Mitonuclear interactions alter sex-specific longevity in a species without sex chromosomes

Abstract

Impaired mitochondrial function can lead to senescence and the ageing phenotype. Theory predicts degenerative ageing phenotypes and mitochondrial pathologies may occur more frequently in males due to the matrilineal inheritance pattern of mitochondrial DNA observed in most eukaryotes. Here, we estimated the sex-specific longevity for parental and reciprocal F1 hybrid crosses for inbred lines derived from two allopatric Tigriopus californicus populations with over 20% mitochondrial DNA divergence. T. californicus lacks sex chromosomes allowing for more direct testing of mitochondrial function in sex-specific ageing. To better understand the ageing mechanism, we estimated two age-related phenotypes (mtDNA content and 8-hydroxy-20-deoxyguanosine (8-OH-dG) DNA damage) at two time points in the lifespan. Sex differences in lifespan depended on the mitochondrial and nuclear backgrounds, including differences between reciprocal F1 crosses which have different mitochondrial haplotypes on a 50 : 50 nuclear background, with nuclear contributions coming from alternative parents. Young females showed the highest mtDNA content which decreased with age, while DNA damage in males increased with age and exceed that of females 56 days after hatching. The adult sex ratio was male-biased and was attributed to complex mitonuclear interactions. Results thus demonstrate that sex differences in ageing depend on mitonuclear interactions in the absence of sex chromosomes.

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

“…Sex-specific life span differs between the four crosses, Abbreviations: FF, F female mated with F male; FS, F female mated with S male; SF, S female mated with F male; SS, S female mated with S male. a Data for benign conditions are from Flanagan et al, 2021. b Maximum life span is a family-based calculation and estimated from all families within each cross.…”

“…The culture medium was the same as the original population cultures. This experiment used the fourth clutch of the crosses generated in Flanagan et al, 2021 for direct comparisons with the survival and longevity under benign conditions. Briefly, males were removed to avoid further harassment after the females were released from the pair.…”

“…Petri dishes were checked every day until the fertilized egg sacs hatched. The offspring from the first three egg clutches were collected and assayed under benign conditions (Flanagan et al, 2021), while the offspring from the fourth clutch were then counted and transferred to a new petri dish for this study. The estimated effect of clutch number on survival was minimal during the previous experiment for the first three clutches under benign conditions (coxph, z = −1.94, p = .052) (Flanagan et al, 2021).…”

“…Given that mitochondria are the location where dietary nutrients are converted to ATP, mitochondrial effects might be expected to highly dependent on nutritional environment. In this study, we use an additional clutch of offspring from the same families assayed in Flanagan et al (2021), raising animals under benign conditions until adulthood, and then transferring them to culture medium without food. In this way, we test how nutritional stress impacts sex differences in longevity, including the role of mitochondrial effects.…”

“…In this study, we use an additional clutch of offspring from the same families assayed in Flanagan et al (2021), raising animals under benign conditions until adulthood, and then transferring them to culture medium without food. In this way, we test how nutritional stress impacts sex differences in longevity, including the role of mitochondrial effects.…”