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

Abstract

Mate choice plays a fundamental role in speciation, yet we know little about the molecular mechanisms that underpin this crucial decision-making process. Female stickleback fish differentially adapted to limnetic and benthic habitats and considered members of reproductively isolated species use different male traits to evaluate prospective partners and reject heterospecific males. Here, we integrate behavioral data from a mate choice experiment involving benthic and limnetic fish with gene expression data from the brains of females making these mate choice decisions. We find substantial gene expression variation between limnetic and benthic species, regardless of behavioral context, suggesting general divergence in gene expression patterns in female brains, in accordance with 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 genomic response that reflects known differences in female preferences which serve to isolate the species. Furthermore, our analysis confirms the role of numerous candidate genes previously implicated in female mate choice decision-making in other teleost species, suggesting that these cognitive molecular processes are, in part, evolutionarily conserved. Taken together, our study adds important new insights to our understanding of the molecular processes underlying female decision-making that maintain isolation between diverging species.