Mitochondrial effects on fertility and longevity in Tigriopus californicus contradict predictions of the mother’s curse hypothesis

Abstract

SUMMARYStrict maternal inheritance of mitochondria favors the evolutionary accumulation of sex-biased fitness effects, as mitochondrial evolution occurs exclusively in female lineages. The “mother’s curse” hypothesis proposes that male-harming mutations should accumulate in mitochondrial genomes when they have neutral or beneficial effects on female fitness. Rigorous empirical tests have largely focused on Drosophila, where support for the predictions of mother’s curse has been mixed. We investigated the impact of mother’s curse mutations in Tigriopus californicus, a minute crustacean. Using nonrecombinant backcrosses, we introgressed four divergent mitochondrial haplotypes into two nuclear backgrounds and recorded measures of fertility and longevity. We found that the phenotypic effects of mitochondrial mutations were context-dependent, being influenced by the nuclear-background in which they were expressed, as well as the sex of the individual and rearing temperature. Mitochondrial haplotype effects were greater for fertility than longevity, and temperature effects were greater for longevity. However, in opposition to mother’s curse expectations, females had a higher level of mitochondrial genetic variance than males for both fertility and longevity, and there was no evidence for mitochondrial mutations favoring female performance at the cost of male performance. These results indicate that selection has not resulted in the accumulation of male mutation load in Tigriopus californicus.

Developmental rate displays effects of inheritance but not of sex in inter-population hybrids ofTigriopus californicus

“…For instance, Li et al (2022) found that females had longer lifespans than males in F1 inter-population hybrids, and Foley et al (2013) showed that differences in nuclear allele frequencies between reciprocal F 2 hybrids (i.e., between alternate mitochondrial genotypes) were sex-dependent, particularly for chromosome 10. However, observed sex-specific effects in hybrid T. californicus are not consistently aligned with the expectations of the ‘mother’s curse’ hypothesis (e.g., Watson et al, 2022), and although previous results have indicated that variation in developmental rate is generally highly dependent on mitonuclear compatibility in T. californicus hybrids (Healy & Burton, 2020; Han & Barreto, 2021), variation in this trait between the sexes was virtually absent at any stage of development in the current study (consistent with the less detailed results of Burton [1990]). Similarly, variation in mitonuclear effects on developmental time between females and males is generally modest or absent in Drosophila sp.…”

“…Alternatively, following from the expectations of a ‘mother’s curse’, decreased reliance on complex I respiration in males could partially negate the possibility of strong effects of mitonuclear incompatibilities on complex I function in this sex. In either case, variation in the proportional contributions of complex I and II respiration between females and males may contribute to the sex-specific effects of incompatibilities on viability, lifespan or longevity reported elsewhere (Willett & Burton, 2001; Li et al, 2022; Watson et al, 2022).…”

“…This dominant role of mitonuclear interactions is particularly evident for variation in developmental rate among F 2 hybrids, and there is strong selection for compatible mitonuclear genotypes in fast-developing hybrids (Healy & Burton, 2020; Han & Barreto, 2021). Previous estimates for the times necessary to reach adulthood in inter-population T. californicus hybrids suggest developmental rate is equivalent in both sexes (Burton, 1990), which is unlike many other traits in this species (Willett & Burton, 2001; Foley et al, 2013; Flanagan et al, 2021; Li et al, 2022; Watson et al, 2022). However, the potential effects of sex throughout development are not well characterized, and the extent to which mitonuclear effects on developmental rate are inherited across hybrid generations in unknown.…”

“…Lack of variation in developmental rate between the sexes T. californicus lacks heteromorphic sex chromosomes, and has complex genetic and environmental mechanisms underlying sex determination (Alexander et al, 2015). Phenotypic differences between females and males have been well characterized for a number of traits in this species, including lifespan, viability, fertility, stress tolerances and gene expression patterns (Willett & Burton, 2001;Willett, 2010;Leong et al, 2018;Willett & Son, 2018;Foley et al, 2019;Li et al, 2019Li et al, , 2020Li et al, , 2022Flanagan et al, 2021Flanagan et al, , 2022Watson et al, 2022), and at least some of these sex-specific patterns have also been observed in inter-population hybrids. For instance, Li et al (2022) found that females had longer lifespans than males in F1 interpopulation hybrids, and Foley et al (2013) showed that differences in nuclear allele frequencies between reciprocal F2 hybrids (i.e., between alternate mitochondrial genotypes) were sexdependent, particularly for chromosome 10.…”

“…Previous estimates for the times necessary to reach adulthood in inter-population T. californicus hybrids suggest developmental rate is equivalent in both sexes (Burton, 1990), which is unlike many other traits in this species (Willett & Burton, 2001;Foley et al, 2013;Flanagan et al, 2021;Li et al, 2022;Watson et al, 2022). However, the potential effects of sex throughout development are not well characterized, and the extent to which mitonuclear effects on developmental rate are inherited across hybrid generations in unknown.…”