Life expectancy, family constellation and stress in giant mole-rats ( Fukomys mechowii )

Abstract

Giant mole-rats ( Fukomys mechowii ) are remarkably long-lived subterranean rodents (maximum recorded lifespan as reported here greater than 26 years) that live in families with one reproductive pair (breeders) and their non-reproductive offspring (non-breeders). Previous studies have shown that breeders live on average approximately twice as long as non-breeders, a finding contradicting the classic trade-off between reproduction and lifespan. Because recent evidence points to the hypothalamic-pituitary-adrenal axis as playing an important role in shaping the pace of ageing in mole-rats, we analysed the influence of the social environment of giant mole-rats on intrafamilial aggression levels, indicators of long-term stress, and, ultimately, mortality. Behavioural data indicated that family constellation, especially the presence or the absence of parents, influences agonistic behaviour. As a measure of long-term stress, we established a non-invasive method of extracting and measuring cortisol from hair of giant mole-rats. Interestingly, orphaned non-breeders exhibited significantly lower levels of cortisol and lower mortality rates than did non-breeders living with both parents. Because hypercortisolism is harmful in the long-term, intrafamilial stress could help explain the earlier onset of senescence in non-breeders, resulting in a shorter lifespan. Our findings suggest that the social environment should be considered as a further factor in ageing studies involving group-living animals. This article is part of the theme issue ‘Ageing and sociality: why, when and how does sociality change ageing patterns?’

Ageing and sociality: why, when and how does sociality change ageing patterns?

“…A role for peroxiredoxins also became evident in several other transcriptome studies in this volume [30,32,33]. Furthermore, Quigley & Amdam [49] also stress the importance of social interactions in modulating senescence in humans, similar to what has been shown in social insects and social rodents [33,40,43,46,47].…”

Effects of Sex and Breeding Status on Skull Morphology in Cooperatively Breeding Ansell’s Mole-Rats and an Appraisal of Sexual Dimorphism in the Bathyergidae

“…However, current evidence suggests that Fukomys indeed exhibits strict social and predominant sexual monogamy, the latter fluctuating in frequency between populations (Burland et al, 2002;Patzenhauerová et al, 2013). While staying faithful to their current mate for prolonged periods (Bappert et al, 2012;Begall et al, 2021), Fukomys may experience serial changes in partners over their lifetime (Burland et al, 2002;Šumbera et al, 2012;Patzenhauerová et al, 2013). Different mating systems are expressed in the other two social bathyergid genera.…”

Increased longevity due to sexual activity in mole-rats is associated with transcriptional changes in the HPA stress axis

“…Altered MC2R expression ( Fig. 6A) coincides with higher cortisol levels in hair samples from non-breeding F. mechowii than in those from breeders of the same species (Begall et al 2020). Furthermore, glucocorticoids such as cortisol exert their effect by binding to the glucocorticoid receptor that, in turn, acts as a transcription factor for many genes (Gjerstad et al 2018).…”

“…Nevertheless, a recent study confirmed one of the most important predictions of the hypothesis: hair cortisol levels of non-breeders are on average about twice as high as those of breeders. However, a subgroup of non-breeders, defined by social environmental factor (one or both parents had died), exhibited cortisol levels nearly as low as in breeders (Begall et al 2020). The drop of cortisol levels in orphaned non-breeders is accompanied by a substantial drop of mortality rates in this subgroup approaching the values of breeders ( Figure 6-figure supplement 1).…”

“…To calculate status-specific mortality rates across age-classes, we subdivided the first 10 years of observation time (corresponding to 1.5 -11.5 years of calendar age) into intervals of six months. We then recapitulated the times each individual spent as conventional non-breeder (both parents present; cortisol levels high, see (Begall et al 2020)), orphaned non-breeder (at least one parent absent since more than 6 month; cortisol levels low, see (Begall et al 2020)) or breeder (cortisol levels low, see (Begall et al 2020)), and calculated status-specific annual mortality rates for each interval by dividing the number of death events of the respective status during a given interval by the sum of observation years for all individuals holding this status in the same interval. In each interval, individuals that were alive across the entire interval contributed 0.5 years observation time, whereas individuals who died or were censored during that interval contributed the time (expressed in years) up to the death or censorship event.…”