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Genetic architecture of a key reproductive isolation trait differs between sympatric and non-sympatric sister species of Lake Victoria cichlids.

ABSTRACT: One hallmark of the East African cichlid radiations is the rapid evolution of reproductive isolation that is robust to full sympatry of many closely related species. Theory predicts that species persistence and speciation in sympatry with gene flow are facilitated if loci of large effect or physical linkage (or pleiotropy) underlie traits involved in reproductive isolation. Here, we investigate the genetic architecture of a key trait involved in behavioural isolation, male nuptial coloration, by crossing two sister species pairs of Lake Victoria cichlids of the genus Pundamilia and mapping nuptial coloration in the F2 hybrids. One is a young sympatric species pair, representative of an axis of colour motif differentiation, red-dorsum versus blue, that is highly recurrent in closely related sympatric species. The other is a species pair representative of colour motifs, red-chest versus blue, that are common in allopatric but uncommon in sympatric closely related species. We find significant quantitative trait loci (QTLs) with moderate to large effects (some overlapping) for red and yellow in the sympatric red-dorsum × blue cross, whereas we find no significant QTLs in the non-sympatric red-chest × blue cross. These findings are consistent with theory predicting that large effect loci or linkage/pleiotropy underlying mating trait differentiation could facilitate speciation and species persistence with gene flow in sympatry.

SUBMITTER: Feller AF

PROVIDER: S-EPMC7209058 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Genetic architecture of a key reproductive isolation trait differs between sympatric and non-sympatric sister species of Lake Victoria cichlids.

Feller Anna F AF Haesler Marcel P MP Peichel Catherine L CL Seehausen Ole O

Proceedings. Biological sciences 20200408 1924

One hallmark of the East African cichlid radiations is the rapid evolution of reproductive isolation that is robust to full sympatry of many closely related species. Theory predicts that species persistence and speciation in sympatry with gene flow are facilitated if loci of large effect or physical linkage (or pleiotropy) underlie traits involved in reproductive isolation. Here, we investigate the genetic architecture of a key trait involved in behavioural isolation, male nuptial coloration, by ...[more]

PMID: 32259470

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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

Genetic architecture of a key reproductive isolation trait differs between sympatric and non-sympatric sister species of Lake Victoria cichlids.

Publications

Genetic architecture of a key reproductive isolation trait differs between sympatric and non-sympatric sister species of Lake Victoria cichlids.

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