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Abstract As the global climate crisis continues, predictions concerning how wild populations will respond to changing climate conditions are informed by an understanding of how populations have responded and/or adapted to climate variables in the past. Changes in the local biotic and abiotic environment can drive differences in phenology, physiology, morphology and demography between populations leading to local adaptation, yet the molecular basis of adaptive evolution in wild non‐model organisms is poorly understood. We leverage comparisons between two lineages ofCalochortus venustusoccurring along parallel transects that allow us to identify loci under selection and measure clinal variation in allele frequencies as evidence of population‐specific responses to selection along climatic gradients. We identify targets of selection by distinguishing loci that are outliers to population structure and by using genotype–environment associations across transects to detect loci under selection from each of nine climatic variables. Despite gene flow between individuals of different floral phenotypes and between populations, we find evidence of ecological specialization at the molecular level, including genes associated with key plant functions linked to plant adaptation to California's Mediterranean climate. Single‐nucleotide polymorphisms (SNPs) present in both transects show similar trends in allelic similarity across latitudes indicating parallel adaptation to northern climates. Comparisons between eastern and western populations across latitudes indicate divergent genetic evolution between transects, suggesting local adaptation to either coastal or inland habitats. Our study is among the first to show repeated allelic variation across climatic clines in a non‐model organism.
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Local Adaptation: Causal Agents of Selection and Adaptive Trait Divergence
Divergent selection across the landscape can favor the evolution of local adaptation in populations experiencing contrasting conditions. Local adaptation is widely observed in a diversity of taxa, yet we have a surprisingly limited understanding of the mechanisms that give rise to it. For instance, few have experimentally confirmed the biotic and abiotic variables that promote local adaptation, and fewer yet have identified the phenotypic targets of selection that mediate local adaptation. Here, we highlight critical gaps in our understanding of the process of local adaptation and discuss insights emerging from in-depth investigations of the agents of selection that drive local adaptation, the phenotypes they target, and the genetic basis of these phenotypes. We review historical and contemporary methods for assessing local adaptation, explore whether local adaptation manifests differently across life history, and evaluate constraints on local adaptation.
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- PAR ID:
- 10412936
- Date Published:
- Journal Name:
- Annual Review of Ecology, Evolution, and Systematics
- Volume:
- 53
- Issue:
- 1
- ISSN:
- 1543-592X
- Page Range / eLocation ID:
- 87 to 111
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Hernandez, R (Ed.)Abstract Gene expression links genotypes to phenotypes, so identifying genes whose expression is shaped by selection will be important for understanding the traits and processes underlying local adaptation. However, detecting local adaptation for gene expression will require distinguishing between divergence due to selection and divergence due to genetic drift. Here, we adapt a QST−FST framework to detect local adaptation for transcriptome-wide gene expression levels in a population of diverse maize genotypes. We compare the number and types of selected genes across a wide range of maize populations and tissues, as well as selection on cold-response genes, drought-response genes, and coexpression clusters. We identify a number of genes whose expression levels are consistent with local adaptation and show that genes involved in stress response show enrichment for selection. Due to its history of intense selective breeding and domestication, maize evolution has long been of interest to researchers, and our study provides insight into the genes and processes important for in local adaptation of maize.more » « less
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Across many species where inversions have been implicated in local adaptation, genomes often evolve to contain multiple, large inversions that arise early in divergence. Why this occurs has yet to be resolved. To address this gap, we built forward-time simulations in which inversions have flexible characteristics and can invade a metapopulation undergoing spatially divergent selection for a highly polygenic trait. In our simulations, inversions typically arose early in divergence, captured standing genetic variation upon mutation, and then accumulated many small-effect loci over time. Under special conditions, inversions could also arise late in adaptation and capture locally adapted alleles. Polygenic inversions behaved similarly to a single supergene of large effect and were detectable by genome scans. Our results show that characteristics of adaptive inversions found in empirical studies (e.g. multiple large, old inversions that are F ST outliers, sometimes overlapping with other inversions) are consistent with a highly polygenic architecture, and inversions do not need to contain any large-effect genes to play an important role in local adaptation. By combining a population and quantitative genetic framework, our results give a deeper understanding of the specific conditions needed for inversions to be involved in adaptation when the genetic architecture is polygenic. This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.more » « less
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PremiseIdentifying the environmental factors responsible for natural selection across different habitats is crucial for understanding the process of local adaptation in plants. Despite its importance, few studies have successfully isolated the environmental factors driving local adaptation in nature. In this study, we evaluated the agents of selection responsible for local adaptation of the monkeyflowerMimulus guttatusto California's coastal and inland habitats. MethodsWe implemented a manipulative reciprocal transplant experiment at coastal and inland sites, where we excluded aboveground stressors in an effort to elucidate their role in the evolution of local adaptation. ResultsExcluding aboveground stressors, most likely a combination of salt spray and herbivory, completely rescued inland annual plant fitness when transplanted to coastal habitat. The exclosures in inland habitat provided a benefit to the performance of coastal perennial plants. However, the exclosures are unlikely to provide much fitness benefit to the coastal plants at the inland site because of their general inability to flower in time to escape from the summer drought. ConclusionsOur study demonstrates that a distinct set of selective agents (aboveground vs. belowground) are responsible for local adaptation at opposite ends of an environmental gradient.more » « less
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Abstract The study of local adaptation in the presence of ongoing gene flow is the study of natural selection in action, revealing the functional genetic diversity most relevant to contemporary pressures. In addition to individual genes, genome-wide architecture can itself evolve to enable adaptation. Distributed across a steep thermal gradient along the east coast of North America, Atlantic silversides (Menidia menidia) exhibit an extraordinary degree of local adaptation in a suite of traits, and the capacity for rapid adaptation from standing genetic variation, but we know little about the patterns of genomic variation across the species range that enable this remarkable adaptability. Here, we use low-coverage, whole-transcriptome sequencing of Atlantic silversides sampled along an environmental cline to show marked signatures of divergent selection across a gradient of neutral differentiation. Atlantic silversides sampled across 1371 km of the southern section of its distribution have very low genome-wide differentiation (median FST = 0.006 across 1.9 million variants), consistent with historical connectivity and observations of recent migrants. Yet almost 14,000 single nucleotide polymorphisms (SNPs) are nearly fixed (FST > 0.95) for alternate alleles. Highly differentiated SNPs cluster into four tight linkage disequilibrium (LD) blocks that span hundreds of genes and several megabases. Variants in these LD blocks are disproportionately nonsynonymous and concentrated in genes enriched for multiple functions related to known adaptations in silversides, including variation in lipid storage, metabolic rate, and spawning behavior. Elevated levels of absolute divergence and demographic modeling suggest selection maintaining divergence across these blocks under gene flow. These findings represent an extreme case of heterogeneity in levels of differentiation across the genome, and highlight how gene flow shapes genomic architecture in continuous populations. Locally adapted alleles may be common features of populations distributed along environmental gradients, and will likely be key to conserving variation to enable future responses to environmental change.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1146/annurev-ecolsys-012722-035231
