Sensory Drive in Cichlid Speciation

Abstract

The role of selection in speciation is a central yet poorly understood problem in evolutionary biology. The rapid radiations of extremely colorful cichlid fish in African lakes have fueled the hypothesis that sexual selection can drive species divergence without geographical isolation. Here we present experimental evidence for a mechanism by which sexual selection becomes divergent: in two sibling species from Lake Victoria, female mating preferences for red and blue male nuptial coloration coincide with their context-independent sensitivities to red and blue light, which in turn correspond to a difference in ambient light in the natural habitat of the species. These results suggest that natural selection on visual performance, favoring different visual properties in different spectral environments, may lead to divergent sexual selection on male nuptial coloration. This interplay of ecological and sexual selection along a light gradient may provide a mechanism of rapid speciation through divergent sensory drive.

Female mating preference functions predict sexual selection against hybrids between sibling species of cichlid fish

“…This depth segregation decreases with water turbidity and is completely lost at islands with highly turbid waters (Seehausen 1996, in press). Maan et al (2006) found that females of the blue and red species of a population from a clear water island had significant differences in their behavioural sensitivities to red and blue light coinciding with the body coloration of conspecific males. This could imply that in early stages of speciation, the visual system adapts to the light environment at different water depths, leading to divergence in female mating preferences for the male nuptial colours that best match their visual sensitivity.…”

“…Disruptive sexual selection has been proposed to be important in the speciation of the endemic cichlid fish of Lakes Victoria and Malawi (Van Oppen et al 1998;Seehausen & van Alphen 1999;Maan et al 2006). However, the prerequisite of open-ended preference rules that are sign-inversed between the species, surprisingly, had never been tested in any cichlid fish.…”

Divergent Selection on Opsins Drives Incipient Speciation in Lake Victoria Cichlids

“…Female mating preferences may be affected by color vision [22,36], and closely related species with red versus blue male nuptial coloration possess LWS alleles with larger and smaller λ max respectively, where the difference in λ max is similar to the one observed here between L and H alleles [20]. It is therefore conceivable that the reciprocal fixation of LWS alleles with small and large λ max would cause populations at the ends of the water transparency cline to diverge in nuptial coloration, a first step towards parapatric ecological by-product speciation [37].…”

“…Globally, most males of these species are blue or blue-black, but yellow-red (N. greenwoodi/omnicaeruleus) or yellow (M. mbipi) males occur at low, but variable frequencies in much of their ranges. In the relatively turbid waters of Lake Victoria, yellow and red light travel further than blue light, and yellow and red colors may hence be perceived as brighter than blue at long path length (deeper water) [22]. This effect is stronger the more turbid the water [21].…”

“…Given the importance of vision in food acquisition, predator avoidance, territorial defence, and mate choice of cichlid fish, these gradients are likely exerting strong selection on opsin genes and on associated mating traits. In several pairs of closely related species of Lake Victoria cichlids, the species with the larger LWS λ max has red male breeding colors and lower detection thresholds for red light, whereas the species with smaller LWS λ max has blue breeding colors and is less sensitive to red light and more sensitive to blue light, consistent with sensory drive (divergence in male coloration evolving as a consequence of divergent visual sensitivities) [20,22,23]. Hence, the LWS gene may be involved in ecological adaptation and mate choice simultaneously.…”