Sexual selection for genetic compatibility: the role of the major histocompatibility complex on cryptic female choice in Chinook salmon (Oncorhynchus tshawytscha)

Abstract

Cryptic female choice (CFC), a form of sexual selection during or post mating, describes processes of differential sperm utilization by females to bias fertilization outcomes towards certain males. In Chinook salmon (Oncorhynchus tshawytscha) the ovarian fluid surrounding the ova of a given female differently enhances the sperm velocity of males. Sperm velocity is a key ejaculate trait that determines fertilization success in externally fertilizing fishes, thus the differential effect on sperm velocity might bias male fertilization outcomes and represent a mechanism of CFC. Once sperm reach the oocyte, CFC could potentially be further facilitated by sperm-egg interactions, which are well understood in externally fertilizing marine invertebrates. Here, we explored the potential genetic basis of both possible mechanisms of CFC by examining whether the genotypic combinations of mates (amino-acid divergence, number of shared alleles) at the major histocompatibility complex (MHC) class I and II explain the variation in sperm velocity and/or male fertilization success that is not explained by sperm velocity, which might indicate MHC-based sperm-egg interactions. We recorded sperm velocity in ovarian fluid, employed paired-male fertilization trials and evaluated the fertilization success of each male using microsatellite-based paternity assignment. We showed that relative sperm velocity was positively correlated with fertilization success, confirming that the differential effect on sperm velocity may be a mechanism of CFC in Chinook salmon. The variation in sperm velocity was independent of MHC class I and II. However, the MHC class II divergence of mates explained fertilization success, indicating that this locus might influence sperm-egg interactions.

Cryptic haplotype-specific gamete selection yields offspring with optimal MHC immune genes

“…Similar observations of a postcopulatory fertilization advantage for MHC‐similar mates were also made in Chinook salmon (Geßner et al. ), guppies (Gasparini et al. ), salamanders (Bos et al.…”

Sperm competition, but not major histocompatibility divergence, drives differential fertilization success between alternative reproductive tactics in Chinook salmon

“…We found no significant effect of female identity on competitive fertilization success; however, we did find a significant female × sire–pair interaction effect indicating evidence of cryptic female choice (CFC). In salmonids, CFC may be mediated by the egg and/or ovarian fluid characteristics (Lahnsteiner, ; Rosengrave et al ., , ; Yeates et al ., , ; Butts et al ., , ; Gessner et al ., , ). Although ovarian fluid can influence the outcome of sperm competition between jack and hooknose males (see Butts et al ., ; Lehnert et al ., ), ovarian fluid was removed from the eggs in our study and therefore evidence of CFC may only be explained by egg–sperm interactions.…”

“…Promerová et al . () found no evidence of nonrandom gamete fusion or allele transmission distortion suggesting that if CFC for MH II is occurring in salmon (as found only by Gessner et al ., to date), it is likely acting on diploid genotypes rather than at the allelic level.…”

Mitonuclear Mate Choice: A Missing Component of Sexual Selection Theory?

“…Once an individual has correctly targeted prospective mates within the population of individuals with species‐typical coadapted mt and N‐mt genes, it will still be faced with variation in the quality of prospective mates (Figure ). There is an expansive literature on the aspects of individual quality that might be assessed among males within a population, including resources, N genes that have higher fitness, and N genes that are compatible with the choosing individual's N genes . Here I propose that assessment of mitochondrial function will be a key part of assessment of individuals within a population because efficiency of respiratory function is such a key component of individual.…”

“…There is an expansive literature on the aspects of individual quality that might be assessed among males within a population, including resources, N genes that have higher fitness, and N genes that are compatible with the choosing individual's N genes. [69][70][71] Here I propose that assessment of mitochondrial function will be a key part of assessment of individuals within a population because efficiency of respiratory function is such a key component of individual. [72] Poor function of cellular respiratory systems can be a product of genotype (including mt or N genes), environment, or the interaction of genotype and environment.…”