Abstract
Divergent selection between ecologically dissimilar habitats promotes local adaptation, which can lead to reproductive isolation (RI). Populations in the Poecilia mexicana species complex have independently adapted to toxic hydrogen sulfide and show varying degrees of RI. Here, we examined the variation in the mate choice component of prezygotic RI. Mate choice tests across drainages (with stimulus males from another drainage) suggest that specific features of the males coupled with a general female preference for yellow color patterns explain the observed variation. Analyses of male body coloration identified the intensity of yellow fin coloration as a strong candidate to explain this pattern, and common-garden rearing suggested heritable population differences. Male sexual ornamentation apparently evolved differently across sulfide-adapted populations, for example because of differences in natural counterselection via predation. The ubiquitous preference for yellow color ornaments in poeciliid females likely undermines the emergence of strong RI, as female discrimination in favor of own males becomes weaker when yellow fin coloration in the respective sulfide ecotype increases. Our study illustrates the complexity of the (partly non-parallel) pathways to divergence among replicated ecological gradients. We suggest that future work should identify the genomic loci involved in the pattern reported here, making use of the increasing genomic and transcriptomic datasets available for our study system.
Highlights
All three population pairs in this study show pronounced genetic differentiation, with low levels of gene flow between the ecotypes adapted to sulfidic and non-sulfidic habitats, and reproductive isolation (RI) emerges through both natural and sexual selection, the latter especially driven by females from non-sulfidic habitats discriminating in favor of males from their own ecotype [12,69,70] and by resident males being superior over migrant males in aggressive male contests [71]
Mate choice reduces interbreeding between females from non-sulfidic stream sections and males of the hydrogen sulfide (H2 S)-adapted ecotype, which may occur at the interface between sulfidic and non-sulfidic waters [60,64,112]
We focused on mate choice of females from non-sulfidic habitats on the basis that sulfide-adapted males are more likely to briefly venture into adjoining non-sulfidic stream sections, while the opposite migration direction is prevented by migrants not tolerating exposure to high H2 S concentrations [12,62,70,112]
Summary
Adaptive Divergence along Ecological Gradients and Reproductive Isolation. A central question in evolutionary biology is how divergent ecological selection—e.g., along ecological gradients [1,2,3]—promotes reproductive isolation (RI) [4,5,6], defining the process of ecological speciation [7,8]. Considering speciation along ecological gradients, RI can arise when natural selection acts against maladapted individuals migrating between habitat types [10], e.g., because migrants show increased mortality [11,12,13], have lower reproductive fitness [6,8,14], or because hybrid offspring have higher mortality and/or lower reproductive fitness compared to the average offspring of the resident (locally adapted) population [15,16,17,18,19,20]
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