Discussion

We show that three sympatric killer whale populations, have comparably long post-reproductive female lifespans. With a median of more than 30% of all adult female years in all three populations being lived by post-reproductive females, it is a substantial life history stage (Fig. 3). This is the first evidence showing a long post-reproductive period as a shared trait among genetically distinct killer whale populations, suggesting that it could have evolved in a common ancestor to current killer whales and that it might be present in other discrete populations. Indeed, phylogenomic analysis suggests that the divergence between the lineages leading to resident and Bigg’s ecotypes is the earliest divergence of extant killer whale lineages occurring over 350,000 years ago64. If the shared presence of a post-reproductive lifespan in both residents and Bigg’s is due to a shared ancestral trait, this suggests that a post-reproductive lifespan is an ancestral state of all extant killer whale ecotypes.
From the survival model output, the survival patterns is similar in all three killer whale populations, with females expected to live substantially longer than males and females being able to live >50 years (Fig. 2). Interestingly, the model predicts that male Bigg’s killer whales may have a longer expected lifespan compared to resident males (Fig. 2.), a pattern that may be influenced by the difference in their environments, both social65,66 and ecological (such as the recent prey abundance of the favourable prey of Bigg’s67). However, this could also be an effect of male dispersal in Bigg’s, resulting in more uncertainty for the model around the ages at death of males. In females the survival trajectory of this study is generally supported by previous estimates of lifespan in killer whales29,30. We used a Bayesian hierarchical approach to estimate the age-specific survival, with the benefit of being able to include individuals with unknown age of birth and death. Further, through permutations we were able to include individuals of unknown sex which likely produces random variation in the model output. Rather than considering maximum longevity, comparing the ages when 95% of years have been lived in each population is a more reliable measure (Fig. 2). This metric indicates that Bigg’s females are expected to live longer than females from both resident populations with a difference of ~10 years (Fig. 2). However, despite the differences in the estimated maximum lifespan, the results clearly show that all three populations have significant post-reproductive periods with similar ages of onset of the post-reproductive life stage in females (Table 4).
The cessation of female reproduction well before the end of life in a limited number of wild mammals largely remains an evolutionary puzzle. Yet, there is growing evidence that it has evolved based on the combined inclusive fitness benefits of helping and the costs of reproductive conflict for older females3. The opportunity for females to help kin is integral to the adaptiveness of ceasing reproduction well before the end of life9,15. Previous research in both humans and resident killer whales, has shown that older females are able to provide help that positively affects the survival and reproduction of their kin15,68,69. Especially in humans, offspring can have a long period, where they rely on older individuals for help providing food4. Our study demonstrates that females of both resident and Bigg’s killer whales can expect to live more than 20 years after they cease reproduction, allowing for a substantial period with the potential for helping kin. In resident killer whales, mothers impact the survival of their offspring well into their adult years15, and grandmothers are important repositories for ecological knowledge for relatives11 increasing the survival of their grandoffspring8. Although dispersal of both males and females is more pronounced within the Bigg’s ecotype, the post-reproductive females are never observed on their own, but always with either their son(s) or daughter(s)41. Further, the smaller matrilines may consist of up to three generations of maternally related kin and are regularly observed associating with individuals outside of the maternal group31,41. These patterns of association provide opportunities for social interactions that can lead to inclusive fitness benefits for older females11,70. While the earlier dispersal of females from Bigg’s groups likely reduces the occurrence of reproductive conflict between mothers and daughters (Fig. 1)4, Bigg’s groups can also consist of reproductively active females from different generations, similar to the resident killer whales. The similarity in the timing of the cessation of reproduction at around 40 years in both the resident and Bigg’s ecotypes, indicate that Bigg’s females may also experience inter-generational reproductive conflict and that this plays an important role in shaping fertility patterns across the different ecotypes. Testing this hypothesis requires more work on quantifying the kin structure and mortality patterns of Bigg’s killer whales.
Here we found that the differences in dispersal patterns between resident and Bigg’s killer whales did not predict the timing of the cessation of reproduction and the length of the post-reproductive lifespan. Similarly in humans, Snopkowski et al. (2014) compared age at menopause across ethnic groups with different patterns of post-marital residence to explore whether differences in dispersal pattern had an effect on the timing of menopause71. They showed that female-biased dispersal, expected to lead to an increase in female local relatedness with age, did not result in an earlier age at menopause compared to groups with male-biased dispersal patterns71. It is possible that modern societies in both humans and killer whales are different from the ancestral societies in which the evolutionary effects of reproductive conflict and the timing of menopause occurred. The lack of variation in the timing of reproductive cessation despite differences in dispersal patterns has important implications for our understanding of the evolution of a long post-reproductive period in mammals, including humans. Although patterns of kinship dynamics may predispose females to evolve a prolonged post-reproductive lifespan, the costs and benefits of reproductive conflict and helping are going to be shaped by the ecology of the population. For example, despite the close resemblance of demographic patterns between short- and long-finned (Globicephalas melas ) pilot whales72,73, indicating similar kinship patterns, a long post-reproductive lifespan has only been observed in the short-finned pilot whales1, which could be a result of difference in ecology of the two species. Moreover, there are several examples of primate species with female-biased dispersal and local mating (e.g. chimpanzee, bonobos and gorillas74–76), and thus an increase in female local relatedness with age similar to humans, where a prolonged post-reproductive lifespan has not evolved1. It is likely that we may find similarly prolonged post-reproductive lifespans in other killer whale populations or other mammal species as we gather more individual-based data on long-lived social mammals. Some evidence already suggests that false killer whales (Pseudorca crassidens )5 and Asian elephants (Elephas maximus ) have a long period as post-reproductive, although for Asian elephants it is likely a social rather than physiological trait77.
The similarity in the timing of menopause among killer whales and humans is curious and could hint at there being a similar driver of the evolution of onset of menopause. Current models investigating the role of kinship dynamics for driving the evolution of menopause make specific predictions regarding how patterns of helping and harming will change with age4,19 yet they do not predict how these patterns will drive the timing of menopause or the length of the post-reproductive lifespan. Hence our prediction that differences in dispersal patterns would lead to different selection pressures for a post-reproductive period in the two different killer whale ecotypes are currently based on the reasoning that kinship dynamics are an indicator for the strength of selection for helping vs harming across the lifespan. It is possible that menopause can not easily be reversed once evolved which may help explain the universality in the timing of menopause in humans, and likely also killer whales, despite the evident differences among societies, such as patterns of dispersal71.
In conclusion, when taken together with previous work, our findings support the hypothesis that kinship dynamics play a key role in the evolution of a prolonged post-reproductive lifespan. However, contrary to our predictions, the timing and expected duration of the post-reproductive lifespan did not vary with the dispersal pattern from the natal group, which likely represents different costs and benefits of helping and harming in the two ecotypes. These were, however, not taken into account in our predictions, but would be valuable to disentangle in future research to better understand the drivers for the timing of long post-reproductive lifespans in mammals. Nevertheless, the clear similarity of the post-reproductive period in some of the most genetically distinct killer whale populations echoes what has been observed across different human societies. This indicates a long post-reproductive period being an ancestral trait in killer whales, and likely present in other killer whale populations and ecotypes.