Extended longevity of reproductives appears to be common in Fukomys mole-rats (Rodentia, Bathyergidae)

Abstract

African mole-rats (Bathyergidae, Rodentia) contain several social, cooperatively breeding species with low extrinsic mortality and unusually high longevity. All social bathyergids live in multigenerational families where reproduction is skewed towards a few breeding individuals. Most of their offspring remain as reproductively inactive "helpers" in their natal families, often for several years. This "reproductive subdivision" of mole-rat societies might be of interest for ageing research, as in at least one social bathyergid (Ansell's mole-rats Fukomys anselli), breeders have been shown to age significantly slower than non-breeders. These animals thus provide excellent conditions for studying the epigenetics of senescence by comparing divergent longevities within the same genotypes without the inescapable short-comings of inter-species comparisons. It has been claimed that many if not all social mole-rat species may have evolved similar ageing patterns, too. However, this remains unclear on account of the scarcity of reliable datasets on the subject. We therefore analyzed a 20-year breeding record of Giant mole-rats Fukomys mechowii, another social bathyergid species. We found that breeders indeed lived significantly longer than helpers (ca. 1.5-2.2fold depending on the sex), irrespective of social rank or other potentially confounding factors. Considering the phylogenetic positions of F. mechowii and F. anselli and unpublished data on a third Fukomys-species (F. damarensis) showing essentially the same pattern, it seems probable that the reversal of the classic trade-off between somatic maintenance and sexual reproduction is characteristic of the whole genus and hence of the vast majority of social mole-rats.

Figure 1. Phylogeny of the genus Fukomys.

Combined phylogeny based on TTR Intron I, 12sRNA and cyt b sequences; adopted from and .

Figure 2. Survival curves of breeding and non-breeding Fukomys mechowii.

Breeders lived significantly longer than non-breeders (log rank test, df = 1, χ² = 15.49, P<0.001). There was no difference between males and females in either reproductive group (breeders ♀♀ vs. ♂♂ df = 1, χ² = 0.21, P = 0.65; non-breeders ♀♀ vs. ♂♂ df = 1, χ² = 0.01, P = 0.92).

Figure 3. Breeding status determines the pace of aging in Fukomys mechowii.

Left: An unusually old (∼9y) non-reproductive Giant mole-rat, showing obvious signs of senescence. Right: his mother (>15y), a breeding individual since 1996. Photos were taken at the same day (M. Schmitt).

Figure 4. Survival of non-breeders growing up in different social environments.

Sexes combined. Survival probabilities did not differ between dominant (early-born) and subdominant (late-born) non-breeders (log rank test, df = 1, χ² = 0.05, P = 0.82).

Figure 5. Activity data based on 72 h-observations.

Box plots showing the time budgets allocated to locomotion, food intake and resting. All behaviours are expressed as % of time spent per 72 h-observation. Group sizes were n = 6 for each breeder group and n = 12 for each non-breeder group, respectively. Colour codes (from left to right for each behaviour): white = female breeders, light grey = male breeders, dark grey = female non-breeders, black = male non-breeders. Boxes represent the interquartile range, bars within boxes are median values and whiskers indicate the 5th and 95th percentile. Significant differences denoted by asterisks.