Inheritance of female mating preference in a sympatric sibling species pair of Lake Victoria cichlids: implications for speciation

Abstract

Female mate choice has often been proposed to play an important role in cases of rapid speciation, in particular in the explosively evolved haplochromine cichlid species flocks of the Great Lakes of East Africa. Little, if anything, is known in cichlid radiations about the heritability of female mating preferences. Entirely sympatric distribution, large ecological overlap and conspicuous differences in male nuptial coloration, and female preferences for these, make the sister species Pundamilia pundamilia and P. nyererei from Lake Victoria an ideally suited species pair to test assumptions on the genetics of mating preferences made in models of sympatric speciation. Female mate choice is necessary and sufficient to maintain reproductive isolation between these species, and it is perhaps not unlikely therefore, that female mate choice has been important during speciation. A prerequisite for this, which had remained untested in African cichlid fish, is that variation in female mating preferences is heritable. We investigated mating preferences of females of these sister species and their hybrids to test this assumption of most sympatric speciation models, and to further test the assumption of some models of sympatric speciation by sexual selection that female preference is a single-gene trait. We find that the differences in female mating preferences between the sister species are heritable, possibly with quite high heritabilities, and that few but probably more than one genetic loci contribute to this behavioural speciation trait with no apparent dominance. We discuss these results in the light of speciation models and the debate about the explosive radiation of cichlid fishes in Lake Victoria.

Figure 1

Mean preference indices and standard errors of all females tested. ^*Significant preferences (p < 0.05). Each female was tested with six different male pairs unless when indicated otherwise above the bars. (a) Parental-type female preferences, and one example of each of the two male colour phenotypes; (b) F₁ hybrid female preferences; (c) F₂ hybrid female preferences.

Figure 2

Mean preference index (x-axis) and variance (y-axis) for parental type, F₁ hybrid and F₂ hybrid females. (a) Experiment series 1: raw preferences; (b) experiment series 2: raw preferences; (c) series 1: residual preferences; (d) series 2: residual preferences; (e) both experiment series combined: residual preferences.

Figure 3

Relationship between strength and consistency of female mating preference: absolute mean preference index and its coefficient of variation (CV) for all females (16 parental type, filled circles; 20 F₁ hybrids, filled diamonds; and 33 F₂ hybrids, open circles). A high CV reflects lack of consistency in relative response to red and blue males; a high absolute mean preference index reflects a strong mean mating preference.