Learning magnifies individual variation in heterospecific mating propensity

Keywords: assortative mating Drosophila persimilis Drosophila pseudoobscura fruit fly learning Recent research indicating learning in the context of sexual behaviour in fruit flies suggests that learning could increase levels of assortative mating between partially diverged populations. We present a graphic model examining the role of learning and a series of experiments evaluating assumptions and predictions of the model. We found that male Drosophila persimilis that previously succeeded in mating with females of the sibling species, D. pseudoobscura, did not have a higher heterospecific mating success than males that were either virgin or previously mated with conspecific females. On the other hand, female D. pseudoobscura with apparently strict mating criteria, which rejected heterospecific males, were also more likely to reject conspecific males than were females inexperienced with males. Finally, D. persimilis males previously rejected by heterospecific females courted significantly less and had half as much heterospecific mating success as males previously accepted by heterospecific females. These results, combined with previous evidence demonstrating that males rejected by heterospecific females learn to avoid courting such females, indicate that learning can increase phenotypic divergence between populations with partial pre-mating isolation. New information regarding learning in the context of courtship and mate choice in fruit flies (Drosophila spp.) has provided exciting fresh opportunities for examining effects of learning on processes leading to population divergence in one of the key model organisms used in research on speciation (e.g. Coyne & Orr 1989; Noor & Feder 2006). Specifically, work with two pairs of sibling species, D. melanogaster–D. simulans and D. persimilis–D. pseudoobscura has indicated that males that experience rejection by heterospecific females rapidly learn to reduce courtship of such females (Dukas 2004b, 2008, 2009). Whereas the studies indicating learning in the context of sexual behaviour in fruit flies suggested that learning can increase assor-tative mating, the experimental protocols used actually simulated interactions between two species that are already fully reproductively isolated because the experience phases always included heterospecific rejection. To understand the role of learning in the divergence of populations that are only partially isolated, however, we have to simulate the realistic scenario in which some proportion of the males succeed in acquiring heterospecific mates while the majority fail. Learning could contribute to population divergence even under such realistic settings, and here we examine this possibility using a graphical model and empirical tests. Suppose that two populations that are partially reproductively isolated come into contact in sympatry …