Genomic compatibility excels possible 'good genes' effects of sexual selection in lake char

Abstract

Mating is rarely random in nature, but the effects of mate choice on offspring performance are still poorly understood. We sampled in total 47 wild lake char (Salvelinus umbla) during two breeding seasons and used their gametes to investigate the genetic consequences of different mating scenarios. In a first study, 1,464 embryos that resulted from sperm competition trials were raised singly in either a stress- or non-stress environment. Offspring growth turned out to be strongly reduced with increased genetic relatedness between the parents while male coloration (that reveal aspects of male health) was no significant predictor of offspring performance. In a second experiment one year later, block-wise full-factorial in vitro breeding was used to produce 3,094 embryos that were raised singly after sublethal exposures to a pathogen or water only. Offspring growth was again strongly reduced with increased genetic relatedness between the parents while male coloration was no significant predictor of offspring performance. We conclude that the genetic benefits of mate choice would be strongest if females avoided genetic similarity, while male breeding colors seem more relevant in intra-sexual selection. Impact SummaryMales and females usually compete for access to mating partners, and they usually choose their mates. Sexual selection is therefore a major force in evolution. It shapes sexual signals and mate preferences depending on the type of mating system. A comparatively simple mating system is when fertilization is external and neither males nor females care for their brood, as is the case in salmonid fish. A group of hypotheses then predicts that female mate preferences have evolved to maximize offspring growth and survival through indirect genetic benefits. There are two types of such indirect benefits. In models of good genes sexual selection, conspicuous signals reveal a males health and vigor because only males in good health can afford these costly traits. Females would then prefer males with strong signals. In compatible genes models, females would instead focus on signals that allow them to complement their own genotype to achieve high offspring viability. An example of the latter is inbreeding avoidance through odors that reveal kinship. We sampled wild lake char to compare the likely consequences of these two types of possible female preferences for offspring growth and survival. We experimentally crossed these fish in vitro and raised large numbers of offspring singly and for several months. Our first experiment revealed that offspring growth would be significantly increased if females would avoid mating with genetically more similar males, while preferring males with strong sexual ornaments (in this case: yellow skin colors) would not improve offspring performance. These results could be confirmed in a second experiment with a larger sample size. We conclude that the genetic benefit of mate choice is largest if females aim for compatible genes rather than focusing on the breeding colors that males display. These breeding colors are therefore likely to play a more important role in other contexts, e.g., in male-male competition.