Female kin as allies and adversaries under social competition

Lead Research Organisation: University of Liverpool
Department Name: Institute of Integrative Biology

Abstract

Animals living in groups must compete for limited resources but can also be highly cooperative in their interactions. Explaining the balance between competition and cooperation is crucial to understanding social behaviour in diverse species from microbes to humans. Although theory of very broad significance provides testable predictions to explain variation in cooperative and competitive behaviours, experimental studies addressing these are currently lacking for vertebrates with typically flexible social behaviour. This project will provide novel experimental tests to determine how the social environment affects cooperative and competitive behaviour in wild house mice.

Relatedness between interacting individuals is thought to be a key predictor of cooperative and competitive behaviour. If competing individuals are able to recognise their relatives, interactions with kin should be more cooperative because by helping a close relative to reproduce, an individual is still passing on some genes to the next generation indirectly. Importantly though, where competition for limited resources is intense between kin, this may reduce or even negate the benefits of cooperating. These underlying principles for understanding patterns of behaviour are particularly relevant to social vertebrates such as mammals, where related members of one sex typically stay in the social group where they were born rather than disperse. However these key general principles have proved difficult to test experimentally, in part due to limited information regarding kin recognition ability of focal species. Our latest research has identified mechanisms used by female house mice to recognise their relatives. Building on this important advance, we now propose to test for predicted responses to reproductive competition within and between female kin groups.

We will manipulate the complex social environment of wild house mice under carefully controlled naturalistic conditions. Our experiments are designed to disentangle effects of competition both within and between kin groups and social groups, and will allow us to assess how responses to social competition are mediated under different conditions. We will quantify and compare the affiliative, cooperative and aggressive behaviour of female mice under contrasting conditions of relatedness of competitors and intensity of competition. Oxytocin (OT) is a peptide hormone and neurotransmitter that is currently receiving very wide attention for its important role in the regulation of social behaviour. We will test for influences of social competition on female OT profiles linked to behaviour, and for evidence that OT facilitates intergenerational transmission of cooperative behaviour among kin via communal rearing of young. We will also quantify variation in female reproductive success under contrasting levels of social competition, and test if reproductive suppression of young females in response to a known chemical cue is dependent on relatedness of competitors in their social environment.

Understanding the conditions and mechanisms that promote social tolerance, aggression and reproductive suppression in mammals has very broad potential applications. As well as beneficiaries in diverse academic fields (evolutionary biology, behavioural ecology, population biology, psychology, anthropology, neurobiology), the work has important potential economical and societal applications. Understanding the factors that promote social tolerance or trigger aggression is of particular significance for users who manage animals, whether wild, laboratory or livestock. These include those managing or breeding endangered animals for conservation purposes, using animals in research, and in the farming industry. The study of olfactory cues used in reproductive suppression of wild house mice is also of direct relevance to long-term development of new methods of rodent pest control, of fundamental significance to global food security.

Planned Impact

The proposed research has fundamental implications for understanding variation in the social behaviour of vertebrate animals. This offers broad potential economical and societal impacts over both short and long-term timescales. Understanding the factors that promote social tolerance or trigger aggression is of particular significance for users who manage animals, whether wild, laboratory or livestock - for example those managing or breeding endangered animals for conservation purposes (conservationists, zoological curators), using animals in research and testing (animal care staff, researchers), and associated regulators and animal welfare advisors (Home office inspectorate, NC3Rs, RSPCA, UFAW), and those involved with the farming industry (farmers, veterinary surgeons, animal breeding industry). Understanding social, environmental and developmental influences on aggression and the maintenance of social tolerance has broad relevance for: i) captive management and breeding of wild animals for conservation; ii) welfare of laboratory animals; iii) better understanding of unexplained variation among laboratory mice (e.g. in biomedical research) where the influences of social grouping on females are largely unknown; iv) management and breeding of livestock where there are problems in maintaining high reproductive performance and welfare; v) animal models of social cognition and behaviour used in biomedical research. In addition the study of olfactory cues used in reproductive suppression of wild house mice is of direct relevance to long-term development of new methods of pest control, of fundamental significance to global food security and to reducing rodent-borne zoonoses.

Quality of life will be enhanced by knowledge resulting from this research through education and increased public understanding of science. The subject area of the proposed research is likely to be of interest to school children studying fundamental aspects of animal behaviour. These users will benefit from a better understanding of both ultimate and proximate mediators of cooperative behaviour. More generally, the public benefit from interest in animal behaviour and evolution, as reflected by the popularity of media articles, TV documentaries and science journalism in these areas. Media interest in the findings of this project will thus enhance public understanding of broader issues relating to science and conservation issues.

The project will also provide career development for the PDRA, with training in transferable skills of communication and multidisciplinary research.
 
Description Significant new knowledge generated: Initial published results of our experimental studies demonstrate significant effects of early life social environment on adult competitive behaviours. Core findings regarding how competition affects cooperation, reproductive skew and reproductive success in communally breeding females are currently in preparation for publication. • New or improved research methods or skills developed: We have validated and tested non-invasive methods for quantifying peripheral oxytocin levels in wild house mice. The insights we have gained from testing these methods with rodent models can be applied to similar studies of social and parental behaviour in diverse taxa. • Summary information: The original aims and objectives of the grant have largely been met. To date 3 published outputs are linked to the project, with a further 5 (including core publications) in preparation. We have made new discoveries as to how the environment can influence social behaviour and how female reproductive success can be constrained by investment in competitive signalling. The team has engaged in multiple engagement activities, including KE with Chester Zoo and Cheshire Wildlife Trust, plus associated research placements. Interdisciplinary training provided during the project is now being applied both in the UK and internationally, via next destination positions of our team. The work has also received early recognition via international research talk invitations. • Important new research questions and applications opened up: Our initial findings have stimulated further successful grant applications (a further NERC standard research grant and a Knowledge Exchange voucher) and funded PhD studentships, including two CASE funded projects. We have established new scientific collaborations with conservation practitioners, with the aim of improving captive breeding success of endangered species. • Increased research capability linked to training: The project has provided unique interdisciplinary training for the PDRA and associated PhD students. This training is now being applied in a further research post by our PDRA, and has facilitated further training and research placements at a leading endocrinology laboratory for our PhD students. Two of our PhD students are now employed in applied conservation roles.
Exploitation Route The primary academic beneficiaries will be researchers in the fields of behavioural and evolutionary ecology, and more broadly, researchers in other fields with an interest in the role of oxytocin in mammalian social behaviour. For example, our initial findings can be applied to advance understanding of developmental and phenotypic plasticity, of benefit to predict how animals will respond to environmental change. Understanding social, environmental and developmental influences on aggression and the maintenance of social tolerance in vertebrate animals also has broad relevance for: i) captive management and breeding of wild animals for conservation; ii) welfare of laboratory animals; iii) management and breeding of livestock where there are problems in maintaining high reproductive performance and welfare; v) animal models of social cognition and behaviour used in biomedical research. Quality of life can also be enhanced by knowledge resulting from this research through benefits to increased public understanding of science.
Sectors Agriculture, Food and Drink,Education,Environment,Healthcare,Leisure Activities, including Sports, Recreation and Tourism

 
Description The methods we adapted for automated monitoring of small mammal behaviour led to a partnership with the North of England Zoological Society, supported by an Innovate UK AKT2I award . The project aimed to evaluate the innovative use of automated systems for monitoring animal behaviour and welfare within zoological collections. Specifically, with Business Partner Chester Zoo, we have investigated the use of radio-frequency identification (RFID) monitoring systems for automated data collection, ultimately supporting the Zoo's remit of preventing extinction. A custom-designed system was piloted, and a report has been produced: 'Towards the Use of RFID Systems to Monitor Behaviour and Welfare of Zoo Animals: An Evaluation of New and Innovative Approaches'.
First Year Of Impact 2023
Sector Environment,Culture, Heritage, Museums and Collections,Other
Impact Types Cultural,Societal,Economic

 
Description How is behaviour constrained within typical sex roles?
Amount £533,128 (GBP)
Funding ID NE/T001046/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 03/2020 
End 03/2023
 
Description Innovate UK AKT2I
Amount £22,372 (GBP)
Funding ID Project number 141 
Organisation Innovate UK 
Sector Public
Country United Kingdom
Start 12/2022 
End 02/2023
 
Description Knowledge Exchange and Impact Voucher - New approaches for faecal analysis in applied conservation
Amount £9,500 (GBP)
Organisation Research Councils UK (RCUK) 
Sector Public
Country United Kingdom
Start 10/2019 
End 07/2020
 
Description NERC ACCE DTP studentship
Amount £78,000 (GBP)
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 06/2017 
End 01/2021
 
Description NERC DTP CASE studentship
Amount £78,000 (GBP)
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 07/2015 
End 07/2019
 
Description NERC PhD studentship
Amount £78,000 (GBP)
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 10/2016 
End 04/2020
 
Description PhD studentship
Amount £60,000 (GBP)
Organisation University of Liverpool 
Sector Academic/University
Country United Kingdom
Start 09/2015 
End 09/2019
 
Title Data for: Fitness costs of female competition linked to resource defence and relatedness of competitors 
Description Female reproductive success is often limited by access to resources and this can lead to social competition both within and between kin groups. Theory predicts that both resource availability and relatedness should influence the fitness consequences of social competition. However, testing key predictions requires differentiating the effects of these two factors. Here we achieve this experimentally by manipulating the social environment of house mice, a facultative communal breeding species with known kin discrimination ability. Our results support the hypothesis that resource defence can be costly for females, potentially trading off against maternal investment. When competition for nest sites was more intense, subjects: 1) were more active during resting phases, 2) responded more strongly to simulated territory intrusions via competitive signalling, and 3) produced smaller weaned offspring. However, we found no evidence that the propensity for kin to cooperate was influenced by relatedness of rivals. Communal breeding between sisters occurred independently of the relatedness of competitors, and costs of competition with non-kin were not mitigated by greater inclusive fitness benefits. Rather, communally breeding sisters weaned fewer offspring when competing with unrelated females, indicating that competition with non-kin is more costly overall. Our findings thus demonstrate that social competition has fitness costs and that associating with kin is beneficial to avoid negative fitness consequences of competing with non-kin, in addition to more widely recognised kin-selected benefits. 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.j0zpc86h1
 
Description Chester Zoo 
Organisation Chester Zoo
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution Shared supervision of three PhD students (two CASE funded), Rhiannon Bolton, Rutendo Wazara, and Alice Clark, providing knowledge exchange to improve success of conservation breeding programmes.
Collaborator Contribution Training and access to facilities for conducting hormone assays.
Impact Results of two projects are in preparation for publication, and were presented by invitation at the annual international EAZA conference in Athens (Sept 18-22 2018). These included initial findings of a European-wide survey of African painted dog captive breeding success, and social welfare of captive Asian elephants . Results will be used to inform captive breeding guidelines. The collaboration is multidisciplinary, involving animal behaviour, endocrinology, and social science (for design of European-wide survey).
Start Year 2015
 
Description Genetics and Development of Cooperation 
Organisation University of Bern
Department Institute of Social and Preventive Medicine
Country Switzerland 
Sector Academic/University 
PI Contribution Two members of our team contributed to a workshop on the genetics and development of cooperation at Bern University in December 2016.
Collaborator Contribution Contributions to group discussions, poster presentations, and a group publication.
Impact Title: Genetics and developmental biology of cooperation Authors: Claudia Kasper, Maddalena Vierbuchen, Ulrich Ernst, Stefan Fischer, Reinder Radersma, Aura Raulo, Filipa Cunha-Saraiva, Min Wu, Kenyon Mobley & Barbara Taborsky Submitted to Molecular Ecology (3rd March 2017)
Start Year 2016
 
Description Amazed by Science Festival 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact As part of the 'Amazed by Science Festival' a member of our team helped with a "Meet the Scientist" event at Chester Zoo. This involved a number of teaching stations at the education centre at Chester Zoo. It was directed towards all ages and abilities, but was mainly attended by young families.
Year(s) Of Engagement Activity 2016
URL https://www.actforwildlife.org.uk/conservation-news/amazed-science-chester-zoo/
 
Description Bioinspire meeting 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Industry/Business
Results and Impact Stakeholders and fundraisers met to discuss progress in developing a new public attraction for showcasing research, within the theme of a 'Bio-inspiration Centre'. Plans for the development are progressing well.
Year(s) Of Engagement Activity 2015
URL http://www.newzoo.org.uk/projects/bio-inspire/
 
Description Collaboration workshop 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Professional Practitioners
Results and Impact Members of the Conservation and Research Team from Chester Zoo visited the University of Liverpool for a workshop to discuss new approaches for faecal analysis in applied conservation. The meeting resulted in a new research partnership supported by a successful bid for a KEI voucher.
Year(s) Of Engagement Activity 2019
URL https://twitter.com/ScienceatCZ/status/1233337691766390784
 
Description Connect! Symposium 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Conservation scholars, practitioners and academics came together at Chester Zoo for a two day workshop, including small group discussions and exercises focused on current conservation issues.
Year(s) Of Engagement Activity 2018
 
Description Meet a scientist speed dating event 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact 100+ school pupils from Liverpool inner-city schools attended, and asked questions about my current research.
Year(s) Of Engagement Activity 2018
URL http://www.farmurban.co.uk/wp-login.php?redirect_to=http%3A%2F%2Fwww.farmurban.co.uk%2F
 
Description New Directions in Conservation Science workshop 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact 80+ postgraduate students and a diverse range of conservation practitioners came together to discuss new directions for evidence based conservation
Year(s) Of Engagement Activity 2017
URL https://acce.shef.ac.uk/event/conservation-symposium-the-future-of-conservation-science/
 
Description Science Fair at Ness gardens 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact 2000+ members of the public attended a science fair at Ness Gardens, associated with the broadcast of Gardener's Question Time. We had a display about British small mammals, and discussed our research with members of the public.
Year(s) Of Engagement Activity 2018
URL https://blogandlog.wordpress.com/2017/09/20/science-fun-at-the-gardeners-question-time-anniversary-g...
 
Description Science Festival at Manchester Museum of Science and Industry 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact As part of a science festival a member of our team assisted at a science fair at Manchester Museum discussing the role of science in zoos.
Year(s) Of Engagement Activity 2016
URL http://www.manchestersciencefestival.com/our-story/about-manchester-science-festival/
 
Description Science Uncovered at Manchester Museum 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact An evening at the Science Uncovered event at Manchester Museum. Activities were focused in the Living Worlds section where a member of our team talked to visitors about research at Chester Zoo and the importance of hormonal analysis in conservation research. The first hour was directed towards A-level students and there was also a lot of interest from prospective interns and from academic partners from all over the North West.
Year(s) Of Engagement Activity 2016
URL http://www.nhm.ac.uk/visit/exhibitions/science-uncovered-2016.html