Tim Clutton-Brock

University of Cambridge | Cam · Department of Zoology

In many cooperatively breeding mammals, an unrelated dominant pair monopolizes reproduction in the social group while subordinates help to raise their offspring. In Kalahari meerkats (Suricata suricatta), dominant males are usually immigrants while dominant females are natal animals that have not left the group where they were born. However, in aro...

Cooperative breeding often evolved in harsh and arid habitats characterized by high levels of environmental uncertainty. Most forms of cooperative behavior have energetic costs and previous studies have shown that the contributions of individuals to alloparental provisioning are conditional on their food intake. However, the effect of naturally occ...

Changing environmental conditions cause changes in the distributions of phenotypic traits in natural populations. However, determining the mechanisms responsible for these changes—and, in particular, the relative contributions of phenotypic plasticity versus evolutionary responses—is difficult. To our knowledge, no study has yet reported evidence t...

Breeding systems in which group members help to raise the offspring of co‐members are associated with arid, unpredictable environments. Cooperative rearing may mitigate the effects of adverse environmental conditions on pup growth and survival. However, few studies have explored the relationship between environmental variation and breeding success,...

Warming global temperatures are affecting a range of aspects of wild populations, but the exact mechanisms driving associations between temperature and phenotypic traits may be difficult to identify. Here, we use a 36‐year data‐set on a wild population of red deer to investigate the causes of associations between temperature and two important compo...

Individual variation in growth rates often generates variation in fitness. However, the ability to draw meaningful inferences from growth data depends on the use of growth models that allow for direct comparisons of growth between the sexes, between populations, and between species. Unlike traditional sigmoid functions, a recently parameterized fam...

Kin selection theory suggests that altruistic behaviors can increase the fitness of altruists when recipients are genetic relatives. Although selection can favor the ability of organisms to preferentially cooperate with close kin, indiscriminately helping all group mates may yield comparable fitness returns if relatedness within groups is very high...

The phenotype of parents can have long-lasting effects on the development of offspring as well as on their behaviour, physiology and morphology as adults. In some cases, these changes may increase offspring fitness but, in others, they can elevate parental fitness at a cost to the fitness of their offspring. We show that in Kalahari meerkats ( Suri...

In singular cooperative breeders few females breed successfully, but those that acquire dominant positions can achieve high levels of breeding success, leading to strong selection for traits that enable individuals to acquire and maintain dominance status. However, little is known about the process by which females acquire dominant breeding status...

There is increasing evidence that some vertebrates can adjust their growth rate in relation to changes in the social context that affect their probability of breeding. Here, we show that, in meerkats (Suricata suricatta), which are singular cooperative breeders, subordinate females increase in body mass after their father is replaced as the dominan...

Robert Hinde led the study of animal behaviour for much of his long working life, drawing on his expertise in zoology and ethology to build bridges with psychology, psychiatry and the social sciences. He pioneered the application of a quantitative scientific approach to observations of behaviour, making important contributions to understanding unde...

The specialization of individuals in specific behavioural tasks is often attributed either to irreversible differences in development, which generate functionally divergent cooperative phenotypes, or to age-related changes in the relative frequency with which individuals perform different cooperative activities; both of which are common in many ins...

Social status can mediate effects on the immune system, with profound consequences for individual health; nevertheless, most investigators of status-related disparities in free-ranging animals have used faecal parasite burdens to proxy immune function in the males of male-dominant species. We instead use direct measures of innate immune function (c...

In many cooperatively breeding animal societies, breeders outlive non-breeding subordinates, despite investing heavily in reproduction [1-3]. In eusocial insects, the extended lifespans of breeders arise from specialized slowed aging profiles [1], prompting suggestions that reproduction and dominance similarly defer aging in cooperatively breeding...

The date received for the article is incorrect. The online typeset version of the article states that the paper was received on the 21 April 2017. It was actually received a year later, on the 21 April 2018.

Dispersal is a key ecological process that influences the dynamics of spatially and socially structured populations and consists of three stages ‐ emigration, transience, and settlement ‐ and each stage is influenced by different social, individual, and environmental factors. Despite our appreciation of the complexity of the process, we lack a firm...

In social mole-rats, breeding females are larger and more elongated than non-breeding female helpers. This status-related morphological divergence is thought to arise from modifications of skeletal growth following the death or removal of the previous breeder and the transition of their successors from a non-breeding to a breeding role. However, it...

For highly social species, population dynamics depend on hierarchical demography that links local processes, group dynamics, and population growth. Here, we describe a stage-structured matrix model of hierarchical demography, which provides a framework for understanding social influences on population change. Our approach accounts for dispersal and...

The phenotype of parents can have long-lasting effects on the development of offspring as well as on their behaviour, physiology, and morphology as adults. In some cases, these changes may increase offspring fitness but, in others, they can elevate parental fitness at a cost to the fitness of their offspring. Here, we show that in Kalahari meerkats...

In Damaraland mole-rats (Fukomys damarensis), non-breeding subordinates contribute to the care of offspring born to the breeding pair in their group by carrying and retrieving young to the nest. In social mole-rats and some cooperative breeders, dominant females show unusually high testosterone levels and it has been suggested that high testosteron...

Meerkats are group-living, insectivorous herpestids in which subordinate members provide extensive care for the dominant female's young. In contrast to some cooperative breeders, subordinate female meerkats are physiologically able to reproduce and occasionally do so successfully; their attempts are more frequently 'suppressed' via eviction or infa...

Demographic senescence is increasingly recognised as an important force shaping the dynamics of wild vertebrate populations. However, our understanding of the processes that underpin these declines in survival and fertility in old age remains limited. Evidence for age‐related changes in foraging behaviour and habitat use is emerging from wild verte...

Dispersal is a key process governing the dynamics of socially and spatially structured populations, and involves three distinct stages: emigration, transience, and settlement. At each stage, individuals have to make movement decisions, which are influenced by social, environmental, and individual factors. Yet, a comprehensive understanding of the d...

Measures of glucocorticoid stress hormones (e.g. cortisol) have often been used to characterize conflict between subordinates and dominants. In cooperative breeders where subordinates seldom breed in their natal group and assist in offspring rearing, increases in subordinate glucocorticoid levels may be caused by conflict among subordinates as well...

Social animal groups often make consensus decisions about when to return to a sleeping site after a day of foraging. These decisions can depend on extrinsic as well as intrinsic factors, and can range from unshared to shared. Here we investigated how decisions of meerkats, Suricata suricatta, to return to their burrows are coordinated, whether they...

In cooperative breeders, aggression from dominant breeders directed at subordinates may raise subordinate stress hormone (glucocorticoid) concentrations. This may benefit dominants by suppressing subordinate reproduction but it is uncertain whether aggression from dominants can elevate subordinate cooperative behaviour, or how resulting changes in...

This paper traces the development of our understanding of the development of different approaches to estimating the strength of reproductive competition and sexual selection in the two sexes, based on measures of the operational sex ratio, the opportunity for sexual selection and contrasts in selection gradients between the sexes. It argues that di...

Aggression directed by male baboons at females during the early stages of their breeding cycle increases chances that males will mate with them as they approach conception.

Early-life adversity can affect health, survival and fitness later in life, and recent evidence suggests that telomere attrition may link early conditions with their delayed consequences. Here, we investigate the link between early-life competition and telomere length in wild meerkats. Our results show that, when multiple females breed concurrently...

Early-life adversity can affect health, survival and fitness later in life, and recent evidence suggests that telomere attrition may link early conditions with their delayed consequences. Here, we investigate the link between early-life competition and telomere length in wild meerkats. Our results show that, when multiple females breed concurrently...

In group-living mammals, the eviction of subordinate females from breeding groups by dominants may serve to reduce feeding competition or to reduce breeding competition. Here, we combined both correlational and experimental approaches to investigate whether increases in food intake by dominant females reduces their tendency to evict subordinate fem...

1.Tuberculosis (TB) is an important and widespread disease of wildlife, livestock, and humans worldwide, but long-term empirical datasets describing this condition are rare. A population of meerkats (Suricata suricatta) in South Africa's Kalahari Desert have been diagnosed with Mycobacterium suricattae, a novel strain of TB, causing fatal disease i...

Vulture populations are experiencing rapid declines across the globe. While the declines have been most precipitous in Asia, recent reports suggest African populations are likewise imminently threatened. As the factors underlying these general population trends are multifaceted and will vary in their relative intensity spatially, it is imperative t...

Vulture populations are experiencing rapid declines across the globe. While the declines have been most precipitous in Asia, recent reports suggest African populations are likewise imminently threatened. As the factors underlying these general population trends are multifaceted and will vary in their relative intensity spatially, it is imperative t...

Additional figures, tables, and analyses Contents: -Supplementary Tables S1-S8 -Dominance ranks (Supplementary Table S8) -Supplementary Figures S1-S3 -Further analyses of age-related variation in endocranial volume (Supplementary Figure S2)

In some eusocial insect societies, adaptation to the division of labour results in multimodal size variation among workers. It has been suggested that variation in size and growth among non-breeders in naked and Damaraland mole-rats may similarly reflect functional divergence associated with different cooperative tasks. However, it is unclear wheth...

In some eusocial insect societies, adaptation to the division of labour results in multimodal size variation among workers. It has been suggested that variation in size and growth among non-breeders in naked and Damaraland mole-rats may similarly reflect functional divergence associated with different cooperative tasks. However, it is unclear wheth...

Research on relative brain size in mammals suggests that increases in brain size may generate benefits to survival and costs to fecundity: comparative studies of mammals have shown that interspecific differences in relative brain size are positively correlated with longevity and negatively with fecundity. However, as yet, no studies of mammals have...

In vertebrates, reproductive endocrine concentrations are strongly differentiated by sex, with androgen biases typifying males and estrogen biases typifying females. These sex differences can be reduced in female-dominant species; however, even the most masculinised of females have less testosterone (T) than do conspecific males. To test if aggress...

The immunocompetence handicap hypothesis posits that androgens in males can be a ‘double-edged sword’, actively promoting reproductive success, while also negatively impacting health. Because there can be both substantial androgen concentrations in females and significant androgenic variation among them, particularly in species portraying female so...

Significance Nonreproductive group members of naked and Damaraland mole rats are thought to be organized in permanent, distinct castes that differ in behavior and physiology, suggesting that their social organization resembles that of obligatorily eusocial insects. This study tests predictions about the distribution of cooperative behavior based on...

Costs of reproduction are expected to be ubiquitous in wild animal populations and understanding the drivers of variation in these costs is an important aspect of life-history evolution theory. We use a 43 year dataset from a wild population of red deer to examine the relative importance of two factors that influence the costs of reproduction to mo...

Differences in phenological responses to climate change among species can desynchronise ecological interactions and thereby threaten ecosystem function. To assess these threats, we must quantify the relative impact of climate change on species at different trophic levels. Here, we apply a Climate Sensitivity Profile approach to 10,003 terrestrial a...

In many animal societies where hierarchies govern access to reproduction, the social rank of individuals is related to their age and weight(1-5) and slow-growing animals may lose their place in breeding queues to younger 'challengers' that grow faster(5,6). The threat of being displaced might be expected to favour the evolution of competitive growt...

Costs of reproduction are expected to be ubiquitous in wild animal populations, and understanding the drivers of variation in these costs is an important aspect of life-history evolution theory. We use a 43-year dataset from a wild population of red deer to examine the relative importance of two factors that influence the costs of reproduction to m...

Research on relative brain size in mammals suggests that increases in brain size may generate benefits to survival and costs to fecundity: comparative studies of mammals have shown that interspecific differences in relative brain size are positively correlated with longevity and negatively with fecundity. However, as yet, no studies of mammals have...

Research on relative brain size in mammals suggests that increases in brain size may generate benefits to survival and costs to fecundity: comparative studies of mammals have shown that interspecific differences in relative brain size are positively correlated with longevity and negatively with fecundity. However, as yet, no studies of mammals have...

The evolution of cooperation has been a focus of interest for evolutionary biologists for over a hundred years (Darwin 1859; Kropotkin 1908; Williams 1966). While all forms of cooperation challenge the centrality of competition in the process of evolution, cooperative and eusocial breeding systems, where offspring produced by a small number of bree...

In male vertebrates, androgens are inextricably linked to reproduction, social dominance, and aggression, often at the cost of paternal investment or prosociality. Testosterone is invoked to explain rank-related reproductive differences, but its role within a status class, particularly among subordinates, is underappreciated. Recent evidence, espec...

Cooperative behaviours by definition are those that provide some benefit to another individual. Allonursing, the nursing of non-descendent young, is often considered a cooperative behavior and is assumed to provide benefits to recipient offspring in terms of growth and survival, and to their mothers, by enabling them to share the lactation load. Ho...

Temporal changes in phenological traits arising as a consequence of recent rapid environmental change have been widely demonstrated in animal populations. Increasingly, studies are seeking to understand the impact of changes in such traits on individual fitness and population dynamics, with the ultimate aim of predicting population persistence or e...

The evolutionary theories of senescence predict that investment in reproduction in early life should come at the cost of reduced somatic maintenance, and thus earlier or more rapid senescence. There is now growing support for such trade-offs in wild vertebrates, but these exclusively come from females. Here, we test this prediction in male red deer...

Evolutionary theory predicts that genetic constraints should be widespread, but empirical support for their existence is surprisingly rare. Commonly-applied univariate and bivariate approaches to detecting genetic constraints can underestimate their prevalence, with important aspects potentially only tractable within a multivariate framework. Howev...

In many animal societies, a small proportion of dominant females monopolize reproduction by actively suppressing subordinates. Theory assumes that this is because subordinate reproduction depresses the fitness of dominants, yet the effect of subordinate reproduction on dominant behaviour and reproductive success has never been directly assessed. He...

Multiple approaches exist to model patterns of space use across species, among them resource selection analysis, statistical home range modelling, and mechanistic movement modelling. Mechanistic home-range models combine the benefits of these approaches, describing emergent territorial patterns based on fine-scale individual- or group-movement rule...

Individual variation in growth is high in cooperative breeders and may reflect plastic divergence in developmental trajectories leading to breeding vs. helping phenotypes. However, the relative importance of additive genetic variance and developmental plasticity in shaping growth trajectories is largely unknown in cooperative vertebrates. This stud...

Allonursing, the nursing of another female’s offspring, is assumed to impose a substantial energetic cost given the high cost of lactation to mothers. However, these costs have not been quantified. In cooperatively breeding mammals where helpers contribute to lactation, they might be expected to modify their behavior to mitigate these potential cos...

Social and environmental factors influence key life-history processes and population dynamics by affecting fitness-related phenotypic traits such as body mass. The role of body mass is particularly pronounced in cooperative breeders due to variation in social status and consequent variation in access to resources. Investigating the mechanisms under...

The social niche specialization hypothesis predicts that group-living animals should specialize in particular social roles to avoid social conflict, resulting in alternative life-history strategies for different roles. Social niche specialization, coupled with role-specific life-history trade-offs, should thus generate between-individual difference...

Extraterritorial prospecting forays are an important route to fitness in many species, allowing the assessment of dispersal opportunities and often extragroup mating prior to dispersal. However, few studies have examined the factors affecting individual variation in prospecting effort and the extent to which individuals time their forays so as to m...

In cooperatively breeding species with high reproductive skew, a single breeding female is dominant to all other group members, but it is not yet known if there are consistent dominance relationships among subordinates. In this study on meerkats (Suricata suricatta), we used naturally observed dominance assertions and submissive interactions within...

During the latter half of the last century, evidence of reproductive competition between males and male selection by females led to the development of a stereotypical view of sex differences that characterized males as competitive and aggressive, and females as passive and choosy, which is currently being revised. Here, we compare social competitio...

Data deposited in the Dryad repository: doi:10.5061/dryad.cf033. Fig. S1. Linear interpolation of growth (black lines) during the focal windows of interest (shaded in grey). Fig. S2. Schematic outlining timescale for growth and environmental measurements. Table S1. Repeatability values and 95% credibility intervals for levels of the random effects...

Allolactation, the nursing of another female's offspring, occurs most commonly where several females raise young simultaneously in the same nest, but also occurs in singular breeders where nonbreeders also lactate for the offspring of dominant females. In this study, we investigated the factors predicting the frequency of allonursing in meerkats, S...

Although the ultimate causes for variation in contributions to helping in cooperative breeders are increasingly well understood, the underlying physiological mechanisms remain largely unknown. Recent work has suggested that glucocorticoids may play an important role in the expression of cooperative behavior. Here, we present the first experimental...

The Only Flame in Town Unusual for mammals, humans are notably socially monogamous, with pair bonding sometimes lasting decades. Why? Lukas and Clutton-Brock (p. 526 ; see the Perspective by Kappeler ) examined data from over 2500 mammalian species across 26 orders containing 60 evolutionary transitions to monogamy. In every case, the ancestral con...

In age-structured populations, environmental autocorrelations influence the long-run population growth rate as well as the variance in future population size. We used the concept of individual reproductive value to examine how autocorrelated environments affect the dynamics of age-structured populations, leading to transparent interpretations and e...

This paper introduces a Theme Issue presenting the latest developments in research on the interplay between flexibility and constraint in social behaviour, using comparative datasets, long-term field studies and experimental data from both field and laboratory studies of mammals. We first explain our focus on mammals and outline the main components...