Female sticklebacks Gasterosteus aculeatus use self-reference to optimize MHC allele number during mate selection

Abstract

Theoretical and empirical studies suggest that an optimal resistance to pathogens and parasites requires an optimal number of MHC alleles per individual. Here we argue that three-spined sticklebacks (Gasterosteus aculeatus) achieve this goal by applying a strategy that involves a self-referential process. According to this model, females complement their own set of alleles with a more or less diverse set of male alleles such that the combined diversity reaches an optimum. In previous experiments, we have identified allele counting as a major mate-choice strategy in large populations. The self-referential allele-counting hypothesis predicts that MHC-based mate choice favors dissimilar MHC alleles in small populations facing the risk of inbreeding. Therefore, we conducted an experiment that simulated a small effective population size with low MHC class-II diversity. Our experiments are based on the analysis of MHC class-IIB alleles that explain a major part of the overall MHC diversity in sticklebacks, as determined by mathematical modeling. The results show that females preferred males with dissimilar alleles. Our present and the previous studies (which we reanalyzed with respect to our new predictions) show that irrespective of high or low population diversity faced by female sticklebacks for their mate choice, they use information about their own and their potential mate's MHC polymorphism for optimal complementation of their own set of alleles. From combining the data of the previous and the present experiment we found that female sticklebacks try to achieve an optimum number of MHC class-IIB alleles for their offspring through mate choice. The chosen MHC diversity is close to the most frequent diversity found naturally in individual fish, which in addition have the lowest parasite burden.