Early-life influences on the development of cooperation in wild mammals

Lead Research Organisation: University of Exeter
Department Name: Biosciences

Abstract

Cooperative animal societies, in which adults help to rear offspring that are not their own, have been the focus of intense research because they can help to understand how cooperation can evolve in the face of natural selection for self-interest. However, this research has also revealed great unexplained variation between individuals in how much they contribute to teamwork and how much effort they invest in rearing offspring. A plausible explanation for this variation comes from research on laboratory animals showing that early life conditions have lifelong impacts on adult health and behaviour, suggesting that differences in helping effort among adults could be attributable to variation in their early life developmental experiences and nutrition. Our research will test this hypothesis using our long-term habituated study population of banded mongooses, a highly cooperative mammal which lives in mixed-sex groups of around twenty individuals throughout sub-Saharan Africa. This species is ideal for the task because there is extreme variation among individual group members in how much they contribute to raising communal litters of offspring, and extreme variation among offspring in how much care and food they receive from adults. We have built up a detailed database on the behaviour and reproductive success of over 2200 individuals which enables us to test the lifetime consequences of this variation in early life care, and we can carry out feeding experiments to test whether maternal nutrition during pregnancy has lifelong impacts on their offspring. We will also measure the underlying hormonal mechanisms which control cooperative behaviour, and test how sensitive these hormonal mechanisms are to early life experiences and maternal nutrition in utero. The output of the research will be an improved understanding of the causes of individual variation in cooperative behaviour, and improved knowledge of mammalian development in populations exposed to natural predators and pathogens.

Planned Impact

The British public has an extremely strong standing interest in natural history, a cultural tradition that has undoubtedly contributed to the extraordinary contributions to biology made by UK science. Our previous work on this species has capitalised on this interest and generated a great deal of media attention, resulting in a prime-time BBC2 TV Series which attracted an audience of over 1.5 million in the UK, and over 20 million worldwide. At the time of writing the BBC are planning to revisit the study population at the end of 2011/2012 for follow up filming; and we are negotiating with a second media production company about a 3D feature film on the mongooses. The PI will build on his existing contacts with the BBC and other media companies to take full advantage of the charismatic nature of the study species and the opportunities or educational outreach that it presents. The proposed research project focuses on a question which is also of inherent interest to the public - how early life experiences affect behaviour, stress, and health in later life providing opportunities to reach a very broad audience to communicate the value of contemporary scientific research on animals in their natural environment, and the value of the natural environment itself. It is not possible to guarantee media contracts at this stage of the application, but based on our past experience we are confident that the proposed research will lead to considerable TV, print and online media coverage. Outreach will be further aided by the technical upgrade to our existing website www.bandedmongoose.org.
A second group of beneficiaries are conservation and wildlife managers aiming to predict the individual, group, and population responses of cooperative mammals to changes in resource availability and climate. Many iconic and conservation priority species (e.g. lions, African wild dogs, Ethiopian wolves, callitrichid primates) are facultative cooperative breeders in which there exist minimum viable group sizes for successful reproduction. These species are inherently susceptible to destabilizing population dynamic forces (e.g. Allee effects) which have been explored theoretically but about which there is little information from wild systems. The proposed research will help to reveal the short and long-term effects of supplementary feeding for levels of cooperation and group productivity, which may help guide intervention for rarer, more elusive cooperatively breeding mammals that are much harder to study. Although population dynamics is not a focus of the current research, we see our results as having potential future impact by laying the groundwork for follow-up research on population responses arising from developmental responses to nutritional stress or the quality of cooperative rearing environments.
Finally, our research will have an impact in raising awareness about the value of the natural environment locally in Uganda, and more broadly among international tourist visitors to Queen Elizabeth National Park. We will set up an 'Experiential Tourism' project whereby tourists will spend a morning out with the mongooses accompanied by Park Rangers, with proceeds going to UWA and its efforts at conservation in Uganda. We will also visit local schools thrice-yearly to give seminars and to raise awareness about the intrinsic value of biodiversity and wildlife in Uganda's protected areas. This is a critically important component of the study because there is very high levels of human-wildlife conflict in QENP.

Publications

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Blount JD (2016) Oxidative shielding and the cost of reproduction. in Biological reviews of the Cambridge Philosophical Society

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Croft DP (2015) The evolution of prolonged life after reproduction. in Trends in ecology & evolution

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Johnstone RA (2020) Exploitative leaders incite intergroup warfare in a social mammal. in Proceedings of the National Academy of Sciences of the United States of America

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Kuijper B (2019) Developing differences: early-life effects and evolutionary medicine. in Philosophical transactions of the Royal Society of London. Series B, Biological sciences

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Kuijper B (2019) Developing differences: early-life effects and evolutionary medicine. in Philosophical transactions of the Royal Society of London. Series B, Biological sciences

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Marshall HH (2016) Variable ecological conditions promote male helping by changing banded mongoose group composition. in Behavioral ecology : official journal of the International Society for Behavioral Ecology

 
Description We are currently exploring the impact of maternal nutrition and stress of future offspring development, hormonal state, and cooperation. We started the experiments in April 2013 and these are running as planned. All procedures are in place to begin analysing data from mid-2015. In the interim we have published a paper this year utilising our new hormonal assays, developed for this project.

In the course of this research we have developed a new genetic pedigree which has opened up new avenues of research into the environmental and social determinants of helping behaviour and life history. This was an original objective, but the new research was unanticipated. We have published or submitted new papers showing that long-term environmental variability can have life-long impacts on banded mongoose health and fitness. This research has potential medical implications, and is suitable for a wide interdisciplinary audience.

We continue (as of 2019) to produce important papers and collaborations from this grant. In particular in February 2019 we edited and published a special issue of Philosophical Transactions of the Royal Society which collated and synthesised research on early life effects from evolutionary biology and medicine. Our hope is that this issue will stimulate further cross-disciplinary research on how conditions experienced during development shape patterns of health and disease in natural populations of human and non-human organisms.
Exploitation Route This is work in progress.
Sectors Environment,Healthcare

URL http://socialisresearch.org
 
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 Hormonal assays for glucocorticoids, testosterone, progesterone, oestrogen 
Description In collaboration with the Endocrinology Unit of Chester Zoo, we have developed assays to measure concentrations of cortisol, testosterone, progesterone, and oestrogen in samples of faeces and blood of banded mongooses. 
Type Of Material Technology assay or reagent 
Provided To Others? No  
Impact This underpins the objectives of our research relating to hormonal mechanisms underpinning social behaviour 
 
Title Molecular genetic pedigree 
Description We have successfully developed a full molecular genetic pedigree for all the individuals in our long-term study population of wild banded mongooses in Uganda. This generation gives information on paternity and maternity with >95% confidence up to 9 generations deep. 
Type Of Material Model of mechanisms or symptoms - mammalian in vivo 
Year Produced 2015 
Provided To Others? Yes  
Impact This pedigree underpins many of the current and future research projects on this population 
 
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. 
 
Title Data supporting Johnstone, Cant, Cram & Thompson (2020) Exploitative leaders incite intergroup warfare in a social mammal 
Description This data supports the following publication:
Rufus A. Johnstone, Michael A. Cant, Dominic L. Cram & Faye J. Thompson (2020) Exploitative leaders incite intergroup warfare in a social mammal. Proceedings of the National Academy of Sciences.
Please read the "Read Me.txt" file for a full description of the data contained in each data set 
Type Of Material Database/Collection of data 
Year Produced 2020 
Provided To Others? Yes  
URL https://figshare.com/articles/dataset/Data_supporting_Johnstone_Cant_Cram_Thompson_2020_Exploitative...
 
Title Data supporting Johnstone, Cant, Cram & Thompson (2020) Exploitative leaders incite intergroup warfare in a social mammal 
Description This data supports the following publication:
Rufus A. Johnstone, Michael A. Cant, Dominic L. Cram & Faye J. Thompson (2020) Exploitative leaders incite intergroup warfare in a social mammal. Proceedings of the National Academy of Sciences.
Please read the "Read Me.txt" file for a full description of the data contained in each data set 
Type Of Material Database/Collection of data 
Year Produced 2020 
Provided To Others? Yes  
URL https://figshare.com/articles/dataset/Data_supporting_Johnstone_Cant_Cram_Thompson_2020_Exploitative...
 
Title Unstandardized breeding choice grouped by maternal litter 
Description Banded mongooses play a delicate balancing act between incest and warfare. Some females have to choose between mating with a relative within their own social group or trying to sneakily mate with a male from a rival group during fights between groups. We show that females are more likely to mate with extra-group males when the risk of inbreeding within their group is high, but not all females get this opportunity for extra-group mating. 
Type Of Material Database/Collection of data 
Year Produced 2020 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.s4mw6m953
 
Description Mongoose genetics 
Organisation Liverpool John Moores University
Country United Kingdom 
Sector Academic/University 
PI Contribution We provide all tissue and blood samples for genetic analysis of parentage. We also provide the long term life history database, and collaborate on a range of publications investigating the genetic population structure of our field population.
Collaborator Contribution Developed microsatellite library for analysis of parentage. Currently working on construction of a full genetic pedigree, which will open up new lines of research.
Impact Numerous papers co-authored with HJ Nichols have investigated the genetic structure of the population, reproductive success, and inbreeding.
Start Year 2007
 
Description Early life effects workshop (Falmouth, September 2015) 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact We held a workshop for 25 world-leading researchers working on the early life developmental effects in medicine and evolutionary biology. The aim was to stimulate a dialogue between evolutionary and medical fields. The anticpated output is a review volume that we will invite attendees to contribute to.
Year(s) Of Engagement Activity 2015
URL http://biosciences.exeter.ac.uk/earlylife/
 
Description Schools outreach 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Schools
Results and Impact Outreach to schools in Uganda and UK. Communicate results of the long-term research to improve young students understanding of science and the importance of biodiversity for economic and environmental sustainability

After these outreach classes (1 school in the UK, 5 in Uganda) pupils were encouraged to follow up using exercising in a children's book 'Billy the Banded Mongoose', written by a member of our team and available for sale via Amazon.
Year(s) Of Engagement Activity 2013,2014
URL http://billythebandedmongoose.co.uk