title: Extremophile Poeciliidae: multivariate insights into the complexity of speciation along replicated ecological gradients.
abstract: Replicate population pairs that diverge in response to similar selective regimes allow for an investigation of (a) whether phenotypic traits diverge in a similar and predictable fashion, (b) whether there is gradual variation in phenotypic divergence reflecting variation in the strength of natural selection among populations, (c) whether the extent of this divergence is correlated between multiple character suites (i.e., concerted evolution), and (d) whether gradual variation in phenotypic divergence predicts the degree of reproductive isolation, pointing towards a role for adaptation as a driver of (ecological) speciation. Here, we use poeciliid fishes of the genera Gambusia and Poecilia that have repeatedly evolved extremophile lineages able to tolerate high and sustained levels of toxic hydrogen sulfide (H2S) to answer these questions.
  
  
  
  We investigated evolutionary divergence in response to H2S in Gambusia spp. (and to a lesser extent Poecilia spp.) using a multivariate approach considering the interplay of life history, body shape, and population genetics (nuclear miscrosatellites to infer population genetic differentiation as a proxy for reproductive isolation). We uncovered both shared and unique patterns of evolution: most extremophile Gambusia predictably evolved larger heads and offspring size, matching a priori predictions for adaptation to sulfidic waters, while variation in adult life histories was idiosyncratic. When investigating patterns for both genera (Gambusia and Poecilia), we found that divergence in offspring-related life histories and body shape were positively correlated across populations, but evidence for individual-level associations between the two character suites was limited, suggesting that genetic linkage, developmental interdependencies, or pleiotropic effects do not explain patterns of concerted evolution. We further found that phenotypic divergence was positively correlated with both environmental H2S-concentration and neutral genetic differentiation (a proxy for gene flow).
  
  
  
  Our results suggest that higher toxicity exerts stronger selection, and that divergent selection appears to constrain gene flow, supporting a scenario of ecological speciation. Nonetheless, progress toward ecological speciation was variable, partially reflecting variation in the strength of divergent selection, highlighting the complexity of selective regimes even in natural systems that are seemingly governed by a single, strong selective agent.
authors.affiliation: School of Biological Sciences, Royal Holloway University of London, Egham, Surrey, TW20 0EX, UK. Rudiger.Riesch@rhul.ac.uk.|Department of Biological Sciences & W. M. Keck Center for Behavioral Biology, North Carolina State University, 127 David Clark Labs, Raleigh, NC, 27695-7617, USA. Rudiger.Riesch@rhul.ac.uk.
authors.forename: Rüdiger
authors.identifier: 0000-0002-6769-8808
authors.initials: R
authors.lastname: Riesch
authors.affiliation: Division of Biology, Kansas State University, 116 Ackert Hall, Manhattan, KS, 66506, USA.
authors.forename: Michael
authors.initials: M
authors.lastname: Tobler
authors.affiliation: Natural History Collections, Museum Wiesbaden, Friedrich-Ebert-Allee 2, 65185, Wiesbaden, Germany.
authors.forename: Hannes
authors.initials: H
authors.lastname: Lerp
authors.affiliation: J. W. Goethe-University Frankfurt/M., Evolutionary Ecology Group, Max-von-Laue Str. 13, 60438, Frankfurt a. M., Germany.
authors.forename: Jonas
authors.initials: J
authors.lastname: Jourdan
authors.affiliation: Department of Biology and Biochemistry, University of Houston, 4800 Calhoun Rd., Houston, TX, 77004, USA.
authors.forename: Tess
authors.initials: T
authors.lastname: Doumas
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK.
authors.forename: Patrik
authors.initials: P
authors.lastname: Nosil
authors.affiliation: Department of Biological Sciences & W. M. Keck Center for Behavioral Biology, North Carolina State University, 127 David Clark Labs, Raleigh, NC, 27695-7617, USA.
authors.forename: R Brian
authors.initials: RB
authors.lastname: Langerhans
authors.affiliation: College of Animal Science and Technology, Northwest A&F University, Xinong Road 22, Yangling, 712100, People's Republic of China.
authors.forename: Martin
authors.initials: M
authors.lastname: Plath
mesh_terms: D000220:Adaptation, Biological; D000818:Animals; D005075:Biological Evolution; D003532:Cyprinodontiformes / Q000378:metabolism / Q000502:physiology*; D017753:Ecosystem; D000071825:Extremophiles / Q000378:metabolism / Q000502:physiology*; D005260:Female; D051456:Gene Flow; D049810:Genetic Speciation; D006862:Hydrogen Sulfide / Q000378:metabolism; D008297:Male; D015999:Multivariate Analysis; D010641:Phenotype; D011036:Poecilia / Q000378:metabolism / Q000502:physiology*; D060047:Reproductive Isolation; D012641:Selection, Genetic
chemical_list: D006862:Hydrogen Sulfide
keywords: Ecological speciation; Gambusia; Hydrogen sulfide; Life-history evolution; Morphometrics; Poecilia; Reproductive isolation