The Evolution of Sex Differences in Mammalian Social Life Histories

Lead Research Organisation: UNIVERSITY OF EXETER
Department Name: Psychology

Abstract

Understanding why social behaviour and life histories have diverged between the sexes in long-lived social mammals, sometimes to an extreme degree, is a key objective in the biological, medical and social sciences. We propose that differences between the sexes in how males and females interact with related individuals across the lifespan are a major force driving the evolution of sex differences in both social behaviour and life history.

In social species related individuals (kin) often live together in close knit family groups and individuals can influence the survival and reproductive success of their relatives both by their behaviour (cooperative and competitive) and reproductive decisions (if an individual reproduces it will use resources that may negatively impact on the survival and reproductive success of kin). Such interactions between kin are a strong evolutionary force, with individuals gaining indirect benefits (through the genes they share with relatives) by increasing the survival and reproductive success of their kin. For example, kin selection can favour individual strategies that increase the reproductive success of kin, even if this comes at a cost to an individual's survival and reproductive success. The opportunity for evolution to be shaped by kin selection is dependent on how and when related individuals interact.

Our pilot work suggests that in many species males and females experience very different patterns of local relatedness across their lifespans (kinship dynamics) due to patterns of dispersal and mating. For example, for some species such as killer whales, females become more related to their local group with age whereas males, in contrast, become less related. We hypothesise that sex differences in kinship dynamics will be a major force driving the evolution of sex differences in both (i) social behaviour and (ii) life history.

We will determine the role of kinship dynamics in driving the evolution of sex differences in social behaviour and life history evolution using a combination of theoretical modelling and empirical data analysis. We will develop a general theory of kinship dynamics and develop new models to predict both the patterns of kinship dynamics and their consequences for the evolution of social life histories in both males and females. Our model will make predictions for patterns of helping and harming in social groups including both behavioural traits (cooperation and conflict) and reproductive traits (e.g. age at first or last reproduction).

We will provide the first test of the behavioural predictions of our new theory by collecting new data on patterns of helping (e.g. babysitting and food sharing) and harming (aggression) in resident killer whales using unmanned aerial vehicles (drones). Resident killer whales are ideally suited to testing the behavioural predictions of the model - they have extreme sex differences in kinship dynamics and have unexplained sex differences in life history. We will test the life history predictions of the theoretical framework by comparing patterns of kinship dynamics and sex differences in life history evolution (e.g. patterns of growth, age at first reproduction, age at last reproduction, reproductive investment and longevity) across social mammals which will allow us to determine the role of kinship dynamics in driving life history evolution and the divergence of life histories between the sexes.

Planned Impact

We expect the work to benefit, both nationally and internationally, the following key end-users:

Ecologists and conservation managers in academia, regulatory authorities and NGOs. Providing new knowledge of how social factors contribute to patterns of fecundity and mortality in natural populations will benefit ecologists studying the population dynamics of long-lived social mammals, and managers of mammalian populations that are of conservation concern. Indeed, one of the study populations (the Southern resident killer whale population) is classified as endangered in both Canada and the USA. Advancing our understanding of the relationship between population social structure and patterns of survival and mortality in the population will help inform future conservation strategies of this and other killer whale populations. Impact in this area will be facilitated by our links with NOAA and the Whale and Dolphin Conservation trust (see letters of support).

Wildlife ecotourism. Whale watching is a significant and growing part of the international ecotourism market. In 2009 for example, more than 13 million people took whale watching tours across 119 countries, which generated an expenditure of $2.1 billion [1]. An important part of this market is based around the Southern resident killer whale population, which is the focus of the behavioural work in this study. For example, the whale watching industry in Washington and British Colombia attracts almost 1 million whale watchers annually and generates $180 million of expenditure [1]. In the UK the whale watching market generates a total expenditure of $21 million per annum [1]. Whilst this market is based mainly around smaller cetaceans, it also includes killer whales in Scottish waters. The outputs of this research will both increase the awareness of potential consumers to this market and provide the ecotourism industry with key information on the biology and ecology of killer whales, which they can use to inform tourists. Impact in this area will be facilitated by our existing links with the Pacific Whale Watch Association, a group of 32 dedicated whale watching businesses that annually take approximately 500,000 visitors on whale watching trips (see letter of support).

The general public and schools. Social mammals are intrinsically appealing to the general public and we aim to capitalise on this interest to improve the public understanding of science and conservation issues. We will aim to inform the public about how social factors shape sex differences in life history in natural populations and how this helps us to understand how our own life history evolved. We will work with school children and young people who are at critical points in their education with the aim of inspiring them to follow a career path in the sciences and raising their awareness of the natural world and the threats that it faces.

[1] O'Connor, S., Campbell, R., Cortez, H., & Knowles, T. (2009). Whale Watching Worldwide: tourism numbers, expenditures and expanding economic benefits, a special report from the International Fund for Animal Welfare. Yarmouth MA, USA, prepared by Economists at Large.

Publications

10 25 50
 
Description Understanding why social behaviour and life histories have diverged between the sexes in long-lived social mammals, sometimes to an extreme degree, is a key objective in the biological, medical and social sciences. In this project, we have examined how differences between the sexes in how males and females interact with related individuals across the lifespan (kinship dynamics) have driven the evolution of sex differences in both social behaviour and life history. We have developed a new theoretical model to predict how patterns of kinship change with age and the potential consequences of these changes for sex differences in social evolution. We have tested this new theory in resident killer whales, which are ideally suited to testing the behavioural predictions of our models - they have extreme sex differences in kinship dynamics and have unexplained sex differences in life history.

This work has led to three key findings:

1. Sex differences in kinship dynamics are widespread in animal societies. Using species comparative data we demonstrated not only that kinship dynamics occur in animal systems but also that the direction and magnitude of kinship dynamics can be accurately predicted using a simple model. Using a new theoretical model, we demonstrated that kinship dynamics can profoundly affect lifetime patterns of behaviour and can drive sex differences in helping and harming behaviour across the lifespan. This work demonstrates that kinship dynamics are likely to be a fundamental dimension of social evolution, especially when considering age-linked changes and sex differences in behaviour and life history.

2. Post-reproductive females provide social support to their adult male offspring. Models of kinship dynamics predict that post-reproductive female killer whales should help their adult sons, but how they help remains unclear. One hypothesis is that they provide social support and reduce the aggression their sons experience. Using 38 years of photographic data, we quantified the occurrence of tooth rake marks on wild resident killer whales and quantified how patterns of aggression were impacted by the age and sex of the individual and its social environment. We found that socially inflicted injuries were lower for male offspring in the presence of their post-reproductive mother, highlighting that directing late-life support may be a key pathway by which post-reproductive females transfer social benefits to their male offspring.

3. Post-reproductive females provide lifelong investment in their adult offspring. Parents often sacrifice their own future reproductive success to boost the survival of their offspring, a phenomenon referred to as parental investment. However, the extent to which parental investment extends across the lifespan of the offspring is not well understood. Using multiple decades of complete census data in our killer whale study population, we found a strong negative correlation between females' number of surviving weaned sons and their annual probability of producing a viable calf, 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.
Exploitation Route The evolution of sex differences in life history has attracted considerable attention across a range of disciplines. Outputs of this work will benefit researchers across disciplines working on the evolution of life history, social behaviour, cooperation and conflict, specifically: (i) Evolutionary biologists and anthropologists interested in the evolution of social behaviour and the relationship between population social structure and life history evolution; (ii) Biologists and ecologists studying the population biology of cooperative species: through new insight into how social factors shape mortality and fertility in natural populations. This will also help conservation biologists and wildlife managers to understand population processes in cooperative breeding long-lived mammals, many of which are of conservation concern; (iii) Biologists working more generally on the social structure of animal societies and the structure and function of animal social networks: from new insight into how patterns of social interactions among related individuals change with age in natural populations; (iv) Behavioural ecologists, evolutionary biologists, and anthropologists interested in the evolution of cooperation and conflict: from new insights into how selection for cooperation and conflict change across the lifespan and how these patterns differ between the sexes and across species.
Sectors Environment

Other

 
Description There are two main areas of impact. First our work has generated considerable public interest. For example, two of the research papers produced as part of this project have Altmetric scores of over 2000. Public and media interest in this work has resulted in numerous radio and television interviews and widespread coverage across major international press. As part of this work, the PI has been a scientific consultant on a Disney channel documentary about killer whales. Second, this work has had an impact on our project partner the Center for Whale Research. Research findings have provided new insight into factors that constrain reproduction in our killer whale study population, which is critically endangered. This information will feed into reports to government bodies that are responsible for the conservation and management of the killer whale population. Moreover, the Center for Whale Research has directly benefited from the new knowledge we have developed as part of this project, which has provided new material for their education centre. In particular, as part of this research, we have installed a new virtual reality exhibit at their education centre that allows the public to join the research team on an encounter with a group of killer whales.
First Year Of Impact 2023
Sector Education,Environment,Culture, Heritage, Museums and Collections,Other
Impact Types Societal

 
Description Perturbation, Social Rewiring, and Population Dynamics in Animal Societies
Amount £65,000 (GBP)
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 08/2023 
End 09/2026
 
Title Age and sex influence social interactions, but not associations, within a killer whale pod 
Description This dataset is associated with the paper "Age and sex influence social interactions, but not associations, within a killer whale pod" 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 electronic supplementary material. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
Impact Weiss MN, Franks DW, Giles DA, Youngstrom S, Wasser SK, Balcomb KC, Ellifrit DK, Domenici P, Cant MA, Ellis S, et al (2021). Age and sex influence social interactions, but not associations, within a killer whale pod. Proceedings of the Royal Society B: Biological Sciences, 288(1953). 
URL https://rs.figshare.com/collections/Supplementary_material_from_Age_and_sex_influence_social_interac...
 
Title Costly lifetime maternal investment in killer whales 
Description R code and data necessary to reproduce all analyses from the manuscript "Costly lifetime maternal investment in killer whales." Included is reproductive history data on 40 southern resident killer whale females, the R code to fit Bayesian regression models, code to produce the plots in the manuscript, and code to perform sensitivity analysis for fixed effect priors. 
Type Of Material Database/Collection of data 
Year Produced 2023 
Provided To Others? Yes  
Impact Weiss, M. N., Ellis, S., Franks, D. W., Nielsen, M. L. K., Cant, M. A., Johnstone, R. A., Ellifrit, D. K., Balcomb, K. C., & Croft, D. P. (2023). Costly lifetime maternal investment in killer whales. Current Biology, 33(4), 744-748.e3. https://doi.org/10.1016/j.cub.2022.12.057 
URL https://zenodo.org/records/7457806
 
Title Mixture models as a method for comparative sociality: social networks and demographic change in resident killer whales 
Description Contains the data associated with the research publication "Mixture models as a method for comparative sociality: social networks and demographic change in resident killer whales" 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
Impact Ellis S, Franks DW, Weiss MN, Cant MA, Domenici P, Balcomb KC, Ellifrit DK, Croft DP (2021). Mixture models as a method for comparative sociality: social networks and demographic change in resident killer whales. Behavioral Ecology and Sociobiology, 75(4) 
URL http://github.com/samellisq/Ellisetal2021_BehavEcolSoc_AnonymisedData
 
Title Patterns and consequences of age-linked change in local relatedness in animal societies 
Description The ultimate payoff of behaviours depends not only on their direct impact on an individual, but also on the impact on their relatives. Local relatedness-the average relatedness of an individual to their social environment-therefore has profound effects on social and life history evolution. Recent work has begun to show that local relatedness has the potential to change systematically over an individual's lifetime, a process called kinship dynamics. However, it is unclear how general these kinship dynamics are, whether they are predictable in real systems and their effects on behaviour and life history evolution. In this study, we combine modelling with data from real systems to explore the extent and impact of kinship dynamics. We use data from seven group-living mammals with diverse social and mating systems to demonstrate not only that kinship dynamics occur in animal systems, but also that the direction and magnitude of kinship dynamics can be accurately predicted using a simple model. We use a theoretical model to demonstrate that kinship dynamics can profoundly affect lifetime patterns of behaviour and can drive sex differences in helping and harming behaviour across the lifespan in social species. Taken together, this work demonstrates that kinship dynamics are likely to be a fundamental dimension of social evolution, especially when considering age-linked changes and sex differences in behaviour and life history. 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
Impact Ellis, S., Johnstone, R.A., Cant, M.A. et al. Patterns and consequences of age-linked change in local relatedness in animal societies. Nat Ecol Evol 6, 1766-1776 (2022). 
URL https://doi.org/10.17605/OSF.IO/PZFEX
 
Title Postreproductive female killer whales reduce socially inflicted injuries in their male offspring 
Description R code and data necessary to reproduce all analyses from the manuscript "Postreproductive female killer whales reduce socially inflicted injuries in their male offspring". 
Type Of Material Database/Collection of data 
Year Produced 2023 
Provided To Others? Yes  
Impact Grimes, C., Brent, L. J., Ellis, S., Weiss, M. N., Franks, D. W., Ellifrit, D. K., & Croft, D. P. (2023). Postreproductive female killer whales reduce socially inflicted injuries in their male offspring. Current Biology, 33(15), 3250-3256.e4. https://doi.org/10.1016/j.cub.2023.06.039 
URL https://zenodo.org/deposit/8026912
 
Title Temporal dynamics of mother-offspring relationships in Bigg's killer whales: opportunities for kin-directed help by post-reproductive females 
Description Age-related changes in the patterns of local relatedness (kinship dynamics) can be a significant selective force for 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 the costs of reproductive conflict and the 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 >40 years of demographic data to investigate the opportunities for helping and harming in the mammal-eating Bigg's killer whale by quantifying how mother-offspring social relationships change with offspring age. 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 of particularly adult sons, while partly mitigating the costs of mother-daughter reproductive conflict. This is an important step towards understanding the evolution of menopause in the few species it occurs. 
Type Of Material Database/Collection of data 
Year Produced 2023 
Provided To Others? Yes  
URL https://datadryad.org/stash/dataset/doi:10.5061/dryad.n02v6wx25
 
Description Center for Whale Research 
Organisation Center for Whale Research
Country United States 
Sector Charity/Non Profit 
PI Contribution The Center for Whale Research has benefited from the research through detailed analysis of its long-term datasets in particular gaining new insight into factors relating to the survival and reproductive success of the critically endangered Southern Resident Killer whales.
Collaborator Contribution This research has been supported by the Center for Whale Research in the USA
Impact This collaboration has resulted in multiple co-authored outputs and public engagement events.
Start Year 2008
 
Description Press release 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact we submitted a press release for this paper https://www.sciencedirect.com/science/article/pii/S0960982222019947?via%3Dihub

the work was covered by 300 news outlets, 8 blogs, 323 X users and 5 Facebook pages
Year(s) Of Engagement Activity 2023
URL https://news.exeter.ac.uk/research/killer-whale-mums-pay-high-price-for-raising-sons/
 
Description Workshop talk 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact A research talk was given for a public event on whales and dolphins followed by a panel discussion. The event sparked interest from the general public and government agencies in the interactions between prey abundance and mortality rates in killer whales.
Year(s) Of Engagement Activity 2024
 
Description press release 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact We released a press release about this research article https://www.sciencedirect.com/science/article/pii/S0960982223008242?via%3Dihub

the work was covered by, 279 news outlets, 6 blogs, 499 X users, 1 Facebook page and 1 Youtube creator
Year(s) Of Engagement Activity 2023
URL https://news.exeter.ac.uk/research/male-killer-whales-protected-by-post-menopause-mothers/