title: Unique evolutionary trajectories in repeated adaptation to hydrogen sulphide-toxic habitats of a neotropical fish (Poecilia mexicana).
abstract: 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 (H2 S) 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 bidirectional 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  = 0.0091). At the level of metabolic pathways, the overlap was Jcorr  = 0.2545, indicating increasing parallelism with increasing level of biological integration. The majority of pathways contained positively selected genes in both sulphide populations. Hence, adaptation to sulphidic 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.
authors.affiliation: Molecular Ecology Group, Senckenberg Biodiversity and Climate Research Centre (BiK-F), Senckenberganlage 25, D-60325 Frankfurt am Main, Hessen, Germany.
authors.forename: Markus
authors.initials: M
authors.lastname: Pfenninger
authors.affiliation: Molecular Ecology Group, Senckenberg Biodiversity and Climate Research Centre (BiK-F), Senckenberganlage 25, D-60325 Frankfurt am Main, Hessen, Germany.
authors.forename: Simit
authors.initials: S
authors.lastname: Patel
authors.affiliation: División Académica de Ciencias Biológicas, Universidad Juárez Autónoma de Tabasco (UJAT), Villahermosa, C.P. 86150 Tabasco, México.
authors.forename: Lenin
authors.initials: L
authors.lastname: Arias-Rodriguez
authors.affiliation: Molecular Ecology Group, Senckenberg Biodiversity and Climate Research Centre (BiK-F), Senckenberganlage 25, D-60325 Frankfurt am Main, Hessen, Germany.
authors.forename: Barbara
authors.initials: B
authors.lastname: Feldmeyer
authors.affiliation: School of Biological Sciences, Centre for Ecology, Evolution and Behaviour, Royal Holloway University of London, Egham Hill, Egham, Surrey TW20 0EX, UK.
authors.forename: Rüdiger
authors.initials: R
authors.lastname: Riesch
authors.affiliation: College of Animal Science and Technology, Northwest A&F University, Xinong Road 22, 712100 Yangling, China.
authors.forename: Martin
authors.initials: M
authors.lastname: Plath
mesh_terms: D000222:Adaptation, Physiological / Q000235:genetics*; D000818:Animals; D017753:Ecosystem; D019143:Evolution, Molecular; D051456:Gene Flow; D014644:Genetic Variation; D005828:Genetics, Population; D006862:Hydrogen Sulfide / Q000633:toxicity*; D011036:Poecilia / Q000235:genetics*; D020641:Polymorphism, Single Nucleotide; D011156:Population Density; D012641:Selection, Genetic; D017422:Sequence Analysis, DNA
chemical_list: D006862:Hydrogen Sulfide
keywords: adaptation; ecological genetics; evolutionary theory; fish; molecular evolution; parallel evolution