Reproductive Conflict and the Evolution of Menopause in Killer Whales

Abstract

Why females of some species cease ovulation prior to the end of their natural lifespan is a long-standing evolutionary puzzle [1-4]. The fitness benefits of post-reproductive helping could in principle select for menopause [1, 2, 5], but the magnitude of these benefits appears insufficient to explain the timing of menopause [6-8]. Recent theory suggests that the cost of inter-generational reproductive conflict between younger and older females of the same social unit is a critical missing term in classical inclusive fitness calculations (the "reproductive conflict hypothesis" [6, 9]). Using a unique long-term dataset on wild resident killer whales, where females can live decades after their final parturition, we provide the first test of this hypothesis in a non-human animal. First, we confirm previous theoretical predictions that local relatedness increases with female age up to the end of reproduction. Second, we construct a new evolutionary model and show that given these kinship dynamics, selection will favor younger females that invest more in competition, and thus have greater reproductive success, than older females (their mothers) when breeding at the same time. Third, we test this prediction using 43 years of individual-based demographic data in resident killer whales and show that when mothers and daughters co-breed, the mortality hazard of calves from older-generation females is 1.7 times that of calves from younger-generation females. Intergenerational conflict combined with the known benefits conveyed to kin by post-reproductive females can explain why killer whales have evolved the longest post-reproductive lifespan of all non-human animals.

Postreproductive lifespans are rare in mammals

“…In killer whales, for example, older females lead their group at times of low resource abundance (Brent et al., ). Moreover, in both humans and killer whales, older females suffer costs by reproducing at the same time as their daughters, which will select for reproductive restraint and cessation in late life (Croft et al., ; Lahdenperä, Gillespie, Lummaa, & Russell, ).…”

The Williams' legacy: A critical reappraisal of his nine predictions about the evolution of senescence

“…It is also noteworthy that many reports are based on case studies from zoos where food provisioning and veterinary care might exaggerate the number of postreproductive years (Croft et al. ). Among mammalian species both the relative occurrence and duration of the postreproductive life can be extremely variable.…”

“…; see also Croft et al. ) but the true adaptive value of this hypothesis and its generality remain to be assessed (Croft et al. ).…”

Linking demographic processes and foraging ecology in wandering albatross—Conservation implications

“…The ageing pattern especially appearance of senescence nicely falls within the primate continuum of ageing, between chimpanzee and human (Bronikowski et al., ), with the same tendencies for males to have shorter life spans and higher mortality at old ages than females (Pardo, Barbraud, & Weimerskirch, ), a sex ratio at birth biased systematically towards males (Weimerskirch, Lallemand, & Martin, ), suggesting that mortality patterns in long‐lived species are shaped by local selective forces rather than phylogeny (Forslund & Pärt, ). Of course, they differ from primates and from other long‐lived marine animals such as killer whale (Croft et al., ) where menopause occurs in that female albatrosses reproduce throughout their life until old ages. Why are males suffering a higher mortality at old ages than females?…”