Female preferences between incipient species of Drosophila athabasca reveal divergent closed functions, epistasis, and segregation of veiled preference alleles.

Abstract

Theoretical models typically assume that speciation is driven by divergence in female preference functions for secondary sexual traits. However, little is known about how these functions diverge between incipient species. This study used song playback experiments and mate choice tests to characterize female preference functions for divergent male courtship songs between two incipient species of Drosophila athabasca complex; D. athabasca (WN) and Drosophila mahican (EA). The study focused on two male song parameters: pulses per burst (PPB) and inter-pulse interval (IPI). Preference functions for PPB were open-ended and lacked species-specificity. In contrast, preference functions for IPI revealed a closed shape, with peak preferences highly divergent between species. Thus, females imposed divergent and ongoing sexual selection on male IPI. Further work demonstrated variation in peak preferences and choosiness for IPI across genetic lines, while F1 hybrid females varied extensively in their mating preferences across different heterospecific line crosses. Finally, F2 female genotypes with foreign single-copy chromosome substitutions showed little to no change in preferences until three or four chromosomes were combined: indicating strong dominance epistasis. These results suggest "veiled" or hidden segregating female preference alleles for male speciation phenotypes. This may explain the rapid speciation observed in this species complex.