Adaptive suppression of subordinate reproduction in cooperative mammals

Lead Research Organisation: University of Cambridge
Department Name: Zoology


In many animals that breed cooperatively, one dominant female in each group effectively monopolises reproduction and other females help to rear her offspring. However, in most animal societies, subordinate females sometimes breed and, in a few species, most mature females breed regularly. Understanding the reasons for these contrasts and the behavioural and physiological mechanisms controlling the distribution of reproduction among females and the degree of reproductive skew is of central importance in explaining the evolution of cooperation, the reproductive strategies of individuals and the population dynamics of cooperative breeders. However, although variation in reproductive skew has been the focus of considerable research in behavioural ecology for more than twenty years, it has not yet been possible to account for the distribution of subordinate breeding either between or within species. Previous attempts to explain the frequency of breeding by subordinates have either assumed that subordinate females breed where dominant females grant them reproductive concessions to ensure that they remain in the group and assist in rearing their offspring or that subordinates breed where dominants are incapable of preventing them from conceiving or rearing young. An alternative possibility, which has received relatively little attention, is that suppressing or evicting subordinate females has substantial costs to the fitness of dominants (partly because subordinate females are commonly their daughters or sisters and partly because the breeding success of dominants depends on the number of resident helpers) and that differences in the frequency of subordinate breeding are a consequence of variation in the net benefits of suppressing subordinates to dominants. While some correlational evidence suggests that this may be the case, no studies have yet measured the costs of subordinate breeding to dominant females or have determined whether variation in the net benefits of suppressing subordinates affects the frequency with which subordinates breed or are evicted from the group by dominants. By far the best way to investigate the ultimate and proximate mechanisms controlling reproductive skew is to manipulate the frequency of breeding by subordinates and dominants and to determine how this affects the breeding success of dominants and their treatment of subordinates. Drawing on an existing study population of Kalahari meerkats Suricta suricatta, where all individuals are recognisable and detailed records of individual differences in growth and breeding success are available for multiple groups over fifteen years, we shall use a combination of quantitative comparisons and experiments manipulating the frequency of reproduction by subordinates and dominants, to (1) measure the costs of subordinate breeding to dominants (2) determine whether variation in the net benefits of suppressing subordinates to dominants affects the extent to which they tolerate subordinates (3) determine whether dominants monitor the growth of subordinates and selectively evict likely challengers from the group (4) determine whether dominants attempt to influence the identity of their likely successors (5) develop generalised game-theory models that can be used to predict the extent to which dominants tolerate subordinates, the degree of reproductive skew and the size and structure of groups in other social vertebrates.


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Description (1) That subordinate breeding in meerkats has substantial costs to the breeding success and growth of dominants.
(2) That dominants modify their tolerance of subordinate reproduction in response to likely costs to their own fitness.
(3) That dominants are more likely to evict subordinates that are not closely related to them from the group.
Exploitation Route Our findings provide insight into the extent to which dominant individuals control reproduction in subordinates - which is of relevance both to a fundamental understanding of animal breeding systems and to the management and conservation of social mammals.
Sectors Agriculture, Food and Drink,Environment

Description Our research on meerkats is widely referenced in research on organismal biology. The films about our work have attracted substantial attention and provided the general public with insight into the structure and function of animal societies. Our work has also formed the basis for collaborative research with members of staff at Duke, Gottingen, Zurich and Pretoria, and has helped to generate two major grants: one at Duke to investigate the effects of maternal testosterone levels on offspring development; one from the ERC to me to explore developmental aspects of variation in cooperative behaviour, worth around 2.5/million euros.
First Year Of Impact 2010
Sector Education,Environment
Impact Types Societal

Description Collaborator: Dr Johanna Nielsen 
Organisation University of Edinburgh
Country United Kingdom 
Sector Academic/University 
PI Contribution Provided data on reproduction, growth and kinship in meerkats
Collaborator Contribution Dr Nielsen has contributed the genetic analysis and the contribution of a pedigree.
Impact MULTI-DISCIPLINARY: Reproduction; Ecology; Genetics. Leclaire, S., Nielsen, J.F., Sharp, S.P., and Clutton-Brock, T.H. (2013) Mating strategies in dominant meerkats: evidence for extra-pair paternity in relation to genetic relatedness between pair mates. Journal of Evolutionary Biology doi: 10.1111/jeb.12151. MacLeod, K.J., Nielsen, J.F. and Clutton-Brock, T.H. (2013) Factors predicting the frequency, likelihood and duration of allonursing in the cooperatively breeding meerkat. Animal Behaviour doi: org/10.1016/j.anbehav.2013.09.012. English, S., Huchard, E., Nielsen, J.F. and Clutton-Brock, T.H. (2013) Early growth, dominance acquisition and lifetime reproductive success in male and female cooperative meerkats. Ecology and Evolution 3: 4401-4407.
Start Year 2011
Description Collaborator: Professor Christine Drea 
Organisation Duke University
Department Evolutionary Anthropology
Country United States 
Sector Academic/University 
PI Contribution We have assisted Professor Drea in investigating the organisational effects of maternal testosterone in meerkats.
Collaborator Contribution Professor Drea has employed an assistant who has worked with us in the Kalahari, extending the number of groups we have been able to sample.
Impact MULTI-DISCIPLINARY: Behaviour; Endocrinology.
Start Year 2011
Description Collaborator: Professor Marta Manser 
Organisation University of Zurich
Department Institute of Evolutionary Biology and Environmental Studies
Country Switzerland 
Sector Academic/University 
PI Contribution We have provided Professor Manser's team with access to habituated animals and to long-term, individual-based data.
Collaborator Contribution Professor Manser's team has explored the communication system of meerkats, extending the range of research that we are involved in.
Impact MULTI-DISCIPLINARY: Endocrinology; Behaviour. Santema, P., Teitel, Z., Manser, M., Bennett, N. and Clutton-Brock, T. (2013) Effects of cortisol administration on cooperative behavior in meerkats. Behavioral Ecology. doi: 10.1093/beheco/art039. Zöttl, M., Lienert, R., Clutton-Brock, T., Millesi, E. and Manser, M. B. (2013) The effects of recruitment to direct predator cues on predator responses in meerkats. Behavioral Ecology 24: 198-204.
Start Year 2011
Description Documentary films 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Two documentaries on our work by Discovery and National Geographic

Regular interest in animal societies and meerkats in particular by other scientists/television researchers/general public.
Year(s) Of Engagement Activity 2012,2013