Mate choice driven by genome in an allopolyploid fish complex

Nonsexual complexes which lack typical reproductive isolation and show multiple conspecific and heterospecific mating options among hybrids and parental species are excellent models to study mate choice based on genetics. The allopolyploid fish complex Squalius alburnoides includes multiple fertile male and female genomotypes reproducing among each other and with the sympatric species of the Squalius genus. We used this hybridogenetic complex to study the relationship between mate preference and mates' genetic background, focusing on a population whose mating options include 2 Squalius species. The preference of S. alburnoides hybrid females towards multiple male genomotypes was assessed in affiliation trials, and the levels of admixture between the genomes of the 2 Squalius species were measured using next-generation genotyping. The genome of the most recent Squalius species in the drainage was admixed with variable genetic portions typically allocated to the other species, but not the opposite, suggesting that the newer species in the drainage may be more prone to interspecific crosses. Female mate preferences were related to males' genetic background, but also to the genetic background of the choosy female itself. Overall, females showed higher preference towards males with admixed genomes over pure males, and towards males with a genetic background more similar to their own. This trend favors crosses between the hybrids and the most recent Squalius species in the drainage, promoting the flow of its genome into the hybridogenetic complex. These findings highlight an intricate interplay between mate choice and mates' genomes, which may be directly related to genetic benefits.