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Ecological Knowledge, Leadership, and the Evolution of Menopause in Killer Whales

2015; Elsevier BV; Volume: 25; Issue: 6 Linguagem: Inglês

10.1016/j.cub.2015.01.037

1879-0445

Lauren J. N. Brent, Daniel W. Franks, Emma Foster, Kenneth C. Balcomb, Michael A. Cant, Darren P. Croft,

Coastal and Marine Management

Classic life-history theory predicts that menopause should not occur because there should be no selection for survival after the cessation of reproduction [1Williams G.C. Pleiotropy, natural selection, and the evolution of senescence.Evolution. 1957; 11: 398-411Crossref Google Scholar]. Yet, human females routinely live 30 years after they have stopped reproducing [2Hill K. Hurtado A.M. Social science: Human reproductive assistance.Nature. 2012; 483: 160-161Crossref PubMed Scopus (7) Google Scholar]. Only two other species—killer whales (Orcinus orca) and short-finned pilot whales (Globicephala macrorhynchus) [3Marsh H. Kasuya T. Evidence for reproductive senescence in female cetaceans.Rep. Int. Whaling Comm. 1986; 8: 57-74Google Scholar, 4Olesiuk P.F. Bigg M.A. Ellis G.M. Life history and population dynamics of resident killer whales (Orcinus orca) in the coastal waters of British Columbia and Washington State.Rep. Int. Whaling Comm. 1990; 12: 209-243Google Scholar]—have comparable postreproductive lifespans. In theory, menopause can evolve via inclusive fitness benefits [5Johnstone R.A. Cant M.A. The evolution of menopause in cetaceans and humans: the role of demography.Proc. Biol. Sci. 2010; 277: 3765-3771Crossref PubMed Scopus (123) Google Scholar, 6Hawkes K. O'Connell J.F. Jones N.G.B. Alvarez H. Charnov E.L. Grandmothering, menopause, and the evolution of human life histories.Proc. Natl. Acad. Sci. USA. 1998; 95: 1336-1339Crossref PubMed Scopus (857) Google Scholar], but the mechanisms by which postreproductive females help their kin remain enigmatic. One hypothesis is that postreproductive females act as repositories of ecological knowledge and thereby buffer kin against environmental hardships [7McAuliffe K. Whitehead H. Eusociality, menopause and information in matrilineal whales.Trends Ecol. Evol. 2005; 20: 650Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar, 8Diamond J. Unwritten knowledge.Nature. 2001; 410: 521Crossref PubMed Scopus (21) Google Scholar]. We provide the first test of this hypothesis using a unique long-term dataset on wild resident killer whales. We show three key results. First, postreproductively aged females lead groups during collective movement in salmon foraging grounds. Second, leadership by postreproductively aged females is especially prominent in difficult years when salmon abundance is low. This finding is critical because salmon abundance drives both mortality and reproductive success in resident killer whales [9Ford J.K. Ellis G.M. Olesiuk P.F. Balcomb K.C. Linking killer whale survival and prey abundance: food limitation in the oceans' apex predator?.Biol. Lett. 2009; 6: 139-142Crossref PubMed Scopus (170) Google Scholar, 10Ward E.J. Holmes E.E. Balcomb K.C. Quantifying the effects of prey abundance on killer whale reproduction.J. Appl. Ecol. 2009; 46: 632-640Crossref Scopus (109) Google Scholar]. Third, females are more likely to lead their sons than they are to lead their daughters, supporting predictions of recent models [5Johnstone R.A. Cant M.A. The evolution of menopause in cetaceans and humans: the role of demography.Proc. Biol. Sci. 2010; 277: 3765-3771Crossref PubMed Scopus (123) Google Scholar] of the evolution of menopause based on kinship dynamics. Our results show that postreproductive females may boost the fitness of kin through the transfer of ecological knowledge. The value gained from the wisdom of elders can help explain why female resident killer whales and humans continue to live long after they have stopped reproducing.