Sociality and cooperative breeding are associated with enhanced longevity in insects and birds, but whether this is also true for mammals is still subject to debate. African mole-rats (Bathyergidae) have recently been claimed to be the only mammalian family in which such an association may exist because cooperatively breeding bathyergids seem to be substantially longer lived than solitary bathyergids. However, although ample longevity data are available for several social bathyergids, almost nothing is known about mortality distribution and lifespan in solitary bathyergids. Here we present robust long-term data on the longevity of a solitary African mole-rat, the silvery mole-rat Heliophobius argenteocinereus. Our findings show that this species is much longer-lived than previously believed. Nonetheless, our comparative analysis suggests that sociality has indeed a positive effect on longevity in this family. We argue that the extreme longevity seen particularly in social bathyergids is probably caused by a combination of subterranean lifestyle and cooperative breeding.

Central Animal Laboratory Faculty of Medicine University of Duisburg Essen Germany

Department of General Zoology Faculty of Biology University of Duisburg Essen Germany

Faculty of Science University of Southern Bohemia České Budějovice Czech Republic

Zobrazit více v PubMed

Kamilar JM, Bribiescas RG, Bradley BJ. 2010. Is group size related to longevity in mammals? Biol. Lett. 6, 736-739. (10.1098/rsbl.2010.0348) PubMed DOI PMC

Healy K. 2015. Eusociality but not fossoriality drives longevity in small mammals. Proc. Biol. Sci. 282, 20142917. (10.1098/rspb.2014.2917) PubMed DOI PMC

Lucas ER, Keller L. 2019. The co-evolution of longevity and social life. Funct. Ecol. 34, 76-87. (10.1111/1365-2435.13445) DOI

Thorley J. 2020. The case for extended lifespan in cooperatively breeding mammals: a re-appraisal. PeerJ. 8, e9214. (10.7717/peerj.9214) PubMed DOI PMC

Buffenstein R, Jarvis JUM. 2002. The naked mole rat—a new record for the oldest living rodent. Sci. Aging Knowledge Environ. 2002, pe7. (10.1126/sageke.2002.21.pe7) PubMed DOI

Dammann P, Šumbera R, Massmann C, Scherag A, Burda H. 2011. Extended longevity of reproductives appears to be common in Fukomys mole-rats (Rodentia, Bathyergidae). PLoS ONE 6, e18757. (10.1371/journal.pone.0018757) PubMed DOI PMC

Ruby JG, Smith M, Buffenstein R. 2018. Naked mole-rat mortality rates defy Gompertzian laws by not increasing with age. Elife 7, e31157. (10.7554/eLife.31157) PubMed DOI PMC

Tacutu R, et al. 2018. Human ageing genomic resources: new and updated databases. Nucleic Acids Res. 46, D1083-D1090. (10.1093/nar/gkx1042) PubMed DOI PMC

Ronget V, Gaillard JM. 2019. Assessing ageing patterns for comparative analyses of mortality curves: going beyond the use of maximum longevity. Funct. Ecol. 34, 65-75. (10.1111/1365-2435.13474) DOI

de Magalhães JP, Costa J, Church GM. 2007. An analysis of the relationship between metabolism, developmental schedules, and longevity using phylogenetic independent contrasts. J. Gerontol. Biol. Sci. Med. Sci. 62, 149-160. (10.1093/gerona/62.2.149) PubMed DOI PMC

Can E, Smith M, Boukens BJ, Coronel R, Bufenstein R, Riegler J. 2022. Naked mole-rats maintain cardiac function and body composition well into their fourth decade of life. GeroScience 44, 731-746. (10.1007/s11357-022-00522-6) PubMed DOI PMC

Begall S, Nappe R, Hohrenk L, Schmidt TC, Burda H, Sahm A, Szafranski K, Dammann P, Henning Y. 2021. Life expectancy, family constellation and stress in giant mole-rats (Fukomys mechowii). Phil. Trans. R. Soc. B 376, 20200207. (10.1098/rstb.2020.0207) PubMed DOI PMC

Dammann P, et al. 2019. Comment on ‘Naked mole-rat mortality rates defy Gompertzian laws by not increasing with age’. eLife 8, E45415. (10.7554/eLife.45415) PubMed DOI PMC

Fang X, et al. 2014. Adaptations to a subterranean environment and longevity revealed by the analysis of mole rat genomes. Cell Rep. 8, 1354-1364. (10.1016/j.celrep.2014.07.030) PubMed DOI PMC

Weigl R. 2005. Longevity of mammals in captivity: from the living collections of the world. Stuttgart, Germany: Kleine Senckenberg-Reihe, Nr. 48.

Bennett NC, Faulkes CG, Hart L, Jarvis JUM. 2009. Bathyergus suillus (Rodentia: Bathyergidae). Mamm. Species 828, 1-7. (10.1644/828.1) DOI

Šumbera, et al. Submitted. The biology of an isolated Mashona mole-rat population from southern Malawi, with implications for the diversity and biogeography of the genus Fukomys. Org. Divers. Evol.

McElreath R. 2020. Statistical rethinking: a Bayesian course with examples in R and stan. New York, NY: Chapman and Hill/CRC Press.

Gelman A. 2008. Scaling regression inputs by dividing by two standard deviations. Stat. Med. 27, 2865-2873. PubMed

Pearl J. 1995. Causal diagrams for empirical research. Biometrika 82, 669-688.

Greenland S, Pearl J, Robins JM. 1999. Causal diagrams for epidemiologic research. Epidemiology 10, 37-48. PubMed

Pearl J, Glymour M, Jewell NP. 2016. Causal inference in statistics: a primer. Chichester, UK: John Wiley & Sons.

Pearl J. 2001. Direct and indirect effects. In Proceedings of the Seventeenth Conference on Uncertainy in Articial Intelligence, pp. 373-392. San Francisco, CA: Morgan Kaufmann. See https://ftp.cs.ucla.edu/pub/stat_ser/R273-U.pdf.

Acharya A, Blackwell M, Sen M. 2016. Explaining causal findings without bias: detecting and assessing direct effects. Am. Political Sci. Rev. 110, 512-529.

Dammann P, Burda H. 2007. Senescence patterns in African mole-rats (Bathyergidae, Rodentia). In Subterranean rodents: news from underground, pp. 251-263. Berlin, Germany: Springer.

Upham NS, Esselstyn JA, Jetz W. 2019. Inferring the mammal tree: species-level sets of phylogenies for questions in ecology, evolution, and conservation. PLoS Biol. 17, e3000494. PubMed PMC

Carpenter B, et al. 2017. Stan: a probabilistic programming language. J. Stat. Softw. 76, 1-32. PubMed PMC

RStudio Team. 2020. RStudio: integrated development for R. Boston, MA: RStudio, PBC. http://www.rstudio.com/.

Cole SR, Hernán MA. 2002. Fallibility in estimating direct effects. Int. J. Epidemiol. 31, 163-165. PubMed

Montgomery JM, Nyhan B, Torres M. 2018. How conditioning on posttreatment variables can ruin your experiment and what to do about it. Am. Political Sci. Rev. 62, 760-775.

Knox D, Lowe W, Mummolo J. 2020. Administrative records mask racially biased policing. Am. Political Sci. Rev. 114, 619-637.

Novikov EA, Burda H. 2013. Ecological and evolutionary preconditions of extended longevity in subterranean rodents. Biol. Bull. Rev. 3, 325-333. (10.1134/S2079086413040051) DOI

Healy K, et al. 2014. Ecology and mode-of-life explain lifespan variation in birds and mammals. Proc. Biol. Sci. 281, 20140298. (10.1098/rspb.2014.0298) PubMed DOI PMC

Schmidt CM, Jarvis JUM, Bennett NC. 2013. The long-lived queen: reproduction and longevity in female eusocial Damaraland mole-rats (Fukomys damarensis). Afr. Zool. 48, 193-196. (10.1080/15627020.2013.11407583) DOI

Dammann P, Burda H. 2006. Sexual activity and reproduction delay ageing in a mammal. Curr. Biol. 16, R117-R118. (10.1016/j.cub.2006.02.012) PubMed DOI

Downing PA, Griffin AS, Cornwallis CK. 2021. Hard-working helpers contribute to long breeder lifespans in cooperative birds. Phil. Trans. R. Soc. B 376, 20190742. (10.1098/rstb.2019.0742) PubMed DOI PMC

Harvey P, Zammuto R. 1985. Patterns of mortality and age at first reproduction in natural populations of mammals. Nature 315, 319-320. (10.1038/315319a0) PubMed DOI

Šklíba J, Lövy M, Burda H, Šumbera R. 2016. Variability of space-use patterns in a free living eusocial rodent, Ansell's mole-rat indicates age-based rather than caste polyethism. Sci. Rep. 6, 37497. (10.1038/srep37497) PubMed DOI PMC

Lövy M, Šklíba J, Šumbera R. 2013. Spatial and temporal activity patterns of the free-living giant mole-rat (Fukomys mechowii), the largest social bathyergid. PLoS ONE 8, e55357. (10.1371/journal.pone.0055357) PubMed DOI PMC

Francioli Y, Thorley J, Finn K, Clutton-Brock T, Zöttl M. 2020. Breeders are less active foragers than non-breeders in wild Damaraland mole-rats. Biol. Lett. 16, 20200475. (10.1098/rsbl.2020.0475) PubMed DOI PMC

Zöttl M, Bensch HM, Finn KT, Hart DW, Thorley JB, Bennett NC, Braude S. 2022. Capture order across social bathyergids indicate similarities in division of labour and spatial organisation. Front. Ecol. Evol. 10, 877221. (10.3389/fevo.2022.877221) DOI

Hölldobler B, Wilson EO. 1990. The ants. Berlin, Germany: Springer.

Carey JR. 2001. Demographic mechanisms for the evolution of long life in social insects. Exp. Gerontol. 36, 713-722. (10.1016/s0531-5565(00)00237-0) PubMed DOI

Jemielity S, Chapuisat M, Parker JD, Keller L. 2005. Long live the queen: studying aging in social insects. Age 27, 241-248. (10.1007/s11357-005-2916-z) PubMed DOI PMC

Dammann P, Šaffa G, Šumbera R.. 2022. Data from: Longevity of a solitary mole-rat species and its implications for the assumed link between sociality and longevity in African mole-rats (Bathyergidae). Figshare. (10.6084/m9.figshare.c.6277193) PubMed DOI PMC

Longevity of a solitary mole-rat species and its implications for the assumed link between sociality and longevity in African mole-rats (Bathyergidae)

Zobrazit více v PubMed

figshare
10.6084/m9.figshare.c.6277193