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.

Keywords: assortative mating; character displacement; disruptive selection; evolutionary response; fitness surface; speciation with gene flow.

Figure 1.

Map of Lake Victoria and the Mwanza Gulf indicating sampling sites, and the seven form pairs at different stages of speciation. Half blue and red circles indicate islands where the Pundamilia pairs occur, the half blue and half black rectangles indicates the occurrence of the Neochromis pairs. Genomic divergence is based on RAD tag F_ST-values from Meier et al. [20] and Brawand et al. [43], and on microsatellites F_ST-values from Seehausen et al. [23] and Magalhaes et al. [22]. Asterisks indicates a significant F_ST-value.

Figure 2.

Fitness surfaces for the (a) Pundamilia and (b) Neochromis form pairs. Only surfaces shown that imply disruptive selection on univariate morphological or ecological traits that differ between the two species and that have a significantly better fit of the quadratic, 3rd or 4th order model compared to the linear model (dAICc of greater than 2.5) using complete sample sizes, all other data are shown in figures S14–S20 of the electronic supplementary material. Density of individuals at each trait value is indicated with thin black lines. For Pundamilia: red dots, P. nyererei and P. sp. nyererei-like; blue dots, P. pundamilia and P. sp. pundamilia-like. For Neochromis: black dots, N. ‘unicuspid scraper’; blue dots, N. omnicaeruleus/N. greenwoodi; green dots, intermediate phenotypes. Large dots indicate average trait values and growth rate averages per species, error bars indicate trait standard deviations.

Figure 3.

Plot of genetic divergence versus the number of univariate morphological and ecological traits showing evidence of disruptive selection. Genetic divergence is based on microsatellites [22,23]. The plot illustrates two different putative speciation mechanisms; for Pundamilia (red), the number of traits under disruptive selection might increase only when reproductive isolation, possibly induced by sexual selection, reaches a certain threshold, for Neochromis (blue), a relatively large number of traits under ecological disruptive selection might be necessary to establish and maintain reproductive isolation. The dashed line separates the form pairs with a significant F_ST-value from the ones without a significant F_ST-value.