The evolution of menopause in toothed whales

This is the final version. Available on open access from Nature Research via the DOI in this recordData availability: All data used in this analysis are available as a database at: github.com/samellisq/marinelifehistdataCode availability: All R and stan code used for this analysis are available at osf.io/26s7m/. In addition, the mortality model is implemented as an R package available from: github.com/samellisq/marinesurvivalUnderstanding 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.Leverhulme TrustNatural Environment Research Council (NERC

Kinship dynamics: patterns and consequences of changes in local relatedness

This is the author accepted manuscript. The final version is available from the Royal Society via the DOI in this recordMounting evidence suggests that patterns of local relatedness can change over time in predictable ways, a process termed kinship dynamics. Kinship dynamics may occur at the level of the population or social group, where the mean relatedness across all members of the population or group changes over time, or at the level of the individual where an individual’s relatedness to its local group changes with age. Kinship dynamics are likely to have fundamental consequences for the evolution of social behaviour and life history because they alter the inclusive fitness payoffs to actions taken at different points in time. For instance, growing evidence suggests that individual kinship dynamics have shaped the evolution of menopause and age-specific patterns of helping and harming. To date, however, the consequences of kinship dynamics for social evolution have not been widely explored. Here we review the patterns of kinship dynamics that can occur in natural populations and highlight how taking a kinship dynamics approach has yielded new insights into behaviour and life history evolution. We discuss areas where analysing kinship dynamics could provide new insight into social evolution and we outline some of the challenges in predicting and quantifying kinship dynamics in natural populations.Natural Environment Research Council (NERC)Leverhulme Trus

Costly lifetime maternal investment in killer whales

This is the final version. Available on open access from Cell Press via the DOI in this recordData and code availability All data and code necessary to replicate analyses in this study have been deposited on Zenodo (DOI: 10.5281/zenodo.7457806).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, 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, 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.Natural Environment Research Council (NERC)Leverhulme Trus

A long post-reproductive lifespan is a shared trait among genetically distinct killer whale populations

This is the final version. Available on open access from Wiley via the DOI in this recordData availability: Data to replicate the analyses are available from the online repository: https://doi.org/10.5061/dryad.6t1g1jwxx. Requests for access to raw data can be directed to the authors, the Center for Whale Research (www.whaleresearch.com) or Fisheries and Oceans Canada (www.dfo-mpo.gc.ca)The extended female post-reproductive lifespan 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 post reproductive lifespan due to the combined costs of inter-generational 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 post-reproductive lifespan in both ecotypes with >30% of adult female years being lived as post-reproductive, supporting the general prediction that an increase in local relatedness with age predisposes the evolution of a post reproductive lifespan. Differences in the magnitude of kinship dynamics however, did not influence the timing or duration of the post-reproductive lifespan with females in both ecotypes terminating reproduction before their mid-40s followed by an expected post reproductive period of ~20 years. Our results highlight the important role of kinship dynamics in the evolution of a long post-reproductive lifespan 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.Nuffield FoundationNatural Environment Research Council (NERC)Leverhulme TrustEarthwatch InstituteNOAA FisheriesFisheries and Oceans Canada Species At Risk Progra

Age and sex influence social interactions, but not associations, within a killer whale pod

This is the author accepted manuscript. The final version is available from the Royal Society via the DOI in this record.Data accessibility: The processed contact, surfacing, and association networks, measures of dyadic sampling effort, estimated maternal kinship, individual attributes, and functions to conduct GLMQAP and general double-semi-partialling are included in the “aninet” R package on GitHub (https://github.com/MNWeiss/aninet). The raw time-series of detections and interactions, and R code necessary to reproduce all analyses, are available in the online supplementary material.Social structure is a fundamental aspect of animal populations. In order to understand the function and evolution of animal societies, it is important to quantify how individual attributes, such as age and sex, shape social relationships. Detecting these influences in wild populations under natural conditions can be challenging, especially when social interactions are difficult to observe and broad-scale measures of association are used as a proxy. In this study, we use unoccupied aerial systems to observe association, synchronous surfacing, and physical contact within a pod of southern resident killer whales (Orcinus orca). We show that interactions do not occur randomly between associated individuals, and that interaction types are not interchangeable. While age and sex did not detectably influence association network structure, both interaction networks showed significant social homophily by age and sex, and centrality within the contact network was higher among females and young individuals. These results suggest killer whales exhibit interesting parallels in social bond formation and social life histories with primates and other terrestrial social mammals, and demonstrate how important patterns can be missed when using associations as a proxy for interactions in animal social network studies.Natural Environment Research Council (NERC)National Fish and Wildlife FoundationPaul G Allen Family FoundationUW Center for Conservation BiologyCenter for Whale Researc