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• W2018283353 abstract "A trade-off between fecundity and life expectancy is fundamental to most theories on the evolution of life histories and ageing. In fact, sexual reproduction has been shown to reduce lifespan in a large number of species across all biological taxa [1Stearns S.C. The Evolution of Life Histories. Oxford University Press, Oxford1992Google Scholar]. The only exception known thus far are eusocial hymenopterans, with reproducing queens usually living much longer than the sterile workers [2Hölldobler B. Wilson E.O. The Ants. Springer Press, Berlin1990Crossref Google Scholar]. Here, we show that in a eusocial mammal, a nearly identical life history has evolved. Among mammals, eusociality has evolved only among the subterranean African mole-rats (Rodentia: Bathyergidae), namely in the naked mole-rat Heterocephalus glaber [3Jarvis J.U.M. Eu-sociality in a mammal – cooperative breeding in naked mole-rat Heterocephalus glaber colonies.Science. 1981; 212: 571-573Crossref PubMed Scopus (309) Google Scholar] and several species of the genus Cryptomys [4Burda H. Individual recognition and incest avoidance in eusocial common mole-rats rather than reproductive suppression by parents.Experientia. 1995; 51: 411-413Crossref PubMed Scopus (81) Google Scholar, 5Bennett N.C. Faulkes C.G. African Mole-Rats: Ecology and Eusociality. Cambridge University Press, Cambridge2000Google Scholar]. Eusociality in mole-rats is characterized by monopolization of reproduction by few individuals (usually a single breeding pair), monogamy of the breeding pair, long-lasting philopatry of the offspring resulting in an overlap of adult generations and cooperative brood care [3Jarvis J.U.M. Eu-sociality in a mammal – cooperative breeding in naked mole-rat Heterocephalus glaber colonies.Science. 1981; 212: 571-573Crossref PubMed Scopus (309) Google Scholar, 4Burda H. Individual recognition and incest avoidance in eusocial common mole-rats rather than reproductive suppression by parents.Experientia. 1995; 51: 411-413Crossref PubMed Scopus (81) Google Scholar, 5Bennett N.C. Faulkes C.G. African Mole-Rats: Ecology and Eusociality. Cambridge University Press, Cambridge2000Google Scholar]. Social mole-rats are known for their remarkable longevity, more than 25 years for naked mole-rats [6Sherman P.W. Jarvis J.U.M. Extraordinary life spans of naked mole-rats (Heterocephalus glaber).J. Zool. 2002; 258: 307-311Crossref Scopus (71) Google Scholar], but a thorough study comparing ageing rates of breeders and non-breeders is still lacking. Using long-term breeding data (1984–2005) of Ansell´s mole-rat Cryptomys anselli, we compared life expectancy of breeding and non-breeding animals held in captivity. Due to strict inbreeding avoidance [4Burda H. Individual recognition and incest avoidance in eusocial common mole-rats rather than reproductive suppression by parents.Experientia. 1995; 51: 411-413Crossref PubMed Scopus (81) Google Scholar], adult offspring remained reproductively quiescent unless removed from their colonies and paired to an unfamiliar mate. This held true also when one or both breeding animals died. Thus, reproductive division of labor was clear-cut in our experimental stock, allowing assignment of each individual to either the ‘breeder’ or ‘non-breeder’ group. Both male and female breeders lived approximately twice as long as non-breeders. No difference was found between the sexes in either reproductive caste. With the exception of a single female, all breeders reached an age of at least 6 years, irrespective of sex. The oldest female breeder was 14.9 years and still alive at the end of data collection. The two oldest male breeders reached ages of nearly 20 years. In contrast, in the non-breeder-group, deaths occurred at a constant rate after reaching maturity, and so far all non-breeders died before their 8th birth date (Figure 1). This pattern was not caused by intrinsic quality differences between breeders and non-breeders which might have resulted from an unintended bias towards high-class-individuals during the selection of breeders. Our pairing scheme was determined by the availability of unfamiliar mates of similar age rather than by any other factor, and neither female nor male future breeders grew faster than non-breeders in their juvenile phase (Figure 2A ). Breeders and non-breeders differ in mean social rank, raising the possibility that social rather than reproductive status causes differential ageing rates. However, in captive Cryptomys anselli colonies there is no competition for mates and barely any for food. As a consequence, aggression levels are very low, and sociopositive behaviours such as allogrooming or huddling, which are shared among all group members, prevail. It is, therefore, unlikely that non-breeders die younger because they suffer from social stress. In support of this assumption, survival probability did not differ between dominant (i.e., early-born) and subdominant (late-born) non-breeders (Figure 2B). We thus conclude that social rank does not affect the pace of ageing in this species. Rate of living can also influence life expectancy. We, therefore, quantified daily activity budgets and found no difference between breeders and non-breeders with regard to the time spent resting, feeding, or working (Figure 2C). Costs of reproduction can be masked by various factors, and positive correlations between individual fertility and longevity have been found in other studies [7Clutton-Brock T.H. Reproductive effort and terminal investment in iteroparous animals.Am. Nat. 1984; 123: 212-229Crossref Scopus (578) Google Scholar, 8Von Holst D. Hutzelmeyer H. Kaetzke P. Khaschei M. Schönheiter R. Socal rank, stress, fitness, and life expectancy in wild rabbits.Naturwissenschaften. 1999; 86: 388-393Crossref PubMed Scopus (67) Google Scholar, 9Tsuji K. Nakata K. Heinze J. Lifespan and Reproduction in a Queenless Ant.Naturwissenschaften. 1996; 83: 577-578Crossref Scopus (52) Google Scholar]. Such results have been interpreted as resulting from either variability in individual quality within the study population [7Clutton-Brock T.H. Reproductive effort and terminal investment in iteroparous animals.Am. Nat. 1984; 123: 212-229Crossref Scopus (578) Google Scholar], social stress suffered by subordinate individuals [8Von Holst D. Hutzelmeyer H. Kaetzke P. Khaschei M. Schönheiter R. Socal rank, stress, fitness, and life expectancy in wild rabbits.Naturwissenschaften. 1999; 86: 388-393Crossref PubMed Scopus (67) Google Scholar], or a more exhaustive life style of non-breeding individuals [9Tsuji K. Nakata K. Heinze J. Lifespan and Reproduction in a Queenless Ant.Naturwissenschaften. 1996; 83: 577-578Crossref Scopus (52) Google Scholar]. In our study, these possibilities can be ruled out, as social rank does not affect life expectancy in Ansell's mole-rats, and breeders do not differ from non-breeders in intrinsic quality or life style besides breeding, yet live approximately twice as long. We conclude, therefore, that sexual activity per se enhances lifespan in this species. This is, to our knowledge, the first time that a survival benefit of reproduction could be shown in a vertebrate. Our results have important implications for understanding the evolution of life histories and ageing. Furthermore, being a long-lived mammal with a bimodal ageing pattern that can be easily induced experimentally, Cryptomys anselli could become a valuable new model organism for studying the proximate mechanisms of ageing. We thank S. Begall, S. Cremers, A. Hartmann, J. Heinze, C. Ingram, L. Keller, M. Moshkin, E. Nevo, A. Schrempf and two anonymous reviewers for constructive comments on earlier versions of the manuscript. Download .pdf (.02 MB) Help with pdf files Document S1. Supplemental Experimental Procedures" @default.
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• W2018283353 title "Sexual activity and reproduction delay ageing in a mammal" @default.
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