to implement and interpret, particularly for large populations. Thus, understanding if and when genetic estimates of demography correspond to true population history is important for assessing the performance of these genetic methods. Here, we used double‐digest restriction‐site associated DNA (ddRAD) sequencing data from archived collections of larval summer flounder (Paralichthys dentatus,n = 279) from three cohorts (1994–1995, 1997–1998 and 2008–2009) along the U.S. East coast to examine how contemporary effective population size and genetic diversity responded to changes in abundance in a natural population. Despite little to no detectable change in genetic diversity, coalescent‐based demographic modelling from site frequency spectra revealed that summer flounder effective population size declined dramatically in the early 1980s. The timing and direction of change corresponded well with the observed decline in spawning stock census abundance in the late 1980s from independent fish surveys. Census abundance subsequently recovered and achieved the prebottleneck size. Effective population size also grew following the bottleneck. Our results for summer flounder demonstrate that genetic sampling and site frequency spectra can be useful for detecting population dynamics, even in species with large effective sizes.more » « less
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Synopsis Understanding recent population trends is critical to quantifying species vulnerability and implementing effective management strategies. To evaluate the accuracy of genomic methods for quantifying recent declines (beginning <120 generations ago), we simulated genomic data using forward-time methods (SLiM) coupled with coalescent simulations (msprime) under a number of demographic scenarios. We evaluated both site frequency spectrum (SFS)-based methods (momi2, Stairway Plot) and methods that employ linkage disequilibrium information (NeEstimator, GONE) with a range of sampling schemes (contemporary-only samples, sampling two time points, and serial sampling) and data types (RAD-like data and whole-genome sequencing). GONE and momi2 performed best overall, with >80% power to detect severe declines with large sample sizes. Two-sample and serial sampling schemes could accurately reconstruct changes in population size, and serial sampling was particularly valuable for making accurate inferences when genotyping errors or minor allele frequency cutoffs distort the SFS or under model mis-specification. However, sampling only contemporary individuals provided reliable inferences about contemporary size and size change using either site frequency or linkage-based methods, especially when large sample sizes or whole genomes from contemporary populations were available. These findings provide a guide for researchers designing genomics studies to evaluate recent demographic declines.more » « less
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Abstract Understanding the evolutionary consequences of anthropogenic change is imperative for estimating long‐term species resilience. While contemporary genomic data can provide us with important insights into recent demographic histories, investigating past change using present genomic data alone has limitations. In comparison, temporal genomics studies, defined herein as those that incorporate time series genomic data, utilize museum collections and repeated field sampling to directly examine evolutionary change. As temporal genomics is applied to more systems, species and questions, best practices can be helpful guides to make the most efficient use of limited resources. Here, we conduct a systematic literature review to synthesize the effects of temporal genomics methodology on our ability to detect evolutionary changes. We focus on studies investigating recent change within the past 200 years, highlighting evolutionary processes that have occurred during the past two centuries of accelerated anthropogenic pressure. We first identify the most frequently studied taxa, systems, questions and drivers, before highlighting overlooked areas where further temporal genomic studies may be particularly enlightening. Then, we provide guidelines for future study and sample designs while identifying key considerations that may influence statistical and analytical power. Our aim is to provide recommendations to a broad array of researchers interested in using temporal genomics in their work.more » « less
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Abstract AimHumans are unintentionally affecting the evolution of fishery species directly through exploitation and indirectly by altering climate. We aim to test for a relationship between biogeographic patterns in the shell phenotypes of an over‐exploited shellfish and the presence of humans to identify human‐mediated adaptive trade‐offs. The implications of these trade‐offs are discussed with respect to the sustainability of the fishery. TaxonThe endemic Hawaiian intertidal limpet, ‘opihi makaiauli (Patellagastropoda, Nacellidae, Cellana exarata) MethodsWe surveyed phenotypic characters associated with temperature and predation avoidance across the entire species range and tested for differences in the relationship between these characters and latitude, on islands with and without humans. ResultsAmong all limpets surveyed, there was a bimodal distribution in shell colour (light, dark) and a parapatric pattern of shell coloration across the archipelago with lighter shells being prevalent on the uninhabited islands and darker, more camouflaged shells being prevalent on the inhabited islands. On the cooler, uninhabited islands, all morphometric characters associated with thermal avoidance (surface area, height and doming) increased with decreasing latitude. On the hotter, inhabited islands, however, shells were flatter, less variable and less adapted for avoiding thermal stress than predation. Main ConclusionsThe biogeographic patterns in shell phenotype and previous genetic studies suggest that the population is beginning to bifurcate in response to disruptive and directional selection as well as geographic isolation between the islands with and without humans. Decreased phenotypic and genetic diversity on the inhabited islands despite much larger populations of ‘opihi suggests a prominent historical bottleneck. The prevalence of maladaptive dark, flat phenotypes for thermal avoidance on the inhabited islands suggests that predation is a stronger selective force, driving adaptive trade‐offs in shape and colour. We propose that this is likely a case of fisheries‐induced evolution and a millennium of harvesting is the most likely selective pressure driving the observed biogeographic patterns in shell morphology. The flatter, darker shells will allow body temperatures to rise higher in direct sunlight, therefore we hypothesize that the thermal niche of ‘opihi is narrower on inhabited islands and will continue to narrow as Earth warms.more » « less
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Abstract Determining metapopulation persistence requires understanding both demographic rates and patch connectivity. Persistence is well understood in theory but has proved challenging to test empirically for marine and other species with high connectivity that precludes classic colonisation–extinction dynamics. Here, we assessed persistence for a yellowtail anemonefish (Amphiprion clarkii) metapopulation using 7 years of annual sampling data along 30 km of coastline. We carefully accounted for uncertainty in demographic rates. Despite stable population abundances through time and sufficient production of surviving offspring for replacement, the pattern of connectivity made the metapopulation unlikely to persist in isolation and reliant on immigrants from outside habitat. To persist in isolation, the metapopulation would need higher fecundity or to retain essentially all recruits produced. This assessment of persistence in a marine metapopulation shows that stable abundance alone does not indicate persistence, emphasising the necessity of assessing both demographic and connectivity processes to understand metapopulation dynamics.more » « less
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Coral reefs are both exceptionally biodiverse and threatened by climate change and other human activities. Here, we review population genomic processes in coral reef taxa and their importance for understanding responses to global change. Many taxa on coral reefs are characterized by weak genetic drift, extensive gene flow, and strong selection from complex biotic and abiotic environments, which together present a fascinating test of microevolutionary theory. Selection, gene flow, and hybridization have played and will continue to play an important role in the adaptation or extinction of coral reef taxa in the face of rapid environmental change, but research remains exceptionally limited compared to the urgent needs. Critical areas for future investigation include understanding evolutionary potential and the mechanisms of local adaptation, developing historical baselines, and building greater research capacity in the countries where most reef diversity is concentrated.more » « less
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Populations can adapt to novel selection pressures through dramatic frequency changes in a few genes of large effect or subtle shifts in many genes of small effect. The latter (polygenic adaptation) is expected to be the primary mode of evolution for many life-history traits but tends to be more difficult to detect than changes in genes of large effect. Atlantic cod (Gadus morhua) were subjected to intense fishing pressure over the twentieth century, leading to abundance crashes and a phenotypic shift toward earlier maturation across many populations. Here, we use spatially replicated temporal genomic data to test for a shared polygenic adaptive response to fishing using methods previously applied to evolve-and-resequence experiments. Cod populations on either side of the Atlantic show covariance in allele frequency change across the genome that are characteristic of recent polygenic adaptation. Using simulations, we demonstrate that the degree of covariance in allele frequency change observed in cod is unlikely to be explained by neutral processes or background selection. As human pressures on wild populations continue to increase, understanding and attributing modes of adaptation using methods similar to those demonstrated here will be important in identifying the capacity for adaptive responses and evolutionary rescue. This article is part of the theme issue ‘Detecting and attributing the causes of biodiversity change: needs, gaps and solutions’.more » « less