The evolution of menopause in toothed whales.

Understanding how and why menopause has evolved is a long-standing challenge across disciplines. Females can typically maximize their reproductive success by reproducing for the whole of their adult life. In humans, however, women cease reproduction several decades before the end of their natural lifespan1,2. Although progress has been made in understanding the adaptive value of menopause in humans3,4, the generality of these findings remains unclear. Toothed whales are the only mammal taxon in which menopause has evolved several times5, providing a unique opportunity to test the theories of how and why menopause evolves in a comparative context. Here, we assemble and analyse a comparative database to test competing evolutionary hypotheses. We find that menopause evolved in toothed whales by females extending their lifespan without increasing their reproductive lifespan, as predicted by the 'live-long' hypotheses. We further show that menopause results in females increasing their opportunity for intergenerational help by increasing their lifespan overlap with their grandoffspring and offspring without increasing their reproductive overlap with their daughters. Our results provide an informative comparison for the evolution of human life history and demonstrate that the same pathway that led to menopause in humans can also explain the evolution of menopause in toothed whales.

Temporal dynamics of mother-offspring relationships in Bigg's killer whales: opportunities for kin-directed help by post-reproductive females.

Age-related changes in the patterns of local relatedness (kinship dynamics) can be a significant selective force shaping the evolution of life history and social behaviour. In humans and some species of toothed whales, average female relatedness increases with age, which can select for a prolonged post-reproductive lifespan in older females due to both costs of reproductive conflict and benefits of late-life helping of kin. Killer whales (Orcinus orca) provide a valuable system for exploring social dynamics related to such costs and benefits in a mammal with an extended post-reproductive female lifespan. We use more than 40 years of demographic and association data on the mammal-eating Bigg's killer whale to quantify how mother-offspring social relationships change with offspring age and identify opportunities for late-life helping and the potential for an intergenerational reproductive conflict. Our results suggest a high degree of male philopatry and female-biased budding dispersal in Bigg's killer whales, with some variability in the dispersal rate for both sexes. These patterns of dispersal provide opportunities for late-life helping particularly between mothers and their adult sons, while partly mitigating the costs of mother-daughter reproductive conflict. Our results provide an important step towards understanding why and how menopause has evolved in Bigg's killer whales.

Costly lifetime maternal investment in killer whales.

Parents often sacrifice their own future reproductive success to boost the survival of their offspring, a phenomenon referred to as parental investment. In several social mammals, mothers continue to improve the survival of their offspring well into adulthood;1,2,3,4,5 however, whether this extended care comes at a reproductive costs to mothers, and therefore represents maternal investment, is not well understood. We tested whether lifetime maternal care is a form of parental investment in fish-eating "resident" killer whales. Adult killer whales, particularly males, are known to receive survival benefits from their mothers;3 however, whether this comes at a cost to mothers' reproductive success is not known. Using multiple decades of complete census data from the "southern resident" population, we found a strong negative correlation between females' number of surviving weaned sons and their annual probability of producing a viable calf. This negative effect did not attenuate as sons grew older, and the cost of sons could not be explained by long-term costs of lactation or group composition effects, supporting the hypothesis that caring for adult sons is reproductively costly. This is the first direct evidence of lifetime maternal investment in an iteroparous animal, revealing a previously unknown life history strategy.

A long postreproductive life span is a shared trait among genetically distinct killer whale populations.

The extended female postreproductive life span found in humans and some toothed whales remains an evolutionary puzzle. Theory predicts demographic patterns resulting in increased female relatedness with age (kinship dynamics) can select for a prolonged postreproductive life span due to the combined costs of intergenerational reproductive conflict and benefits of late-life helping. Here, we test this prediction using >40 years of longitudinal demographic data from the sympatric yet genetically distinct killer whale ecotypes: resident and Bigg's killer whales. The female relatedness with age is predicted to increase in both ecotypes, but with a less steep increase in Bigg's due to their different social structure. Here, we show that there is a significant postreproductive life span in both ecotypes with >30% of adult female years being lived as postreproductive, supporting the general prediction that an increase in local relatedness with age predisposes the evolution of a postreproductive life span. Differences in the magnitude of kinship dynamics however did not influence the timing or duration of the postreproductive life span with females in both ecotypes terminating reproduction before their mid-40s followed by an expected postreproductive period of about 20 years. Our results highlight the important role of kinship dynamics in the evolution of a long postreproductive life span in long-lived mammals, while further implying that the timing of menopause may be a robust trait that is persistent despite substantial variation in demographic patterns among populations.