Social influences on aging in a wild cooperative mammal

Lead Research Organisation: University of Exeter
Department Name: Biosciences

Abstract

A key goal of research in biological and medical science is to understand why some individuals in a population remain healthy into old age, whereas others decline rapidly and die early. Research on model laboratory organisms such as fruit flies and mice suggests that the rate of decline in bodily function with age, or the rate of senescence, will depend on how individuals allocate resources to survival versus reproduction across the lifespan, and on the quantity and quality of resources available during growth and development. In highly social or cooperative animals, both these factors are strongly dependent on an individual's social status and its interactions with other group members. Our research will test for the first time the influence of these social factors on rates of aging and physiological senescence in a highly social, mammal, the banded mongoose, using a combination of long-term data analysis, behavioural experiments and physiological measures of senescence. Specifically we will address questions: (1) how does variation in individual attributes and social factors (such as helping effort, dominance status, and group structure) influence rates of aging in males and females; (2) how do these factors influence measured levels of oxidative stress, a suggested marker of physiological senescence; and (3) how does variation in social investment received during development influence adult survival and condition? We will address the last question using a large-scale field experiment in which we provision pups with nutrients for growth or with antioxidants to test for downstream effects on adult condition, reproductive performance, and levels of oxidative stress. The research will generate important new information on the main factors influencing variation and mortality and fertility in natural populations of social vertebrates, and how natural selection shapes the evolution of life history in long-lived animals living in close-knit family groups, including, potentially, ancestral humans. In addition, our work will provide the first test of mechanistic explanations of senescence in a natural mammal population, and the first experimental test of early-life effects on adult fitness traits. These investigations promise to advance our understanding of the evolutionary processes and proximate causes of aging.

Publications

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Cant MA (2011) The role of threats in animal cooperation. in Proceedings. Biological sciences

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Johnstone RA (2010) The evolution of menopause in cetaceans and humans: the role of demography. in Proceedings. Biological sciences

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Müller CA (2010) Imitation and traditions in wild banded mongooses. in Current biology : CB

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Thompson FJ (2017) Explaining negative kin discrimination in a cooperative mammal society. in Proceedings of the National Academy of Sciences of the United States of America

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Vitikainen E (2016) Evidence of Oxidative Shielding of Offspring in a Wild Mammal in Frontiers in Ecology and Evolution

 
Description We carried out a comprehensive test of the oxidative stress theory of aging in our long-term banded mongoose system. We discovered that, unusually for mammals, males live longer than females in this system. We showed that high levels of one measure of oxidative stress, MDA, was associated with increased mortality in both males and females. A surprising finding, discovered using longitudinal blood sampling, is that pregnant females exhibit lower levels of MDA than before or after gestation. This led us to carry out a meta-analysis of the published literature which shows that breeding females across a range of species show reduced, rather than elevated, levels of oxidative damage during pregnancy. We proposed the 'oxidative shielding' hypothesis to account for these otherwise puzzling results- females may gain from reducing oxidative damage when pregnant to protect their unborn offspring from transgenerational damage. This hypothesis has receved much attention since its publication in 2016 ( 100 citations to date, March 2020).

In addition we are carrying out sophisticated survival analysis on our long-term data to test the causes of sex differences in longevity in this species. This employs cutting-edge statistical techniques to test a novel hypothesis concerning the role of the social environment in ageing, namely, that males live longer than females in this species because males for a 'social queue' to inherit breeding status. We expect the results of these analyses to emerge soon and to have a major impact on our understanding of aging in wild animal populations.
Exploitation Route Our oxidative shielding has already stimulated discussion and some tests in wild and lab systems.
Sectors Education,Environment,Other

URL http://socialisresearch.org
 
Description The findings from this grant have contributed to the development of a new theoretical model to explain life history allocation across the lifespan in long-lived species. This theory may help to explain inconsistent patterns in previous tests of the oxidative stress theory of aging. Our research on banded mongooses suggests that mothers 'shield' their offspring during pregnancy by upregulating defense against oxidative damage. We argue that a transgenerational model is needed to understand individual variation in oxidative damage and survival in mammals, including humans. This work will be of high impact with potential biomedical implications. We have has a proposal for a special edition of Phil Trans accepted, which draws together 30+ world leading academics, both medics and evolutinary biologists to write a special interdisciplinary edition on the evolution of early life effects and their relevance to medicne.
First Year Of Impact 2017
Sector Environment,Healthcare
Impact Types Societal,Policy & public services

 
Description European Research Council Consolidator's Grant
Amount € 1,500,000 (EUR)
Organisation European Research Council (ERC) 
Sector Public
Country Belgium
Start 01/2013 
End 12/2017
 
Title Banded mongoose long term database 
Description A continuous database of behaviour and life history of the banded mongoose population since 1995. This will be deposited with NERC within the next three months. It provides valuable demographic and life history information about schedules of growth, fertility, survival and dispersal in a wild mammal population stretching over 6 generational lengths. 
Type Of Material Database/Collection of data 
Provided To Others? No  
Impact The creation and maintenance of this database allows very powerful analyses of social influences on health and life history in wild mammals. It formed the foundation for my successful ERC grant application in 2012, and underpins research on early life influences on cooperation, the topic of my current NERC grant. 
 
Description Endocrinology of development and health in wild mammals 
Organisation Chester Zoo
Department Endocrinology Unit
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution The collaboration involves the provision of blood samples from the long-term banded mongoose project for hormone analysis at the Endocrinological Unit of Chester Zoo. This has enabled us to gain important new insight into the development of hormonal responses in wild mammals, and set the stage for two successful grant applications (NERC and ERC).
Collaborator Contribution Our collaborators there developed and validated assays to measure levels of cortisol, faecal glucocorticoids, testosterone, progesterone and oestrogen.
Impact Demonstrated safe and effect use of widely available contraceptives to safely control reproduction in wild mammals. This information will likely be useful to guide captive breeding and conservation programmes in future.
Start Year 2011