Molecular Ecology - accepted article
Replicated ecological gradients are prime systems to study processes of molecular evolution underlying ecological divergence. Here we investigated the repeated adaptation of the Neotropical fish Poecilia mexicana to habitats containing toxic hydrogen sulphide (H2S), and compared two population pairs of sulphide-adapted and ancestral fish by sequencing population pools of > 200 individuals (Pool-Seq). We inferred the evolutionary processes shaping divergence and tested the hypothesis of increase of parallelism from SNPs to molecular pathways.
Coalescence analyses showed that the divergence occurred in the face of substantial bi-directional gene-flow. Population divergence involved many short, widely dispersed regions across the genome. Analyses of allele frequency spectra suggest that differentiation at most loci was driven by divergent selection, followed by a selection-mediated reduction of gene-flow. Reconstructing allelic state changes suggested that selection acted mainly upon de novo mutations in the sulphide-adapted populations. Using a corrected Jaccard-index to quantify parallel evolution, we found a negligible proportion of statistically significant parallel evolution of Jcorr=0.0032 at the level of SNPs, divergent genome regions (Jcorr=0.0061), and genes therein (Jcorr=0.0076). At the level of metabolic pathways, the overlap wasJcorr=0.2455, indicating increasing parallelism with increasing level of biological integration. The majority of pathways contained positively selected genes in both sulphide populations.
Adaptation to sulphide habitats necessitated adjustments throughout the genome. The largely unique evolutionary trajectories may be explained by a high proportion of de novo mutations driving the divergence. Our findings favour Gould's view that evolution is often the unrepeatable result of stochastic events with highly contingent effects.