Mate choice for genetic compatibility in the house mouse

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.

Keywords: Cryptic female choice; meiotic drive; segregation distortion; selection arena hypothesis; sexual selection; sperm selection; t-complex.

Figure 1

Picture of house mice in the free-living study population (by Sabine Wunderlin).

Figure 2

Schematic map of + and t haplotype forms of mouse chromosome 17. Shaded boxes represent the t-associated inversions. The MHC markers genotyped here are indicated. The Hba-ps4 marker was used for t-haplotype identification.

Figure 3

Number of uterine scars ± 95% CI per mating cross. Red scars indicate live births and yellow scars prenatal mortality.

Figure 4

Drive estimates ± 95% CI for each mating cross. The expected value (asterisk) for crosses of +/t males and +/t females lies outside the observed value. The dashed line indicates the Mendelian expectation of 0.5.

Figure 5

Proportion of +/t adult males and females according to litter birth date. The dashed line indicates a 1:1 proportion of +/t to +/+.

Figure 6

Incidence function of paternity by a +/t male relative to the proportion of +/t males among potential sires and to female genotype, with 95% confidence intervals. The gray line indicates a 1:1 relationship.

Figure 7

Amino acid sequence of MHC class II genes aligned: (A) Aα and (B) Eβ. Asterisks indicate sites involved in antigen binding identified from Brown et al. (1993) and Reche and Reinherz (2003); p = residues in proximity to the antigen but likely do not contribute to the specificity and binding properties of the molecule, f = residues interacting with flanking regions of the peptide core extending beyond the binding groove (Reche and Reinherz 2003).