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1. Polygenic Selection within a Single Generation Leads to Subtle Divergence among Ecological Niches

   https://doi.org/10.1093/gbe/evaa257  

   Ehrlich, Moritz A ; Wagner, Dominique N ; Oleksiak, Marjorie F ; Crawford, Douglas L ( February 2021 , Genome Biology and Evolution)

   Fraser, Bonnie (Ed.)

   Abstract Selection on standing genetic variation may be effective enough to allow for adaptation to distinct niche environments within a single generation. Minor allele frequency changes at multiple, redundant loci of small effect can produce remarkable phenotypic shifts. Yet, demonstrating rapid adaptation via polygenic selection in the wild remains challenging. Here we harness natural replicate populations that experience similar selection pressures and harbor high within-, yet negligible among-population genetic variation. Such populations can be found among the teleost Fundulus heteroclitus that inhabits marine estuaries characterized by high environmental heterogeneity. We identify 10,861 single nucleotide polymorphisms in F. heteroclitus that belong to a single, panmictic population yet reside in environmentally distinct niches (one coastal basin and three replicate tidal ponds). By sampling at two time points within a single generation, we quantify both allele frequency change within as well as spatial divergence among niche subpopulations. We observe few individually significant allele frequency changes yet find that the “number” of moderate changes exceeds the neutral expectation by 10–100%. We find allele frequency changes to be significantly concordant in both direction and magnitude among all niche subpopulations, suggestive of parallel selection. In addition, within-generation allele frequency changes generate subtle but significant divergence among niches, indicative of local adaptation. Although we cannot distinguish between selection and genotype-dependent migration as drivers of within-generation allele frequency changes, the trait/s determining fitness and/or migration likelihood appear to be polygenic. In heterogeneous environments, polygenic selection and polygenic, genotype-dependent migration offer conceivable mechanisms for within-generation, local adaptation to distinct niches. 

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2. Ecological genomics of local adaptation in Cornus florida L. by genotyping by sequencing

   https://doi.org/10.1002/ece3.2623  

   Pais, Andrew L. ; Whetten, Ross W. ; Xiang, Qiu‐Yun ( December 2016 , Ecology and Evolution)

   Discovering local adaptation, its genetic underpinnings, and environmental drivers is important for conserving forest species. Ecological genomic approaches coupled with next‐generation sequencing are useful means to detect local adaptation and uncover its underlying genetic basis in nonmodel species. We report results from a study on flowering dogwood trees (Cornus florida L.) using genotyping by sequencing (GBS). This species is ecologically important to easternUSforests but is severely threatened by fungal diseases. We analyzed subpopulations in divergent ecological habitats within North Carolina to uncover loci under local selection and associated with environmental–functional traits or disease infection. At this scale, we tested the effect of incorporating additional sequencing before scaling for a broader examination of the entire range. To test for biases ofGBS, we sequenced two similarly sampled libraries independently from six populations of three ecological habitats. We obtained environmental–functional traits for each subpopulation to identify associations with genotypes via latent factor mixed modeling (LFMM) and gradient forests analysis. To test whether heterogeneity of abiotic pressures resulted in genetic differentiation indicative of local adaptation, we evaluatedF_stper locus while accounting for genetic differentiation between coastal subpopulations and Piedmont‐Mountain subpopulations. Of the 54 candidate loci with sufficient evidence of being under selection among both libraries, 28–39 were Arlequin–BayeScanF_stoutliers. ForLFMM, 45 candidates were associated with climate (of 54), 30 were associated with soil properties, and four were associated with plant health. Reanalysis of combined libraries showed that 42 candidate loci still showed evidence of being under selection. We conclude environment‐driven selection on specific loci has resulted in local adaptation in response to potassium deficiencies, temperature, precipitation, and (to a marginal extent) disease. High allele turnover along ecological gradients further supports the adaptive significance of loci speculated to be under selection.

    

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3. Inversion invasions: when the genetic basis of local adaptation is concentrated within inversions in the face of gene flow

   https://doi.org/10.1098/rstb.2021.0200  

   Schaal, Sara M. ; Haller, Benjamin C. ; Lotterhos, Katie E. ( August 2022 , Philosophical Transactions of the Royal Society B: Biological Sciences)

   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’. 

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4. Recovery from hybrid breakdown reveals a complex genetic architecture of mitonuclear incompatibilities

   https://doi.org/10.1111/mec.15985  

   Pereira, Ricardo J. ; Lima, Thiago G. ; Pierce‐Ward, N. Tessa ; Chao, Lin ; Burton, Ronald S. ( June 2021 , Molecular Ecology)

   Reproductive isolation is often achieved when genes that are neutral or beneficial in their genomic background become functionally incompatible in a foreign genomic background, causing inviability, sterility or other forms of low fitness in hybrids. Recent studies suggest that mitonuclear interactions are among the initial incompatibilities to evolve at early stages of population divergence across taxa. Yet, the genomic architecture of mitonuclear incompatibilities has rarely been elucidated. We employ an experimental evolution approach starting with low‐fitness F₂interpopulation hybrids of the copepodTigriopus californicus, in which frequencies of compatible and incompatible nuclear alleles change in response to an alternative mitochondrial background. After about nine generations, we observe a generalized increase in population size and in survivorship, suggesting efficiency of selection against maladaptive phenotypes. Whole genome sequencing of evolved populations showed some consistent allele frequency changes across three replicates of each reciprocal cross, but markedly different patterns between mitochondrial backgrounds. In only a few regions (~6.5% of the genome), the same parental allele was overrepresented irrespective of the mitochondrial background. About 33% of the genome showed allele frequency changes consistent with divergent selection, with the location of these genomic regions strongly differing between mitochondrial backgrounds. In 87% and 89% of these genomic regions, the dominant nuclear allele matched the associated mitochondrial background, consistent with mitonuclear co‐adaptation. These results suggest that mitonuclear incompatibilities have a complex polygenic architecture that differs between populations, potentially generating genome‐wide barriers to gene flow between closely related taxa.

    

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5. Whole genome resequencing identifies local adaptation associated with environmental variation for redband trout

   https://doi.org/10.1111/mec.16810  

   Andrews, Kimberly R. ; Seaborn, Travis ; Egan, Joshua P. ; Fagnan, Matthew W. ; New, Daniel D. ; Chen, Zhongqi ; Hohenlohe, Paul A. ; Waits, Lisette P. ; Caudill, Christopher C. ; Narum, Shawn R. ( December 2022 , Molecular Ecology)

   Aquatic ectotherms are predicted to harbour genomic signals of local adaptation resulting from selective pressures driven by the strong influence of climate conditions on body temperature. We investigated local adaptation in redband trout (Oncorhynchus mykiss gairdneri) using genome scans for 547 samples from 11 populations across a wide range of habitats and thermal gradients in the interior Columbia River. We estimated allele frequencies for millions of single nucleotide polymorphism loci (SNPs) across populations using low‐coverage whole genome resequencing, and used population structure outlier analyses to identify genomic regions under divergent selection between populations. Twelve genomic regions showed signatures of local adaptation, including two regions associated with genes known to influence migration and developmental timing in salmonids (GREB1L,ROCK1,SIX6). Genotype–environment association analyses indicated that diurnal temperature variation was a strong driver of local adaptation, with signatures of selection driven primarily by divergence of two populations in the northern extreme of the subspecies range. We also found evidence for adaptive differences between high‐elevation desert vs. montane habitats at a smaller geographical scale. Finally, we estimated vulnerability of redband trout to future climate change using ecological niche modelling and genetic offset analyses under two climate change scenarios. These analyses predicted substantial habitat loss and strong genetic shifts necessary for adaptation to future habitats, with the greatest vulnerability predicted for high‐elevation desert populations. Our results provide new insight into the complexity of local adaptation in salmonids, and important predictions regarding future responses of redband trout to climate change.

    

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