Food deprivation exposes sex‐specific trade‐offs between stress tolerance and life span in the copepod Tigriopus californicus

Abstract

A long-standing dogma in biology is that the ability to withstand stress is associated with longer life (Kirkwood & Austad, 2000). This is supported by overlap in the genetic bases for these two traits, including the roles of molecular chaperones, antioxidants, and genes involved in repair of oxidative damage (Landis et al., 2004;Vermeulen & Loeschcke, 2007). More direct evidence comes from artificial selection experiments, in which selection for longer life span increases resistance to stressors such as starvation, desiccation, ethanol, and high temperature (Scannapieco et al., 2009;Service et al., 1985), and selection for increased stress resistance (desiccation, starvation, and high temperature) also increases longevity (

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

“…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.…”

“…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, 2019, 2020, 2022; Flanagan et al, 2021, 2022; Watson 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 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]).…”

“…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.…”