Genomic architecture of parallel ecological divergence: beyond a single environmental contrast (original) (raw)
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Molecular Ecology
Parallel patterns of adaptive divergence and speciation are cited as powerful evidence for the role of selection driving these processes. However, it is often not clear whether parallel phenotypic divergence is underlain by parallel genetic changes. Here we asked about the genetic basis of parallel divergence in the marine snail Littorina saxatilis, which has repeatedly evolved coexisting ecotypes adapted to either crab predation or wave action. We sequenced the transcriptome of snails of both ecotypes from three distant geographical locations (Spain, Sweden and United Kingdom) and mapped the reads to the L. saxatilis reference genome. We identified genomic regions potentially under divergent selection between ecotypes within each country, using an outlier approach based on FST values calculated per locus. In line with previous studies indicating that gene re-use generally is common, we expected to find extensive sharing of outlier loci due to recent shared ancestry and gene flow be...
Molecular ecology, 2016
Parallel divergence and speciation provide evidence for the role of divergent selection in generating biological diversity. Recent studies indicate that parallel phenotypic divergence may not have the same genetic basis in different geographical locations - "outlier loci" (loci potentially affected by divergent selection) are often not shared among parallel instances of phenotypic divergence. However, limited sharing may be due, in part, to technical issues if false positive outliers occur. Here, we test this idea in the marine snail Littorina saxatilis, which has evolved two partly isolated ecotypes (adapted to crab predation vs. wave action) in multiple locations independently. We argue that if the low extent of sharing observed in earlier studies in this system is due to sampling effects, we expect outliers not to show elevated FST when sequenced in new samples from the original locations, and also not to follow predictable geographical patterns of elevated FST . Follow...
Molecular Ecology, 2009
The Galician sympatric ecotypes of Littorina saxatilis have been proposed as a model system for studying parallel ecological speciation. Such a model system makes a clear prediction: candidate loci (for divergent adaptation) should present a higher level of geographical differentiation than noncandidate (neutral) loci. We used 2356 amplified fragment length polymorphisms (AFLPs) and four microsatellite loci to identify candidate loci for ecological adaptation using the F ST outlier method. Three per cent of the studied AFLP loci were identified as candidate loci associated with adaptation, after multitest adjustments, thus contributing to ecotype differentiation (candidate loci were not detected within ecotypes). Candidate and noncandidate loci were analysed separately at four different F ST partitions: differences between ecotypes (overall and local), differences between localities and micro-geographical differences within ecotypes. The magnitude of F ST differed between candidate and noncandidate loci for all partitions except in the case of microgeographical differentiation within ecotypes, and the microsatellites (putatively neutral) showed an identical pattern to noncandidate loci. Thus, variation in candidate loci is determined partially independent by divergent natural selection (in addition to stochastic forces) at each locality, while noncandidate loci are exclusively driven by stochastic forces. These results support the evolutionary history described for these particular populations, considered to be a clear example of incomplete sympatric ecological speciation.
Evolution letters, 2018
Adaptive divergence and speciation may happen despite opposition by gene flow. Identifying the genomic basis underlying divergence with gene flow is a major task in evolutionary genomics. Most approaches (e.g., outlier scans) focus on genomic regions of high differentiation. However, not all genomic architectures potentially underlying divergence are expected to show extreme differentiation. Here, we develop an approach that combines hybrid zone analysis (i.e., focuses on spatial patterns of allele frequency change) with system-specific simulations to identify loci inconsistent with neutral evolution. We apply this to a genome-wide SNP set from an ideally suited study organism, the intertidal snail , which shows primary divergence between ecotypes associated with different shore habitats. We detect many SNPs with clinal patterns, most of which are consistent with neutrality. Among non-neutral SNPs, most are located within three large putative inversions differentiating ecotypes. Man...
Shared and nonshared genomic divergence in parallel ecotypes ofLittorina saxatilisat a local scale
Molecular Ecology, 2015
Parallel speciation occurs when selection drives repeated, independent adaptive divergence that reduces gene flow between ecotypes. Classical examples show parallel speciation originating from shared genomic variation, but this does not seem to be the case in the rough periwinkle (Littorina saxatilis) that has evolved considerable phenotypic diversity across Europe, including several distinct ecotypes. Small 'wave' ecotype snails inhabit exposed rocks and experience strong wave action, while thick-shelled, 'crab' ecotype snails are larger and experience crab predation on less exposed shores. Crab and wave ecotypes appear to have arisen in parallel, and recent evidence suggests only marginal sharing of molecular variation linked to evolution of similar ecotypes in different parts of Europe. However, the extent of genomic sharing is expected to increase with gene flow and more recent common ancestry. To test this, we used de novo RAD-sequencing to quantify the extent of shared genomic divergence associated with phenotypic similarities amongst ecotype pairs on three close islands (<10 km distance) connected by weak gene flow (Nm~0.03) and with recent common ancestry (<10 000 years). After accounting for technical issues, including a large proportion of null alleles due to a large effective population size, we found~8-28% of positive outliers were shared between two islands and~2-9% were shared amongst all three islands. This low level of sharing suggests that parallel phenotypic divergence in this system is not matched by shared genomic divergence despite a high probability of gene flow and standing genetic variation.
Biological Journal of the Linnean Society, 2008
The population genetic structure of marine species lacking free-swimming larvae is expected to be strongly affected by random genetic drift among populations, resulting in genetic isolation by geographical distance. At the same time, ecological separation over microhabitats followed by direct selection on those parts of the genome that affect adaptation might also be strong. Here, we address the question of how the relative importance of stochastic vs. selective structuring forces varies at different geographical scales. We use microsatellite DNA and allozyme data from samples of the marine rocky shore snail Littorina saxatilis over distance scales ranging from metres to 1000 km, and we show that genetic drift is the most important structuring evolutionary force at distances > 1 km. On smaller geographical scales (< 1 km), divergent selection between contrasting habitats affects population genetic structure by impeding gene flow over microhabitat borders (microsatellite structure), or by directly favouring specific alleles of selected loci (allozyme structure). The results suggest that evolutionary drivers of population genetic structure cannot a priori be assumed to be equally important at different geographical scales.
Parallel evolution of similar phenotypes provides strong evidence for the operation of natural selection. Where these phenotypes contribute to reproductive isolation, they further support a role for divergent, habitat-associated selection in speciation. However, the observation of pairs of divergent ecotypes currently occupying contrasting habitats in distinct geographical regions is not sufficient to infer parallel origins. Here we show striking parallel phenotypic divergence between populations of the rocky-shore gastropod, Littorina saxatilis, occupying contrasting habitats exposed to either wave action or crab predation. This divergence is associated with barriers to gene exchange but, nevertheless, genetic variation is more strongly structured by geography than by ecotype. Using approximate Bayesian analysis of sequence data and amplified fragment length polymorphism markers, we show that the ecotypes are likely to have arisen in the face of continuous gene flow and that the demographic separation of ecotypes has occurred in parallel at both regional and local scales. Parameter estimates suggest a long delay between colonization of a locality and ecotype formation, perhaps because the postglacial spread of crab populations was slower than the spread of snails.
Parallel Evolution of Local Adaptation and Reproductive Isolation in the Face of Gene Flow
Evolution, 2013
Parallel evolution of similar phenotypes provides strong evidence for the operation of natural selection. Where these phenotypes contribute to reproductive isolation, they further support a role for divergent, habitat-associated selection in speciation. However, the observation of pairs of divergent ecotypes currently occupying contrasting habitats in distinct geographical regions is not sufficient to infer parallel origins. Here we show striking parallel phenotypic divergence between populations of the rocky-shore gastropod, Littorina saxatilis, occupying contrasting habitats exposed to either wave action or crab predation. This divergence is associated with barriers to gene exchange but, nevertheless, genetic variation is more strongly structured by geography than by ecotype. Using approximate Bayesian analysis of sequence data and amplified fragment length polymorphism markers, we show that the ecotypes are likely to have arisen in the face of continuous gene flow and that the demographic separation of ecotypes has occurred in parallel at both regional and local scales. Parameter estimates suggest a long delay between colonization of a locality and ecotype formation, perhaps because the postglacial spread of crab populations was slower than the spread of snails. Adaptive differentiation may not be fully genetically independent despite being demographically parallel. These results provide new insight into a major model of ecologically driven speciation.
bioRxiv, 2021
Local adaptation to different environments may reinforce neutral evolutionary divergence, especially in populations in the periphery of a species’ geographic range. Seascape genomics (high-throughput genomics coupled with ocean climate databases) facilitates the exploration of neutral and adaptive variation in concert, developing a clearer picture of processes driving local adaptation in marine populations. This study used a seascape genomics approach to test the relative roles of neutral and adaptive processes shaping population divergence of a widespread coral reef snail, Coralliophila violacea. We collected C. violacea from colonies of their coral host (Porites spp.) at ten locations spanning a large portion of their geographic range. We used RAD-seq to investigate possible local adaptation via genetic-environmental associations with five ocean climate variables. Four genetic partitions were concordant with regions previously observed in mtDNA (Indian Ocean, Coral Triangle, and H...