Locally adapted fish populations maintain small-scale genetic differentiation despite perturbation by a catastrophic flood event

Martin Plath,Francisco J García de León,Bernd Hermann,Michael Tobler,Christiane Schröder,Rüdiger Riesch,Ralph Tiedemann,Ingo Schlupp

doi:10.1186/1471-2148-10-256

Martin Plath, Francisco J García de León + Show 6 more

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https://doi.org/10.1186/1471-2148-10-256

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Abstract

BackgroundLocal adaptation to divergent environmental conditions can promote population genetic differentiation even in the absence of geographic barriers and hence, lead to speciation. Perturbations by catastrophic events, however, can distort such parapatric ecological speciation processes. Here, we asked whether an exceptionally strong flood led to homogenization of gene pools among locally adapted populations of the Atlantic molly (Poecilia mexicana, Poeciliidae) in the Cueva del Azufre system in southern Mexico, where two strong environmental selection factors (darkness within caves and/or presence of toxic H2S in sulfidic springs) drive the diversification of P. mexicana. Nine nuclear microsatellites as well as heritable female life history traits (both as a proxy for quantitative genetics and for trait divergence) were used as markers to compare genetic differentiation, genetic diversity, and especially population mixing (immigration and emigration) before and after the flood.ResultsHabitat type (i.e., non-sulfidic surface, sulfidic surface, or sulfidic cave), but not geographic distance was the major predictor of genetic differentiation. Before and after the flood, each habitat type harbored a genetically distinct population. Only a weak signal of individual dislocation among ecologically divergent habitat types was uncovered (with the exception of slightly increased dislocation from the Cueva del Azufre into the sulfidic creek, El Azufre). By contrast, several lines of evidence are indicative of increased flood-induced dislocation within the same habitat type, e.g., between different cave chambers of the Cueva del Azufre.ConclusionsThe virtual absence of individual dislocation among ecologically different habitat types indicates strong natural selection against migrants. Thus, our current study exemplifies that ecological speciation in this and other systems, in which extreme environmental factors drive speciation, may be little affected by temporary perturbations, as adaptations to physico-chemical stressors may directly affect the survival probability in divergent habitat types.

Highlights

Local adaptation to divergent environmental conditions can promote population genetic differentiation even in the absence of geographic barriers and lead to speciation
The absence of light in caves inhibits the use of visual senses, and cave-dwellers are under selection to cope with the impossibility for visual orientation and communication [37,38,39,40], especially if they evolved from a diurnal surface-dwelling form like in P. mexicana (Poeciliidae) [41,42] and Astyanax mexicanus (Characidae, [43,44,45])
We found 12 different novel alleles to occur in chamber XIII after the flood that had previously been recorded exclusively in one or both of the other cave chambers, which was reflected by large and significant pair-wise Fst-values for the comparison of pre- and post-flood data (e.g., 0.173 in chamber XIII; Table 4)

Summary

Introduction

Local adaptation to divergent environmental conditions can promote population genetic differentiation even in the absence of geographic barriers and lead to speciation. Poecilia mexicana in the Cueva del Azufre System In the Cueva del Azufre system in southern Mexico, ecologically divergent aquatic habitats are characterized by the presence or absence of toxic hydrogen sulfide (H2S) and/or light (i.e., cave versus surface habitats [26,27,30]), resulting in several non-toxic surface habitats, a toxic creek (El Azufre), as well as a toxic and a non-toxic cave: the ‘Cueva del Azufre’ ( called ‘Cueva de Villa Luz’ or ‘Cueva de las Sardinas’ [31]), and the ‘Cueva Luna Azufre’, respectively ([26,32]; Fig. 1). The hydrogen sulfide in this system stems from natural (volcanic) sources [33] Both the presence of H2S and the absence of light exert strong selection on organisms exposed to them. The absence of light in caves inhibits the use of visual senses, and cave-dwellers are under selection to cope with the impossibility for visual orientation and communication [37,38,39,40], especially if they evolved from a diurnal surface-dwelling form like in P. mexicana (Poeciliidae) [41,42] and Astyanax mexicanus (Characidae, [43,44,45])

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