Sexual imprinting overrides order effects

Abstract

Mate choice is a complex decision that requires the integration of cues from potential mates with individual preferences. Choosers' preferences are shaped by recent events, early life experience and by the evolutionary history of its own species. To better understand the interaction between these factors, we studied mate choice in the female house mouse, Mus musculus. Females of one of the musculus subspecies, Mus musculus musculus, show preference for males of their own subspecies compared to males of the sibling subspecies, Mus musculus domesticus. Such an assortative preference is ecologically relevant at contact zones, where it contributes to the reproductive isolation of sympatric populations and can be reproduced in controlled laboratory conditions, but its origins are still under debate. Here, we show that female mouse mate choice depends on both early postnatal life experience and the order of prospective mates encountered as an adult and that these effects interact asymmetrically. Whereas females raised in their normal M. m. musculus environment display a robust assortative preference, females fostered in a M. m. domesticus family prefer the first male encountered, regardless of subspecies. Thus, early life experience of M. m. musculus females, when concordant with genetic self-identity, overrides sampling order effects, ensuring robust assortative choice. In the absence of this match between phylogeny and early life experience, first impression effects dominate mate choice. Assortative mate choice is one of the mechanisms underlying the reproductive isolation between the two subspecies of house mouse, M. m. musculus and M. m. domesticus. These two lineages diverged from a common Asian ancestor which followed different human migratory routes and have subsequently established a secondary contact zone in central Europe [1], where they exhibit asymmetric mate preference: M. m. musculus females prefer their own subspecies, whereas M. m. domesticus females mate indiscriminately with both [2]. Using inbred strains of wild-derived mice as representatives of the M. m. musculus subspecies and laboratory mice as representatives of M. m. domesticus, the preference of M. m. musculus females can be studied under laboratory conditions,