Periodic Reporting for period 4 - Group-Dynamics-TCB (Effects of group dynamics on selection, development and demography in cooperative vertebrates)
Periodo di rendicontazione: 2023-01-01 al 2024-12-31
In a small number of social mammals, including some primates, rodents and carnivores, a single dominant female virtually monopolises breeding in each group and is assisted in feeding and guarding her offspring by non-breeding ‘helpers’ of either or both sexes. In many of these species, dominant females actively attempt to prevent breeding by subordinates, often killing any young they produce and eventually evicting them from the group. In contrast to most other social mammals, subordinate females are often temporarily infertile and show signs of physiological suppression of reproduction. Other unusual characteristics of these species include ‘strategically’ variable growth rates that are adjusted to opportunities to breed and the likelihood of competition with other group members. However, it is not yet clear whether breeders and helpers also show divergent patterns of growth and development before acquiring their adult status, as they do in many social insects. In some mammals that breed cooperatively (including the social mole-rats) dominant breeding females are also unusually long-lived and, in captivity, can survive for up to thirty years or more while subordinate females have much shorter lifespans. These differences parallel contrasts between queens and workers in social insects and raise important questions about the mechanisms controlling rates of ageing in mammals. Finally, cooperative breeders are of interest because they represent the most advanced examples of cooperation in mammals, raising fundamental questions about the evolution of cooperation and competition, the hormonal mechanisms that control them and their consequences for population dynamics and demography that are relevant both to our general understanding of mammalian societies and to the origins and evolution of cooperation in humans.
This project focusses on studies of two mammalian cooperative breeders (Kalahari meerkats and Damaraland mole-rats) that provide unusual opportunities to explore the evolution of cooperative breeding and the mechanisms controlling reproductive suppression, development and cooperation. We have worked for the past twenty-five years on Kalahari meerkats (Suricata suricatta), a social desert-adapted mongoose, at a site in South Africa and have access to 10-15 wild groups of identifiable individuals whose development, reproduction and behaviour have been monitored since their birth. Since our study groups have been closely habituated to humans, we can collect regular data on their daily weight gain, growth and hormonal status of large samples of identifiable individuals of known age and breeding history. At the same site, we work on Damaraland mole-rats (Fukomys damarensis), a cooperative rodent that lives underground in the Kalahari in colonies of up to 30+ members. Like meerkats, colonies usually contain a single breeding female. We work with around fifty colonies of wild mole-rats whose members are caught, blood-sampled and measured twice a year. In parallel, we have developed a breeding facility at our study site in the Kalahari where we have 50+ captive colonies of mole-rats where it is possible to manipulate the size and composition of groups.
Our work has three groups of specific aims:
(1) to explore the mechanisms controlling the development of individuals in both species. A primary goal of this project is to understand the control of fertility in females and the causes and consequences of transitions between reproductive states in both species, including the gene regulatory and signalling mechanisms associated with these transitions. At one level, we are exploring what underlying changes in hormonal status and gene function occur when individuals transition from being helpers to breeders; how these transitions affect the ageing rate of individuals; and to what extent variation in cooperative behaviour and ageing rates are heritable. At another level, we are investigating whether there are divergent developmental pathways between individuals that later become breeders and those that become helpers similar to the caste systems of many social insects and how aspects of the social environment affect these processes
(2) To explore the dynamics of social groups and assess their effects on the development of individuals. In both species, we are investigating the extent to which helpers affect the workloads, litter size, and breeding frequency of dominant females and the survival of their offspring. In meerkats, we also aim to investigate the extent to which the fitness of individuals (as measured by their lifetime breeding success) depends on their own phenotype versus the characteristics of their group and use these to model the relative importance of direct and indirect (‘kin selected’) components of fitness in conjunction with Professor A Gardner (St Andrews). These models will also explore the relative impact of selection operating at different levels on the evolution of cooperation. We shall also investigate whether there is any indication that the behaviour of individuals is adapted to increasing group persistence or proliferation. In mole-rats, we shall manipulate the size and kinship composition of groups and investigate how this affects the development of individuals.
(3) Using our meerkat study, we are also investigating the consequences of short-term climate fluctuations and longer-term directional changes in climate on the growth, survival and breeding success of individuals and the effects of these changes on the size and persistence of breeding groups and local populations. In particular, we are exploring the extent to which increases in temperature interact with fluctuations in rainfall in their effects on population dynamics and demography and how these changes affect the susceptibility of individuals to TB, which is endemic in the population.
The most novel aspects of our work involve the combination of detailed, long-term data on individuals of known age, reproductive history and relatedness under wild and captive conditions with cutting edge techniques of measuring heritability, gene function, individual development and group dynamics. Our work also involves novel approaches to the measurement and analysis of development, communication and gene regulation in wild animals and to modelling multi-level selection and the dynamics of hierarchically structured populations of vertebrates. It will provide insight into the social mechanisms affecting individual development, multi-level selection and the population dynamics and management of group-living mammals. While traditional studies of animal adaptation have focussed on the effects of the physical environment on animal adaptation, the social environment that individuals are exposed to has a profound impact both on the selection pressures operating on both sexes and the evolution of adaptation and on the development of individuals. Our two studies provide unrivalled opportunities to explore these processes in wild mammals. Our work will also provide new insights into the dynamics of social groups in wild mammals and the ways in which climate change is likely to affect recruitment and survival in other populations of social mammals and will help to provide an informed basis for the design of management and conservation strategies.
This project focusses on studies of two mammalian cooperative breeders (Kalahari meerkats and Damaraland mole-rats) that provide unusual opportunities to explore the evolution of cooperative breeding and the mechanisms controlling reproductive suppression, development and cooperation. We have worked for the past twenty-five years on Kalahari meerkats (Suricata suricatta), a social desert-adapted mongoose, at a site in South Africa and have access to 10-15 wild groups of identifiable individuals whose development, reproduction and behaviour have been monitored since their birth. Since our study groups have been closely habituated to humans, we can collect regular data on their daily weight gain, growth and hormonal status of large samples of identifiable individuals of known age and breeding history. At the same site, we work on Damaraland mole-rats (Fukomys damarensis), a cooperative rodent that lives underground in the Kalahari in colonies of up to 30+ members. Like meerkats, colonies usually contain a single breeding female. We work with around fifty colonies of wild mole-rats whose members are caught, blood-sampled and measured twice a year. In parallel, we have developed a breeding facility at our study site in the Kalahari where we have 50+ captive colonies of mole-rats where it is possible to manipulate the size and composition of groups.
Our work has three groups of specific aims:
(1) to explore the mechanisms controlling the development of individuals in both species. A primary goal of this project is to understand the control of fertility in females and the causes and consequences of transitions between reproductive states in both species, including the gene regulatory and signalling mechanisms associated with these transitions. At one level, we are exploring what underlying changes in hormonal status and gene function occur when individuals transition from being helpers to breeders; how these transitions affect the ageing rate of individuals; and to what extent variation in cooperative behaviour and ageing rates are heritable. At another level, we are investigating whether there are divergent developmental pathways between individuals that later become breeders and those that become helpers similar to the caste systems of many social insects and how aspects of the social environment affect these processes
(2) To explore the dynamics of social groups and assess their effects on the development of individuals. In both species, we are investigating the extent to which helpers affect the workloads, litter size, and breeding frequency of dominant females and the survival of their offspring. In meerkats, we also aim to investigate the extent to which the fitness of individuals (as measured by their lifetime breeding success) depends on their own phenotype versus the characteristics of their group and use these to model the relative importance of direct and indirect (‘kin selected’) components of fitness in conjunction with Professor A Gardner (St Andrews). These models will also explore the relative impact of selection operating at different levels on the evolution of cooperation. We shall also investigate whether there is any indication that the behaviour of individuals is adapted to increasing group persistence or proliferation. In mole-rats, we shall manipulate the size and kinship composition of groups and investigate how this affects the development of individuals.
(3) Using our meerkat study, we are also investigating the consequences of short-term climate fluctuations and longer-term directional changes in climate on the growth, survival and breeding success of individuals and the effects of these changes on the size and persistence of breeding groups and local populations. In particular, we are exploring the extent to which increases in temperature interact with fluctuations in rainfall in their effects on population dynamics and demography and how these changes affect the susceptibility of individuals to TB, which is endemic in the population.
The most novel aspects of our work involve the combination of detailed, long-term data on individuals of known age, reproductive history and relatedness under wild and captive conditions with cutting edge techniques of measuring heritability, gene function, individual development and group dynamics. Our work also involves novel approaches to the measurement and analysis of development, communication and gene regulation in wild animals and to modelling multi-level selection and the dynamics of hierarchically structured populations of vertebrates. It will provide insight into the social mechanisms affecting individual development, multi-level selection and the population dynamics and management of group-living mammals. While traditional studies of animal adaptation have focussed on the effects of the physical environment on animal adaptation, the social environment that individuals are exposed to has a profound impact both on the selection pressures operating on both sexes and the evolution of adaptation and on the development of individuals. Our two studies provide unrivalled opportunities to explore these processes in wild mammals. Our work will also provide new insights into the dynamics of social groups in wild mammals and the ways in which climate change is likely to affect recruitment and survival in other populations of social mammals and will help to provide an informed basis for the design of management and conservation strategies.
We have maintained the long-term, individual-based monitoring of growth, hormonal status, reproduction and survival in our study population of wild meerkats and in samples of 50+ groups of wild Damaraland mole-rats and in 50+ colonies of captive mole-rats as outlined in our original proposal. We have made significant progress with all three projects outlined on our grant application.
In Project 1 (Individual development) we have explored the hormonal and genomic mechanisms controlling individual development in all three populations, integrating correlational and experimental work. In particular, we have investigated whether there is evidence of discrete developmental pathways leading to distinct castes and have investigated the hormonal and genomic changes that occur in individuals when they acquire the breeding role and assessed effects on their fecundity and survival. We have also investigated whether there are consistent differences in rates of ageing between breeders and non-breeders, using both measures of attrition in telomere length and changes in reproductive performance in the meerkats. We have also explored the development of cooperative behaviour, assessed the extent of individual differences and measured their heritability using our multi-generational pedigree and Animal Model analyses.
In Project 2 (Group dynamics) we have used out long-term data on meerkats to explore the formation, persistence and extinction of breeding groups and to measure the costs of dispersal. We have also investigated the social and environmental factors affecting the persistence of breeding groups and the factors that lead to group extinctions and have documented long-term changes in range stability and explored the effects of inter-group competition. In addition, we have examined variation in the tenure of breeding positions in both sexes and explored the factors that eventually limit the breeding lifespans of individuals. In the mole-rats, we have explored the dynamics of breeding groups both in natural populations and in our captive colonies. We have investigated the effects of variation in the size and composition of breeding groups on individual growth, reproductive success and survival. We are now starting to assess the relative importance of the phenotype of individuals versus the characteristics of groups on the lifetime breeding success of individuals.
In Project 3 (Group dynamics and population dynamics) we have examined the impact of inter-year differences in rainfall and temperature on growth, breeding success and survival in meerkats and modelled the likely consequences of continuing climate change for the demography of local populations. Our work has shown how the effects of temperature and rainfall interact in their influence on demographic parameters. In addition, it has shown that, through their effects on group size and stability, climate changes affect the incidence of TB infections that are a common cause of group failure. Finally, we have assessed the extent to which social organisation mitigates the impact of extreme conditions and shown that increases in group size reduce the demographic consequences of extreme weather, providing a possible explanation of the association between cooperative breeding and harsh, unpredictable environments.
In Project 1 (Individual development) we have explored the hormonal and genomic mechanisms controlling individual development in all three populations, integrating correlational and experimental work. In particular, we have investigated whether there is evidence of discrete developmental pathways leading to distinct castes and have investigated the hormonal and genomic changes that occur in individuals when they acquire the breeding role and assessed effects on their fecundity and survival. We have also investigated whether there are consistent differences in rates of ageing between breeders and non-breeders, using both measures of attrition in telomere length and changes in reproductive performance in the meerkats. We have also explored the development of cooperative behaviour, assessed the extent of individual differences and measured their heritability using our multi-generational pedigree and Animal Model analyses.
In Project 2 (Group dynamics) we have used out long-term data on meerkats to explore the formation, persistence and extinction of breeding groups and to measure the costs of dispersal. We have also investigated the social and environmental factors affecting the persistence of breeding groups and the factors that lead to group extinctions and have documented long-term changes in range stability and explored the effects of inter-group competition. In addition, we have examined variation in the tenure of breeding positions in both sexes and explored the factors that eventually limit the breeding lifespans of individuals. In the mole-rats, we have explored the dynamics of breeding groups both in natural populations and in our captive colonies. We have investigated the effects of variation in the size and composition of breeding groups on individual growth, reproductive success and survival. We are now starting to assess the relative importance of the phenotype of individuals versus the characteristics of groups on the lifetime breeding success of individuals.
In Project 3 (Group dynamics and population dynamics) we have examined the impact of inter-year differences in rainfall and temperature on growth, breeding success and survival in meerkats and modelled the likely consequences of continuing climate change for the demography of local populations. Our work has shown how the effects of temperature and rainfall interact in their influence on demographic parameters. In addition, it has shown that, through their effects on group size and stability, climate changes affect the incidence of TB infections that are a common cause of group failure. Finally, we have assessed the extent to which social organisation mitigates the impact of extreme conditions and shown that increases in group size reduce the demographic consequences of extreme weather, providing a possible explanation of the association between cooperative breeding and harsh, unpredictable environments.
Our work on strategic growth responses to variation in social condition (including variation in the intensity of competition for breeding opportunities) suggests that effects of this kind may be widespread in other mammals. If so, it is not impossible that they occur in domestic mammals as well as humans and our work highlights promising lines for future research into the social mechanisms that stimulate growth. Our research on the genetic and genomic mechanisms underlying the transition from helpers to breeders provides the first glimpse into genome-wide gene regulatory changes linked to the helper-breeder transition in cooperative mammals. The role of gene regulation in contributing to differences in social roles is shared with eusocial insects. Our work thus far indicates that, in contrast to social insects, this plasticity is retained into adulthood and is associated with potential costs to somatic maintenance, especially as investment in reproduction cumulatively increases over time. Understanding this process is important because it contributes to delineating shared versus distinct aspects of social evolution in mammals versus insects. Additionally, it suggests that social role-dependent patterns of ageing at the molecular level, which we are primed to now test conclusively. Our work also highlights differential sensitivity to social roles across tissues. Interestingly, while the effects of breeding status are widespread in the peripheral tissues of females, they are not particularly striking in brain regions canonically associated with social decision-making. This research has socioeconomic impact via its support of three field-based lab managers and support for multiple post-doctoral level trainees. It also contributes to capacity building via their training in field and wet lab techniques. Our work on the factors affecting group dynamics provides some of the first data available on variations in the persistence of breeding groups and the cause of group extinctions in any social mammal. It highlights promising lines for future research. Similarly, our investigation of variation in the breeding tenure of dominant individuals of both sexes provides one of the first investigations of variation in breeding tenure in any monogamous mammal. Finally, our work on the direct effects of variation in rainfall and temperature on growth and reproductive success shows how these variables interact in their effect on demographic parameters and how these effects can influence other sources of mortality, including the frequency of endemic disease. It suggests that similar complexities are likely in many other systems and that changes in climatic conditions are likely to have demographic consequences that will be difficult to predict.