Sexual imprinting on ecologically divergent traits leads to sexual isolation in sticklebacks

Abstract

During sexual imprinting, offspring learn parental phenotypes and then select mates who are similar to their parents. Imprinting has been thought to contribute to the process of speciation in only a few rare cases; this is despite imprinting's potential to generate assortative mating and solve the problem of recombination in ecological speciation. If offspring imprint on parental traits under divergent selection, these traits will then be involved in both adaptation and mate preference. Such 'magic traits' easily generate sexual isolation and facilitate speciation. In this study, we show that imprinting occurs in two ecologically divergent stickleback species (benthics and limnetics: Gasterosteus spp.). Cross-fostered females preferred mates of their foster father's species. Furthermore, imprinting is essential for sexual isolation between species; isolation was reduced when females were raised without fathers. Daughters imprinted on father odour and colour during a critical period early in development. These traits have diverged between the species owing to differences in ecology. Therefore, we provide the first evidence that imprinting links ecological adaptation to sexual isolation between species. Our results suggest that imprinting may facilitate the evolution of sexual isolation during ecological speciation, may be especially important in cases of rapid diversification, and thus play an integral role in the generation of biodiversity.

Biased learning affects mate choice in a butterfly

“…Although biases in mate-preference learning have not yet been reported in species outside of B. anynana, they may have been overlooked because of the long training periods used in other mate-preference learning studies (13,14,(47)(48)(49). Song-learning biases are especially apparent in laboratory studies when training periods or event number are reduced (reviewed in ref.…”

Early song discrimination by nestling sparrows in the wild

“…For example, relative abundance of conspecifics and heterospecifics in a population may affect the benefits of excluding heterospecifics in a territorial setting or courting heterospecific mates (Ord et al, 2011;Reeve, 1989). Similarly, prior experience with conspecific or heterospecific individuals of the opposite sex can affect mate recognition (Dukas, 2008;Hebets, 2003;Kozak and Boughman, 2009;Kozak et al, 2011;Svensson et al, 2010;Verzijden and ten Cate, 2007). Playback experiments to naïve juveniles allow us to study species recognition in a different context: recognition of conspecific tutors for learning.…”

Predator experience overrides learned aversion to heterospecifics in stickleback species pairs

“…These species are currently sympatric and learning contributes to strong female preference for conspecific over heterospecific mates [41][42][43]. Benthic and limnetic threespine sticklebacks (Gasterosteus spp.)…”

“…Although they are not formally named species, they are recognized as different species because they are strongly reproductively isolated (total reproductive isolation ¼ 0.87) [51]. Sexual isolation between benthics and limnetics is the most important contributor to reproductive isolation and females avoid heterospecific mates using cues such as male size, nuptial colour, shape and odour [41,42,[48][49][50][51][52][53][54]. Selection against hybrids and reinforcement in sympatry have also contributed to the strength of sexual isolation [48,[55][56][57][58].…”