Extremophile Poeciliidae: multivariate insights into the complexity of speciation along replicated ecological gradients

Abstract

BackgroundReplicate 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.ResultsWe 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).ConclusionsOur 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0705-1) contains supplementary material, which is available to authorized users.

Extreme environments and the origins of biodiversity: Adaptation and speciation in sulphide spring fishes

“…The clearly defined selective regimes in extreme environments enable hypothesis‐driven tests of responses at all levels of biological organization and facilitate integrative approaches to study the causes and consequences of adaptive evolution (Nevo, ; Tobler, Riesch, & Plath, ). In addition, the availability of replicated lineages exposed to the same physicochemical stressors allows for evolutionary analyses in a comparative context, spanning vast geographic and phylogenetic distances (Riesch, Plath, Schlupp, Tobler, & Langerhans, ; Riesch et al., ). Here, we review recent research on fishes inhabiting hydrogen sulphide‐rich springs that sheds light onto mechanisms of adaptation, speciation and convergent evolution.…”

Multiple traits and multifarious environments: integrated divergence of morphology and life history

“…Understanding complex phenotypic divergence is critical for comprehending adaptive evolution. Yet few studies have explicitly investigated joint/independent changes of disparate type of phenotypes (Conner and Via 1993, Hendry and Quinn 1997, Wesner et al 2011, Riesch et al 2016. Here, our PLS-SEM results showed that the two character suites did not greatly influence one another during phenotypic divergence among blue holes.…”

“…the guppy Poecilia reticulata: Reznick and Endler 1982 (life history); Hendry et al 2006 (morphology)). In the comparatively rare cases where co-divergence in multiple trait suites are examined (Conner and Via 1993, Hendry and Quinn 1997, Wesner et al 2011, Riesch et al 2016, seldom is this combined with the study of multiple selective factors. However, only by simultaneously investigating multiple types of traits and multiple agents of selection can we more fully understand the complexity of adaptive diversification (Lardner 2000, DeWitt andLangerhans 2003).…”

Testes mass in the livebearing fish Brachyrhaphis rhabdophora (Poeciliidae) varies hypoallometrically with body size but not between predation environments

“…Correspondingly, display rates are lower because males trade off sexual selection (opportunity to reproduce) with natural selection (due to predation; Godin, 1995;Langerhans et al, 2005;Luyten & Liley, 1985), and competition among males occurs after fertilization in the form of sperm competition rather than prior to copulation (Kawase et al, 2017;Stockley et al, 1997). Though studies have described testes mass as it fluctuates in various high-mortality environments (Riesch et al, 2011), few studies have yet revealed how testes mass correlates with body mass among size classes and predation environments (Riesch et al, 2013(Riesch et al, , 2016.…”

“…In contrast, Poecilia mexicana males living in high‐mortality sulphidic environments have lower GSIs than those living in low‐mortality nonsulphidic environments (Riesch, Plath, & Schlupp, ). More recently, Poecilia mexicana and other related species exhibited no substantial differences in GSI across environments differing in mortality rates (Riesch et al, ). The results in Gambusia hubbsi (Riesch et al, ) are what we would expect according to life history theory: In high‐predation environments, males have less competition (lower density of conspecifics) prior to fertilization than males in low‐predation environments.…”