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Prevalence of disruptive selection predicts extent of species differentiation in Lake Victoria cichlids.

ABSTRACT: Theory suggests that speciation with gene flow is most likely when both sexual and ecological selection are divergent or disruptive. Divergent sexual and natural selection on the visual system have been demonstrated before in sympatric, morphologically similar sister species of Lake Victoria cichlids, but this does not explain the subtle morphological differences between them. To investigate the significance of natural selection on morphology during speciation, we here ask whether the prevalence of disruptive ecological selection differs between sympatric sister species that are at different stages of speciation. Some of our species pairs do (Pundamilia) and others do not (Neochromis) differ distinctively in sexually selected male nuptial coloration. We find that (i) evidence for disruptive selection, and for evolutionary response to it, is prevalent in traits that are differentiated between sister species; (ii) prevalence of both predicts the extent of genetic differentiation; and (iii) genetic differentiation is weaker in species pairs with conserved male nuptial coloration. Our results speak to the existence of two different mechanisms of speciation with gene flow: speciation mainly by sexual selection tightly followed by ecological character displacement in some cases and speciation mainly by divergent ecological selection in others.

SUBMITTER: van Rijssel JC

PROVIDER: S-EPMC5805951 | biostudies-literature | 2018 Jan

REPOSITORIES: biostudies-literature

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Prevalence of disruptive selection predicts extent of species differentiation in Lake Victoria cichlids.

van Rijssel Jacco C JC Moser Florian N FN Frei David D Seehausen Ole O

Proceedings. Biological sciences 20180101 1871

Theory suggests that speciation with gene flow is most likely when both sexual and ecological selection are divergent or disruptive. Divergent sexual and natural selection on the visual system have been demonstrated before in sympatric, morphologically similar sister species of Lake Victoria cichlids, but this does not explain the subtle morphological differences between them. To investigate the significance of natural selection on morphology during speciation, we here ask whether the prevalence ...[more]

PMID: 29367400

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Project description:Studying phenotypic and genetic differentiation between very young species can be very informative with regard to learning about processes of speciation. Identifying and characterizing genetic species structure and distinguishing it from spatial genetic structure within a species is a prerequisite for this and is often not given sufficient attention. Young radiations of cichlid fish are classical speciation study systems. However, it is only during the past decade that population genomics based on next-generation sequencing has begun to provide the power to resolve species and distinguish speciation from spatial population structure for the youngest of these radiations. The Lake Victoria haplochromine cichlids constitute the youngest large cichlid fish radiation, probably <20,000 years old. Earlier work showed that communities of rocky reef cichlids are composed of many reciprocally monophyletic species despite their very recent origins. Here, we build on this work by studying assemblages of offshore demersal cichlids, adding analyses of within-species spatial structure to the sympatric species structure. We sampled seven multispecies communities along a 6-km-long transect from one side of the Mwanza Gulf to the other side. We investigated whether phenotypically diagnosed putative species are reciprocally monophyletic and whether such monophyly is stable across species geographic ranges. We show that all species are genetically strongly differentiated in sympatry, that they are reciprocally monophyletic, and that monophyly is stable across distribution ranges. We found significant differentiation between geographically distinct populations in two species, but no or weak isolation by distance. We further found subtle but significant morphological differences between all species and a linear relationship between genomic and morphological distance which suggests that differences in morphology begin to accumulate after speciation has already affected genome-wide restrictions of gene flow.

Project description:Adaptation to heterogeneous sensory environments has been implicated as a key parameter in speciation. Cichlid fish are a textbook example of divergent visual adaptation, mediated by variation in the sequences and expression levels of cone opsin genes (encoding the protein component of visual pigments). In some vertebrates including fish, visual sensitivity is also tuned by the ratio of vitamin A1 /A2 -derived chromophores (i.e., the light-sensitive component of the visual pigment bound to the opsin protein), where higher proportions of A2 cause a more red-shifted wavelength absorbance. This study explores the variation in chromophore ratios across multiple cichlid populations in Lake Victoria, using as a proxy the expression of the gene Cyp27c1, which has been shown to regulate the conversion of vitamin A1 into vitamin A2 in several vertebrates. This study focuses on sympatric Pundamilia cichlids, where species with blue or red male coloration co-occur at multiple islands but occupy different depths and consequently different visual habitats. In the red species, we found higher cyp27c1 expression in populations from turbid waters than from clear waters, but there was no such pattern in the blue species. Across populations, differences between the sympatric species in cyp27c1 expression had a consistent relationship with species differences in opsin expression patterns, but the red/blue identity reversed between clear and turbid waters. To assess the contribution of heritable vs. environmental causes of variation, we tested whether light manipulations induce a change in cyp27c1 expression in the laboratory. We found that cyp27c1 expression was not influenced by experimental light conditions, suggesting that the observed variation in the wild is due to genetic differences. Nonetheless, compared to other cichlid species, cyp27c1 is expressed at very low levels in Pundamilia, suggesting that it may not be relevant for visual adaptation in this species. Conclusively, establishing the biological importance of this variation requires testing of actual A1 /A2 ratios in the eye, as well as its consequences for visual performance.

Dataset Information

Prevalence of disruptive selection predicts extent of species differentiation in Lake Victoria cichlids.

Publications

Prevalence of disruptive selection predicts extent of species differentiation in Lake Victoria cichlids.

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