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

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.

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

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.

Developmental effects of environmental light on male nuptial coloration in Lake Victoria cichlid fish

BackgroundEfficient communication requires that signals are well transmitted and perceived in a given environment. Natural selection therefore drives the evolution of different signals in different environments. In addition, environmental heterogeneity at small spatial or temporal scales may favour phenotypic plasticity in signaling traits, as plasticity may allow rapid adjustment of signal expression to optimize transmission. In this study, we explore signal plasticity in the nuptial coloration of Lake Victoria cichlids,Pundamilia pundamiliaandPundamilia nyererei.These two species differ in male coloration, which mediates species-assortative mating. They occur in adjacent depth ranges with different light environments. Given the close proximity of their habitats, overlapping at some locations, plasticity in male coloration could contribute to male reproductive success but interfere with reproductive isolation.MethodsWe rearedP. pundamilia,P. nyererei,and their hybrids under light conditions mimicking the two depth ranges in Lake Victoria. From photographs, we quantified the nuptial coloration of males, spanning the entire visible spectrum. In experiment 1, we examined developmental colour plasticity by comparing sibling males reared in each light condition. In experiment 2, we assessed colour plasticity in adulthood, by switching adult males between conditions and tracking coloration for 100 days.ResultsWe found that nuptial colour inPundamiliadid respond plastically to our light manipulations, but only in a limited hue range. Fish that were reared in light conditions mimicking the deeper habitat were significantly greener than those in conditions mimicking shallow waters. The species-specific nuptial colours (blue and red) did not change. When moved to the opposing light condition as adults, males did not change colour.DiscussionOur results show that species-specific nuptial colours, which are subject to strong divergent selection by female choice, are not plastic. We do find plasticity in green coloration, a response that may contribute to visual conspicuousness in darker, red-shifted light environments. These results suggest that light-environment-induced plasticity in male nuptial coloration inP. pundamiliaandP. nyerereiis limited and does not interfere with reproductive isolation.

Developmental effects of environmental light on male nuptial coloration in Lake Victoria cichlid fish

Background. Efficient communication requires that signals are well transmitted and perceived in a given environment. Natural selection therefore drives the evolution of different signals in different environments. In addition, environmental heterogeneity at small spatial or temporal scales may favour phenotypic plasticity in signaling traits, as plasticity may allow rapid adjustment of signal expression to optimize transmission. In this study, we explore signal plasticity in the nuptial coloration of Lake Victoria cichlids, Pundamilia pundamilia and Pundamilia nyererei. These two species differ in male coloration, which mediates species-assortative mating. They occur in adjacent depth ranges with different light environments. Given the close proximity of their habitats, overlapping at some locations, plasticity in male coloration could contribute to male reproductive success but interfere with reproductive isolation. Methods. We reared P. pundamilia, P. nyererei, and their hybrids under light conditions mimicking the two depth ranges in Lake Victoria. From photographs, we quantified the nuptial coloration of males, spanning the entire visible spectrum. In experiment 1, we examined developmental colour plasticity by comparing sibling males reared in each light condition. In experiment 2, we assessed colour plasticity in adulthood, by switching adult males between conditions and tracking coloration for 100 days. Results. We found that nuptial colour in Pundamilia did respond plastically to our light manipulations, but only in a limited hue range. Fish that were reared in light conditions mimicking the deeper habitat were significantly greener than those in conditions mimicking shallow waters. The species-specific nuptial colours (blue and red) did not change. When moved to the opposing light condition as adults, males did not change colour. Discussion. Our results show that species-specific nuptial colours, which are subject to strong divergent selection by female choice, are not plastic. We do find plasticity in green coloration, a response that may contribute to visual conspicuousness in darker, red-shifted light environments. These results suggest that light-environment-induced plasticity in male nuptial coloration in P. pundamilia and P. nyererei is limited and does not interfere with reproductive isolation.