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:Gasterosteusspp.). 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.

Sexual isolation between species often depends on preferences for conspecific mates. Recent models suggest that whether conspecific preference is determined genetically or learned will affect the process of speciation: Learned conspecific preferences might make speciation more likely. However, we understand little about how often and for which taxa, conspecific preferences are learned. Some species learn conspecific preference by imprinting on conspecifics; others learn from experience with heterospecifics. Even when one sex learns conspecific preference, the other may not. We tested whether conspecific mate preference is learned through social experience in males and females from 2 three-spined stickleback species that show strong sexual isolation (benthics and limnetics: Gasterosteus spp.). We reared fish with either mostly conspecifics or mostly heterospecifics and measured how this experience affected conspecific preference. In both sexes, experience enhanced conspecific mate preference but the sexes differed in the outcome. Females learned to prefer their own species through experience with conspecifics; males learned to discriminate through experience with heterospecifics. We also found species differences in the effect of social experience related to differences in sociality. Our results suggest that learned conspecific mate preference may have facilitated rapid speciation in the post Pleistocene radiation of sticklebacks.