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 Considering the phylogenetic positions of F. mechowii and F. anselli and unpublished data on a third Fukomys-species (F. damarensis) showing essentially the same pattern, it seems probable that the reversal of the classic trade-off between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.

Highlights

  • Sexual reproduction is costly and often traded off against somatic maintenance and longevity [1], [2]

  • A few years ago, the same pattern was revealed for the first time in a mammal, namely the highly social Ansell’s mole-rat Fukomys anselli: breeders of both sexes lived on average roughly twice as long as nonbreeders and reached remarkable maximum lifespans of .20 years [5]

  • It is not known whether the pattern found in F. anselli is observed in other social mole-rats, and if so, how great the effect is

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Summary

Introduction

Sexual reproduction is costly and often traded off against somatic maintenance and longevity [1], [2]. Three of them exhibit high degrees of sociality and reproductive skew: they live in multigenerational families in which only few individuals (often just a single founder pair) reproduce. It has been speculated that ‘‘the social molerats [in general], like some eusocial insects [...], have evolved mechanisms that defer senescence in breeding females’’ [6] This is an important claim, since if true, there would be ample opportunities to study the proximate mechanisms (e.g. endocrinology, gene expression patterns, epigenetics etc.) triggering divergent ageing rates within the same genotypes without the inevitable limitations of inter-specific comparisons, e.g. between fast and slow-ageing species. Lifespan .30y [9]), the question of potential intraspecific, status-dependent differences in ageing rates has not been seriously addressed in this species to date It is not known whether the pattern found in F. anselli is observed in other social mole-rats (or cooperatively breeding vertebrates from other taxa), and if so, how great the effect is. Social structure, and reproductive biology appear to match those of F. anselli and other Fukomys-species studied far [10]–[16]

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