Abstract

Ecological speciation assumes reproductive isolation to be the product of ecologically based divergent selection. Beside natural selection, sexual selection via phenotype-assortative mating is thought to promote reproductive isolation. Using the neotropical fish Poecilia mexicana from a system that has been described to undergo incipient ecological speciation in adjacent, but ecologically divergent habitats characterized by the presence or absence of toxic H2S and darkness in cave habitats, we demonstrate a gradual change in male body colouration along the gradient of light/darkness, including a reduction of ornaments that are under both inter- and intrasexual selection in surface populations. In dichotomous choice tests using video-animated stimuli, we found surface females to prefer males from their own population over the cave phenotype. However, female cave fish, observed on site via infrared techniques, preferred to associate with surface males rather than size-matched cave males, likely reflecting the female preference for better-nourished (in this case: surface) males. Hence, divergent selection on body colouration indeed translates into phenotype-assortative mating in the surface ecotype, by selecting against potential migrant males. Female cave fish, by contrast, do not have a preference for the resident male phenotype, identifying natural selection against migrants imposed by the cave environment as the major driver of the observed reproductive isolation.

Highlights

  • Environmental gradients can impose divergent selection on populations living along them [1]

  • Using the neotropical fish Poecilia mexicana from a system that has been described to undergo incipient ecological speciation in adjacent, but ecologically divergent habitats characterized by the presence or absence of toxic H2S and darkness in cave habitats, we demonstrate a gradual change in male body colouration along the gradient of light/darkness, including a reduction of ornaments that are under both inter- and intrasexual selection in surface populations

  • MANCOVA on those PC scores detected significant effects of the covariate “SL” and the interaction term “population × SL” (Table 2(a)). The latter suggests that a considerable portion of the total variance can be ascribed to population differences in the relationships between male body size and body colouration; below we discuss this effect for PC5 (see Figure 5(a))

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Summary

Introduction

Environmental gradients can impose divergent selection on populations living along them [1]. Can this drive adaptive trait divergence among populations [2, 3], but it can foster the evolution of reproductive isolation barriers [4,5,6]. Natural selection can prevent interbreeding of locally adapted populations if (a) immigrants exhibit reduced viability in the habitat type they are not adapted to [7,8,9],. Populations living in extreme environments are of particular interest to evolutionary ecologists. Environments can be extreme due to the presence of toxins and toxicants, like hydrogen sulphide (H2S) [20, 21]. H2S is acutely toxic to most metazoans because it inhibits aerobic respiration due to its interference with mitochondrial respiration and blood oxygen transport while simultaneously leading to extreme hypoxia in the water [20, 21]

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