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.
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.
People |
ORCID iD |
Michael Cant (Principal Investigator) | |
Andrew Young (Co-Investigator) |
Publications
Blount JD
(2016)
Oxidative shielding and the cost of reproduction.
in Biological reviews of the Cambridge Philosophical Society
Brent LJN
(2015)
Ecological knowledge, leadership, and the evolution of menopause in killer whales.
in Current biology : CB
Croft DP
(2015)
The evolution of prolonged life after reproduction.
in Trends in ecology & evolution
Inzani E
(2019)
Spontaneous abortion as a response to reproductive conflict in the banded mongoose.
in Biology letters
Inzani EL
(2016)
Female reproductive competition explains variation in prenatal investment in wild banded mongooses.
in Scientific reports
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
Khera M
(2021)
Cooperatively breeding banded mongooses do not avoid inbreeding through familiarity-based kin recognition
in Behavioral Ecology and Sociobiology
Kuijper B
(2019)
Developing differences: early-life effects and evolutionary medicine.
in Philosophical transactions of the Royal Society of London. Series B, Biological sciences
Marshall H
(2016)
Variable ecological conditions promote male helping by changing banded mongoose group composition
in Behavioral Ecology
Marshall HH
(2018)
Data collection and storage in long-term ecological and evolutionary studies: The Mongoose 2000 system.
in PloS one
Marshall HH
(2019)
Stable isotopes are quantitative indicators of trophic niche.
in Ecology letters
Marshall HH
(2017)
Lifetime fitness consequences of early-life ecological hardship in a wild mammal population.
in Ecology and evolution
Mitchell J
(2017)
Pregnancy is detected via odour in a wild cooperative breeder.
in Biology letters
Mitchell J
(2016)
Heterozygosity but not inbreeding coefficient predicts parasite burdens in the banded mongoose
in Journal of Zoology
Nichols HJ
(2014)
Evidence for frequent incest in a cooperatively breeding mammal.
in Biology letters
Nichols HJ
(2015)
Adjustment of costly extra-group paternity according to inbreeding risk in a cooperative mammal.
in Behavioral ecology : official journal of the International Society for Behavioral Ecology
Nichols HJ
(2021)
A double pedigree reveals genetic but not cultural inheritance of cooperative personalities in wild banded mongooses.
in Ecology letters
Sanderson J
(2014)
Hormonal mediation of a carry-over effect in a wild cooperative mammal
in Functional Ecology
Sanderson J
(2015)
The origins of consistent individual differences in cooperation in wild banded mongooses, Mungos mungo
in Animal Behaviour
Sanderson JL
(2015)
Banded mongooses avoid inbreeding when mating with members of the same natal group.
in Molecular ecology
Sanderson JL
(2015)
Elevated glucocorticoid concentrations during gestation predict reduced reproductive success in subordinate female banded mongooses.
in Biology letters
Scott K
(2017)
Group size and visitor numbers predict faecal glucocorticoid concentrations in zoo meerkats.
in Royal Society open science
Shelafoe C
(2023)
Caregiver's cognitive traits are associated with pup fitness in a cooperatively breeding mammal
in Scientific Reports
Sheppard C
(2021)
Individual foraging specialization in group-living species
in Animal Behaviour
Sheppard CE
(2018)
Decoupling of Genetic and Cultural Inheritance in a Wild Mammal.
in Current biology : CB
Sheppard CE
(2018)
Intragroup competition predicts individual foraging specialisation in a group-living mammal.
in Ecology letters
Thompson F
(2017)
Individual and demographic consequences of mass eviction in cooperative banded mongooses
in Animal Behaviour
Thompson F
(2017)
Causes and consequences of intergroup conflict in cooperative banded mongooses
in Animal Behaviour
Thompson FJ
(2016)
Reproductive competition triggers mass eviction in cooperative banded mongooses.
in Proceedings. Biological sciences
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
Vitikainen E
(2016)
Evidence of Oxidative Shielding of Offspring in a Wild Mammal
in Frontiers in Ecology and Evolution
Vitikainen E
(2017)
Biased escorts: offspring sex, not relatedness explains alloparental care patterns in a cooperative breeder
in Proceedings of the Royal Society B: Biological Sciences
Vitikainen EIK
(2019)
Live long and prosper: durable benefits of early-life care in banded mongooses.
in Philosophical transactions of the Royal Society of London. Series B, Biological sciences
Wells D
(2021)
Extra-group paternity varies with proxies of relatedness in a social mammal with high inbreeding risk
in Behavioral Ecology
Wells DA
(2020)
Inbreeding depresses altruism in a cooperative society.
in Ecology letters
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 from: Banded mongooses avoid inbreeding when mating with members of the same natal group |
Description | Inbreeding and inbreeding avoidance are key factors in the evolution of animal societies, influencing dispersal and reproductive strategies which can affect relatedness structure and helping behaviours. In cooperative breeding systems, individuals typically avoid inbreeding through reproductive restraint and/or dispersing to breed outside their natal group. However, where groups contain multiple potential mates of varying relatedness, strategies of kin recognition and mate choice may be favoured. Here, we investigate male mate choice and female control of paternity in the banded mongoose (Mungos mungo), a cooperatively breeding mammal where both sexes are often philopatric and mating between relatives is known to occur. We find evidence suggestive of inbreeding depression in banded mongooses, indicating a benefit to avoiding breeding with relatives. Successfully breeding pairs were less related than expected under random mating, which appeared to be driven by both male choice and female control of paternity. Male banded mongooses actively guard females to gain access to mating opportunities, and this guarding behaviour is preferentially directed towards less closely related females. Guard-female relatedness did not affect the guard's probability of gaining reproductive success. However, where mate-guards are unsuccessful, they lose paternity to males that are less related to the females than themselves. Together, our results suggest that both sexes of banded mongoose use kin discrimination to avoid inbreeding. Although this strategy appears to be rare among cooperative breeders, it may be more prominent in species where relatedness to potential mates is variable, and/or where opportunities for dispersal and mating outside of the group are limited. |
Type Of Material | Database/Collection of data |
Year Produced | 2015 |
Provided To Others? | Yes |
URL | https://datadryad.org/stash/dataset/doi:10.5061/dryad.gc371 |
Title | Data from: Reproductive competition triggers mass eviction in cooperative banded mongooses |
Description | In many vertebrate societies, forced eviction of group members is an important determinant of population structure, but little is known about what triggers eviction. Three main explanations are (1) the reproductive competition hypothesis; (2) the coercion of cooperation hypothesis; and (3) the adaptive forced dispersal hypothesis. The last hypothesis proposes that dominant individuals use eviction as an adaptive strategy to propagate copies of their alleles through a highly structured population. We tested these hypotheses as explanations for eviction in cooperatively breeding banded mongooses (Mungos mungo), using a 16-year dataset on life history, behaviour and relatedness. In this species, groups of females, or mixed-sex groups, are periodically evicted en masse. Our evidence suggests that reproductive competition is the main ultimate trigger for eviction for both sexes. We find little evidence that mass eviction is used to coerce helping, or as a mechanism to force dispersal of relatives into the population. Eviction of females changes the landscape of reproductive competition for remaining males, which may explain why males are evicted alongside females. Our results show that the consequences of resolving within-group conflict resonate through groups and populations to affect population structure, with important implications for social evolution. |
Type Of Material | Database/Collection of data |
Year Produced | 2016 |
Provided To Others? | Yes |
URL | https://datadryad.org/stash/dataset/doi:10.5061/dryad.8c26b |
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 |