Abstract
In house mice, genetic compatibility is influenced by the t haplotype, a driving selfish genetic element with a recessive lethal allele, imposing fundamental costs on mate choice decisions. Here, we evaluate the cost of genetic incompatibility and its implication for mate choice in a wild house mice population. In laboratory reared mice, we detected no fertility (number of embryos) or fecundity (ability to conceive) costs of the t, and yet we found a high cost of genetic incompatibility: heterozygote crosses produced 40% smaller birth litter sizes because of prenatal mortality. Surprisingly, transmission of t in crosses using +/t males was influenced by female genotype, consistent with postcopulatory female choice for + sperm in +/t females. Analysis of paternity patterns in a wild population of house mice showed that +/t females were more likely than +/+ females to have offspring sired by +/+ males, and unlike +/+ females, paternity of their offspring was not influenced by +/t male frequency, further supporting mate choice for genetic compatibility. As the major histocompatibility complex (MHC) is physically linked to the t, we investigated whether females could potentially use variation at the MHC to identify male genotype at the sperm or individual level. A unique MHC haplotype is linked to the t haplotype. This MHC haplotype could allow the recognition of t and enable pre- and postcopulatory mate choice for genetic compatibility. Alternatively, the MHC itself could be the target of mate choice for genetic compatibility. We predict that mate choice for genetic compatibility will be difficult to find in many systems, as only weak fertilization biases were found despite an exceptionally high cost of genetic incompatibility.
Highlights
The question of why females choose mates in the absence of any direct benefits, such as access to resources, protection from harassment and predators, or provision of parental care, is still not resolved
We detected no fertility or fecundity costs of the t, and yet we found a high cost of genetic incompatibility: heterozygote crosses produced 40% smaller birth litter sizes because of prenatal mortality
Analysis of paternity patterns in a wild population of house mice showed that +/t females were more likely than +/+ females to have offspring sired by +/+ males, and unlike +/+ females, paternity of their offspring was not influenced by +/t male frequency, further supporting mate choice for genetic compatibility
Summary
The question of why females choose mates in the absence of any direct benefits, such as access to resources, protection from harassment and predators, or provision of parental care, is still not resolved. Much theoretical and empirical research has addressed the “good genes” hypothesis of mate choice, where females base mate choice on the quality of genes that their offspring would inherit through the sire (indirect benefits) (Andersson and Simmons 2006). Under the “compatible genes” hypothesis, a female bases mate choice decisions on the potential interaction between the genes inherited through herself and her mate. Genetic compatibility has the potential to influence offspring quality as much as beneficial genes of the sire, and may strongly influence mate choice evolution (Neff and Pitcher 2005; Puurtinen et al 2009).
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