Introduction

The evolution of an extended female post-reproductive lifespan is extremely rare in nature and is at present only known in five species of wild mammals1–3. Outside of the prolonged post-reproductive lifespan seen in humans the only other species of mammals in which females have evolved early cessation of reproduction are toothed whales: short-finned pilot whales (Globicephala macrorhynchus ), narwhals (Monodon monoceros ), belugas (Delphinapterus leucas ) and resident-ecotype killer whales (Orcinus orca )1,4. Some evidence suggests that also the false killer whales (Pseudorca crassidens ) have a substantial post-reproductive period5. In resident-ecotype killer whales, for example, adult females typically give birth to their last calf in their mid 30’s to early 40’s followed by a post-reproductive lifespan that may span many decades1. In the classical view of evolutionary theory, early termination of reproduction is not a beneficial trait6,7 and understanding why and how the post-reproductive lifespan has evolved remains a considerable challenge for evolutionary biology.
Adaptive explanations for the evolution of a long post-reproductive lifespan have tended to focus on the inclusive fitness benefits of helping kin in late life8–10. Females can gain inclusive fitness benefits in late life by ceasing reproduction and instead invest their energy in helping existing offspring survive and reproduce (‘the mother hypothesis’)6. Further, through behaviours that help increase the survival of grandchildren, such as providing ecological knowledge11 or provisioning12, post-reproductive females can increase their inclusive fitness (’the grandmother hypothesis’)13. In humans, grandmother benefits appear to be key for the evolution of a long post-reproductive lifespan13,14 and recent work in resident killer whales provides support for both the mother and grandmother hypothesis with the presence of both mothers and post-reproductive grandmothers having a positive impact on the survival of their adult offspring and grandofffspring8,15. However, the inclusive fitness benefits from helping are likely not on its own sufficient to explain the timing of menopause in both killer whales and humans16 leading to the search for additional mechanisms that can contribute to the early termination of reproduction17,18. Recent work has shown that kin-selected costs, as well as benefits, are important for the evolution of extended post-reproductive lifespans4,19.
Demographic patterns with either female-biased dispersal and local mating or natal philopatry of both sexes and non-local mating, give rise to age-specific changes in the relatedness of an individual to its group (kinship dynamics), in particular an increase in average female relatedness to other group members with age19. In the case of resident killer whales, females are born into social unit (“matriline”) consisting of their mother, siblings and other more distant relatives20. As they age, their own sons replace more distantly related males in the matriline, increasing their average local relatedness to the group over time21. This ultimately leads to an asymmetry in selection for helping and harming with age, which means that older females that are more related on average to the group are under stronger selection to help, while younger females are under stronger selection to harm4. Thus, in competition for reproduction older females experience a larger inclusive fitness cost compared with younger females21. The combination of such inclusive costs of inter-generational reproductive conflict and inclusive fitness benefits of helping kin are hypothesised to be key predictors for the evolution of a long post-reproductive lifespan in mammals1,4,19.
Investigating kinship dynamics and age-specific life history changes requires long-term social and demographic data that captures most of the lifespan of animals. These data are therefore rare in long-lived mammals. The long term data collected on different populations of killer whales in the coastal waters of the USA and Canada now extends over more than four decades, providing an unique opportunity to examine the link between kinship dynamics and life history evolution in a long-lived marine mammal. In addition to the support for the mother and grandmother hypotheses in resident killer whales8,15, there is strong support for the reproductive conflict hypothesis with offspring of older females that are born into conflict with offspring of a younger female having a 1.7 times higher mortality risk21. However, it is still unknown whether these traits are shared between different populations of killer whales. Killer whales are among the most widely dispersed mammals on the planet and are found in all oceans22,23. Lineages that differ morphologically24 and behaviourally25 and are genetically isolated26, are referred to as ecotypes. Three killer whale ecotypes are sympatric in the northeast Pacific and among them are several populations of both resident and Bigg’s killer whales27,28. In the waters off the west coast of North America are the Northern and Southern populations of resident killer whales and the West Coast Transient populations of Bigg’s killer whales (Table 1; a third offshore ecotype is also encounterd, but only very rarely is not considered here)26,27,29. Both populations of residents are specialist fish-eaters with salmon making up the almost all of their prey20,30, whereas Bigg’s killer whales are specialised in hunting marine mammals31. This differentiation in diet is reflected in the social behaviour of the ecotypes with resident killer whales typically being observed travelling in larger social groups consisting of several maternal groups, compared to Bigg’s killer whales. The mean group size of cohesive maternal groups however are similar for the two ecotypes (Table 1)32. In resident killer whales there is almost no dispersal of males and limited dispersal of females from the maternal group. In contrast, there is dispersal of both sexes from the maternal group of Bigg’s killer whales31,33, which may be related to maintaining optimal group foraging size for predating on marine mammals34,35.