Sisters' curse: sexually antagonistic effects constrain the spread of a mitochondrial haplogroup superior in sperm competition

Abstract

Maternal inheritance of mitochondria creates a sex-specific selective sieve with implications for male longevity, disease susceptibility and infertility. Because males are an evolutionary dead end for mitochondria, mitochondrial mutations that are harmful or beneficial to males but not females cannot respond directly to selection. Although the importance of this male/female asymmetry in evolutionary response depends on the extent to which mitochondrial mutations exert antagonistic effects on male and female fitness, few studies have documented sex-specific selection acting on mitochondria. Here, we exploited the discovery of two highly divergent mitochondrial haplogroups (A and B2) in central Panamanian populations of the pseudoscorpion Cordylochernes scorpioides. Next-generation sequencing and phylogenetic analyses suggest that selection on the ND4 and ND4L mitochondrial genes may partially explain sexually antagonistic mitochondrial effects on reproduction. Males carrying the rare B2 mitochondrial haplogroup enjoy a marked advantage in sperm competition, but B2 females are significantly less sexually receptive at second mating than A females. This reduced propensity for polyandry is likely to significantly reduce female lifetime reproductive success, thereby limiting the spread of the male beneficial B2 haplogroup. Our findings suggest that maternal inheritance of mitochondria and sexually antagonistic selection can constrain male adaptation and sexual selection in nature.

Sperm competitive advantage of a rare mitochondrial haplogroup linked to differential expression of mitochondrial oxidative phosphorylation genes

“…In the study reported here in which B2‐haplogroup females were each mated to both an A and a B2 male, DNA profiling demonstrated that B2‐haplogroup males sired more than three times as many offspring than A males. In conjunction with the results of an earlier sperm competition experiment involving only A haplogroup females (Padua et al., ), our research on C. scorpioides indicates that the B2 sperm competitive advantage is independent of female haplogroup. This intrinsic B2 advantage cannot be attributed to differences in nuclear genetic background.…”

“…Despite the strong B2 advantage in sperm competition, the B2 haplotype occurs at low frequency (12%) in central Panamanian populations of C. scorpioides (Zeh et al., ). The rarity of B2 appears to be the consequence of sister's curse, that is, the haplogroup's antagonistic effects on female fitness (Padua et al., ). While essentially all C. scorpioides virgin females are sexually receptive, sexual receptivity at second mating has been shown to be significantly lower in females carrying B2 haplogroup mitochondria (Padua et al., ).…”

“…The rarity of B2 appears to be the consequence of sister's curse, that is, the haplogroup's antagonistic effects on female fitness (Padua et al., ). While essentially all C. scorpioides virgin females are sexually receptive, sexual receptivity at second mating has been shown to be significantly lower in females carrying B2 haplogroup mitochondria (Padua et al., ). Given the evidence for substantial fitness benefits to polyandry in this pseudoscorpion (Newcomer et al., ), the reduced propensity for polyandry by B2 haplogroup females is likely to incur significant costs to female lifetime reproductive success.…”

“…It is important to acknowledge that our study has not definitively established that haplogroup differences in sperm competitive ability result from differences in levels of OXPHOS gene expression. Haplogroup differences could be due to functionally significant DNA sequence differences in just one or multiple OXPHOS genes (Padua et al., ). Nonetheless, the extreme, 22‐fold overexpression of atp8 in the testes of B2 males is consistent with this gene playing an important role in the B2 advantage.…”

Maternal transmission, sex ratio distortion, and mitochondria

“…A number of studies have begun to examine functional differences between mitochondrial variants, with consequences on host fitness. For example, a recent study in the neotropical pseudoscorpion Cordylochernes scorpioides found that trade-offs explained the persistence of two divergent mitochondrial genomes; although males carrying one of these genomes had higher sperm competitive ability, females with this mitochondrial genome had reduced sexual receptivity (70). In warblers, hybridization has resulted in the introgression of a mitochondrial variant that is associated with differences in flight efficiency and migratory potential (71).…”