Unraveling mate choice evolution through indirect genetic effects

Attractiveness is not solely determined by a single sexual trait but rather by a combination of traits. Because the response of the chooser is based on the combination of sexual traits in the courter, variation in the chooser's responses that are attributable to the opposite-sex courter genotypes (i.e., the indirect genetic effects [IGEs] on chooser response) can reflect genetic variation in overall attractiveness. This genetic variation can be associated with the genetic basis of other traits in both the chooser and the courter. Investigating this complex genetic architecture, including IGEs, can enhance our understanding of the evolution of mate choice. In the present study on the field cricket Gryllus bimaculatus, we estimated (1) genetic variation in overall attractiveness and (2) genetic correlations between overall attractiveness and other pre- and postcopulatory traits (e.g., male latency to sing, female latency to mount, male guarding intensity, male and female body mass, male mandible size, and testis size) within and between sexes. We revealed a genetic basis for attractiveness in both males and females. Furthermore, a genetic variance associated with female attractiveness was correlated with a genetic variance underlying larger male testes. Our findings imply that males that mate with attractive females can produce offspring that are successful in terms of precopulatory sexual selection (daughters who are attractive) and postcopulatory sexual selection (sons with an advantage in sperm competition), potentially leading to runaway sexual selection. Our study exemplifies how the incorporation of the IGE framework provides novel insights into the evolution of mate choice. The attractiveness of an individual is not determined by just one trait but rather by a combination of traits. When an individual chooses a mate, the decision is based on the combination of traits in the individual of the opposite sex. Thus, if the chooser's reactions depend on the genotype of the courter, it indicates that there is genetic variation in the overall attractiveness of the courting sex. Applying this perspective in our study on field crickets, we found genetic variation in the overall attractiveness of males and females. We further explored whether overall attractiveness was genetically correlated with other traits within a sex or across sexes. We found that a genetic variance that made females more attractive was correlated with a genetic variance increasing male testes size. This suggests that when males mate with attractive females, their daughters are more likely to be chosen as mates themselves and their sons more able to monopolize egg fertilization. This could potentially lead to a positive feedback where attractiveness and the preference for attractiveness reinforce each other. Our study illustrates the utility of calculating the overall attractiveness of the courting individual and its genetic variance based on the choosers' responses to understand the mechanisms underpinning mate choice and its evolution.