Mate choice in the brain: Species differ in how male traits ‘turn on’ gene expression in female brains

Mate choice plays a fundamental role in speciation, yet we know little
about the molecular mechanisms that underpin this crucial decision-making
process. Stickleback fish differentially adapted to limnetic and benthic
habitats are reproductively isolated and females of each species use
different male traits to evaluate prospective partners and reject
heterospecific males. Here, we integrate behavioral data from a mate
choice experiment with gene expression profiles from the brains of females
actively deciding whether to mate. We find substantial gene expression
variation between limnetic and benthic females, regardless of behavioral
context, suggesting general divergence in constitutive gene expression
patterns, corresponding to their genetic differentiation. Intriguingly,
female gene co-expression modules covary with male display traits but in
opposing directions for sympatric populations of the two species,
suggesting male displays elicit a dynamic genomic response that reflects
known differences in female preferences. Furthermore, we confirm the role
of numerous candidate genes previously implicated in female mate choice in
other species, suggesting that evolutionary tinkering with these conserved
molecular processes underlies divergent mate preferences and sexual
isolation. Taken together, our study adds important new insights to our
understanding of the molecular processes underlying female decision-making
critical for generating sexual isolation and speciation.