Cooperative Mammal Research Articles

Contributions of genetic and nongenetic sources to variation in cooperative behavior in a cooperative mammal.

The evolution of cooperative behavior is a major area of research among evolutionary biologists and behavioral ecologists, yet there are few estimates of its heritability or its evolutionary potential, and long-term studies of identifiable individuals are required to disentangle genetic and nongenetic components of cooperative behavior. Here, we use long-term data on over 1800 individually recognizable wild meerkats (Suricata suricatta) collected over 30 years and a multigenerational genetic pedigree to partition phenotypic variation in three cooperative behaviors (babysitting, pup feeding, and sentinel behavior) into individual, additive genetic, and other sources, and to assess their repeatability and heritability. In addition to strong effects of sex, age, and dominance status, we found significant repeatability in individual contributions to all three types of cooperative behavior both within and across breeding seasons. Like most other studies of the heritability of social behavior, we found that the heritability of cooperative behavior was low. However, our analysis suggests that a substantial component of the repeatable individual differences in cooperative behavior that we observed was a consequence of additive genetic variation. Our results consequently indicate that cooperative behavior can respond to selection, and suggest scope for further exploration of the genetic basis of social behavior.

Report of suspected kidnapping in cooperative breeding Southern Ground-Hornbill in South Africa with consequences for conservation reintroductions

Kidnapping in avian species is a rarely observed phenomenon and warrants greater investigation. Kidnapping, reported for some cooperative breeding birds and mammals, has now been confirmed for the Southern Ground-Hornbill Bucorvus leadbeateri and has implications for management of reintroductions of neighbouring groups. A juvenile was kidnapped from a newly reintroduced group in Limpopo, South Africa. It is suggested that this kidnapping was driven by the group to weaken and destabilise a neighbouring group, rather than strengthen their own with an additional helper.

Effects of climate change on pup growth and survival in a cooperative mammal, the meerkat

Abstract 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, and the role of helpers. Here, we show that reductions in the growth and survival of meerkat (Suricata suricatta) pups have been associated with increases in daily maximum air temperatures (Tmax) in the southern Kalahari over the last 20 years. On days when Tmax was high, meerkat pups gained less body mass than on cooler days. Reductions in the diurnal body mass gain (ΔMb) of pups on hotter days were not a consequence of reductions in the frequency with which pups were fed by adults as feeding rate increased with Tmax, suggesting that the reductions in ΔMb by pups on hot days reflected a decrease in water content of the food items or an increased water and energy cost of thermoregulation. Reductions in pup ΔMb on hot days were smaller in larger groups, in which helper‐to‐pup ratios were relatively high. As increases in air temperature are predicted with climate change, further reductions in meerkat pup growth and survival seem inevitable. A free Plain Language Summary can be found within the Supporting Information of this article.

Rank-Related Contrasts in Longevity Arise from Extra-Group Excursions Not Delayed Senescence in a Cooperative Mammal

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 vertebrates, too [4-6]. Although lacking the permanent castes of eusocial insects, breeders of vertebrate societies could delay aging via phenotypic plasticity (similar rank-related changes occur in growth, neuroendocrinology, and behavior [7-10]), and such plastic deferment of aging may reveal novel targets for preventing aging-related diseases [11]. Here, we investigate whether breeding dominants exhibit extended longevity and delayed age-related physiological declines in wild cooperatively breeding meerkats. We show that dominants outlive subordinates but exhibit faster telomere attrition (a marker of cellular senescence and hallmark of aging [12]) and that in dominants (but not subordinates), rapid telomere attrition is associated with mortality. Our findings further suggest that, rather than resulting from specialized aging profiles, differences in longevity between dominants and subordinates are driven by subordinate dispersal forays, which become exponentially more frequent with age and increase subordinate mortality. These results highlight the need to critically examine the causes of rank-related longevity contrasts in other cooperatively breeding vertebrates, including social mole-rats, where they are currently attributed to specialized aging profiles in dominants [4].

A high-quality pedigree and genetic markers both reveal inbreeding depression for quality but not survival in a cooperative mammal.

Inbreeding depression, the reduced fitness of offspring of closely related parents, is commonplace in both captive and wild populations and has important consequences for conservation and mating system evolution. However, because of the difficulty of collecting pedigree and life-history data from wild populations, relatively few studies have been able to compare inbreeding depression for traits at different points in the life cycle. Moreover, pedigrees give the expected proportion of the genome that is identical by descent (IBDg ) whereas in theory with enough molecular markers realized IBDg can be quantified directly. We therefore investigated inbreeding depression for multiple life-history traits in a wild population of banded mongooses using pedigree-based inbreeding coefficients (fped ) and standardized multilocus heterozygosity (sMLH) measured at 35-43 microsatellites. Within an information theoretic framework, we evaluated support for either fped or sMLH as inbreeding terms and used sequential regression to determine whether the residuals of sMLH on fped explain fitness variation above and beyond fped . We found no evidence of inbreeding depression for survival, either before or after nutritional independence. By contrast, inbreeding was negatively associated with two quality-related traits, yearling body mass and annual male reproductive success. Yearling body mass was associated with fped but not sMLH, while male annual reproductive success was best explained by both fped and residual sMLH. Thus, our study not only uncovers variation in the extent to which different traits show inbreeding depression, but also reveals trait-specific differences in the ability of pedigrees and molecular markers to explain fitness variation and suggests that for certain traits, genetic markers may capture variation in realized IBDg above and beyond the pedigree expectation.

Telomere dynamics in wild banded mongooses: Evaluating longitudinal and quasi-longitudinal markers of senescence

Telomere length and the rate of telomere shortening have been suggested as particularly useful physiological biomarkers of the processes involved in senescent decline of somatic and reproductive function. However, longitudinal data on changes in telomere length across the lifespan are difficult to obtain, particularly for long-lived animals. Quasi-longitudinal studies have been proposed as a method to gain insight into telomere dynamics in long-lived species. In this method, minimally replicative cells are used as the baseline telomere length against which telomere length in highly replicative cells (which represent the current state) can be compared. Here we test the assumptions and predictions of the quasi-longitudinal approach using longitudinal telomere data in a wild cooperative mammal, the banded mongoose, Mungos mungo. Contrary to our prediction, telomere length (TL) was longer in leukocytes than in ear cartilage. Longitudinally, the TL of ear cartilage shortened with age, but there was no change in the TL of leukocytes, and we also observed many individuals in which TL increased rather than decreased with age. Leukocyte TL but not cartilage TL was a predictor of total lifespan, while neither predicted post-sampling survival. Our data do not support the hypothesis that cross-tissue comparison in TL can act as a quasi-longitudinal marker of senescence. Rather, our results suggest that telomere dynamics in banded mongooses are more complex than is typically assumed, and that longitudinal studies across whole life spans are required to elucidate the link between telomere dynamics and senescence in natural populations.

Explaining negative kin discrimination in a cooperative mammal society

Kin selection theory predicts that, where kin discrimination is possible, animals should typically act more favorably toward closer genetic relatives and direct aggression toward less closely related individuals. Contrary to this prediction, we present data from an 18-y study of wild banded mongooses, Mungos mungo, showing that females that are more closely related to dominant individuals are specifically targeted for forcible eviction from the group, often suffering severe injury, and sometimes death, as a result. This pattern cannot be explained by inbreeding avoidance or as a response to more intense local competition among kin. Instead, we use game theory to show that such negative kin discrimination can be explained by selection for unrelated targets to invest more effort in resisting eviction. Consistent with our model, negative kin discrimination is restricted to eviction attempts of older females capable of resistance; dominants exhibit no kin discrimination when attempting to evict younger females, nor do they discriminate between more closely or less closely related young when carrying out infanticidal attacks on vulnerable infants who cannot defend themselves. We suggest that in contexts where recipients of selfish acts are capable of resistance, the usual prediction of positive kin discrimination can be reversed. Kin selection theory, as an explanation for social behavior, can benefit from much greater exploration of sequential social interactions.

Competitive growth in a cooperative mammal.

In many animal societies where hierarchies govern access to reproduction, the social rank of individuals is related to their age and weight and slow-growing animals may lose their place in breeding queues to younger 'challengers' that grow faster. The threat of being displaced might be expected to favour the evolution of competitive growth strategies, where individuals increase their own rate of growth in response to increases in the growth of potential rivals. Although growth rates have been shown to vary in relation to changes in the social environment in several vertebrates including fish and mammals, it is not yet known whether individuals increase their growth rates in response to increases in the growth of particular reproductive rivals. Here we show that, in wild Kalahari meerkats (Suricata suricatta), subordinates of both sexes respond to experimentally induced increases in the growth of same-sex rivals by raising their own growth rate and food intake. In addition, when individuals acquire dominant status, they show a secondary period of accelerated growth whose magnitude increases if the difference between their own weight and that of the heaviest subordinate of the same sex in their group is small. Our results show that individuals adjust their growth to the size of their closest competitor and raise the possibility that similar plastic responses to the risk of competition may occur in other social mammals, including domestic animals and primates.

Robbing rivals: interference foraging competition reflects female reproductive competition in a cooperative mammal

Intense intrasexual competition for breeding opportunities is a characteristic of cooperatively breeding species with high reproductive skew. In such ‘singular’ cooperative breeders, females suffer greater variability in direct reproductive success than do males, and this in turn leads to greater intrasexual competition in females. Under such circumstances, selection should favour traits that enhance female competitive ability, such as size, fighting skill or aggression. However, despite burgeoning interest in female intrasexual competition, there is limited evidence that female cooperative breeders exhibit more pronounced competitive traits than do males. We examined whether intrasexual competition has influenced the expression of a competitive behavioural trait (i.e. prey theft) in a ‘singular’, cooperatively breeding mammal, the dwarf mongoose, Helogale parvula. We used both observational and experimental data to assess whether wild dwarf mongooses exploit interference foraging competition to persecute their reproductive rivals, and whether the sexes differ with regard to this behaviour. We found that nonalpha female mongooses preferentially stole from other females rather than males, and that, under natural foraging conditions, they were more likely to steal prey from their closest rival (i.e. the female immediately below themselves in the dominance hierarchy) than from easier targets much lower in rank. In contrast, male dwarf mongooses (and alpha females) did not exhibit any sex bias, stealing prey indiscriminately from all lower ranking group members. We conclude that the acute intrasexual rivalry suffered by female dwarf mongooses has led to the differential development of this competitive behavioural trait.

Elevated glucocorticoid concentrations during gestation predict reduced reproductive success in subordinate female banded mongooses.

Dominant females in social species have been hypothesized to reduce the reproductive success of their subordinates by inducing elevated circulating glucocorticoid (GC) concentrations. However, this ‘stress-related suppression' hypothesis has received little support in cooperatively breeding species, despite evident reproductive skews among females. We tested this hypothesis in the banded mongoose (Mungos mungo), a cooperative mammal in which multiple females conceive and carry to term in each communal breeding attempt. As predicted, lower ranked females had lower reproductive success, even among females that carried to term. While there were no rank-related differences in faecal glucocorticoid (fGC) concentrations prior to gestation or in the first trimester, lower ranked females had significantly higher fGC concentrations than higher ranked females in the second and third trimesters. Finally, females with higher fGC concentrations during the third trimester lost a greater proportion of their gestated young prior to their emergence from the burrow. Together, our results are consistent with a role for rank-related maternal stress in generating reproductive skew among females in this cooperative breeder. While studies of reproductive skew frequently consider the possibility that rank-related stress reduces the conception rates of subordinates, our findings highlight the possibility of detrimental effects on reproductive outcomes even after pregnancies have become established.

Adjustment of costly extra-group paternity according to inbreeding risk in a cooperative mammal

Females of many animal species seek mating opportunities with multiple males, despite being able to obtain sufficient sperm to father their offspring from a single male. In animals that live in stable social groups, females often choose to mate outside their group resulting in extra-group paternity (EGP). One reason proposed to explain female choice for extra-group males is to obtain compatible genes, for example, in order to avoid inbreeding depression in offspring. The benefits of such extra-group paternities could be substantial if they result in fitter, outbred offspring. However, avoiding inbreeding in this way could be costly for females, for example, through retaliation by cuckolded males or through receiving aggression while prospecting for extra-group mating opportunities. We investigate the costs and benefits of EGP in the banded mongoose Mungos mungo, a cooperatively breeding mammal in which within-group mates are sometimes close relatives. We find that pups born to females that mate with extra-group males are more genetically heterozygous are heavier and are more likely to survive to independence than pups born to females that mate within their group. However, extra-group matings also involve substantial costs as they occur during violent encounters that sometimes result in injury and death. This appears to lead femalebanded mongooses to adaptively adjust EGP levels according to the current risk of inbreeding associated with mating within the group. For group-living animals, the costs of intergroup interactions may help to explain variation in both inbreeding rates and EGP within and between species.

Hormonal mediation of a carry‐over effect in a wild cooperative mammal

Summary 1. Recent research has shown that parental investment in one breeding attempt often has a profound negative impact on the level of parental investment in subsequent breeding attempts. However, the mechanistic underpinnings that mediate such carry-over effects are poorly understood. 2. Here, we hypothesise that carry-over effects arise because energetic losses lead to elevated levels of glucocorticoid ‘stress’ hormones which inhibit future investment and thereby maintain energetic homeostasis. We investigate this hypothesis through a detailed investigation of a carry-over effect of (allo-) parental investment in the cooperatively breeding banded mongoose (Mungos mungo). 3. Using a combination of non-invasive hormone monitoring and feeding experiments, we demonstrate (i) that high glucocorticoid concentrations prior to breeding predict reduced alloparental investment; (ii) that energetic losses associated with high alloparental investment lead to an increase in glucocorticoid concentrations during the breeding attempt; and (iii) that elevated glucocorticoid concentrations persist into a time period that is known to affect future investment, although high pup mortality meant that we could not measure effects on subsequent alloparental investment directly. 4. Together, our results provide strong evidence for the hypothesis that carry-over effects on parental investment are mediated by circulating glucocorticoid concentrations. Since an individual’s stress physiology is shaped by early-life and social factors, our findings may help to explain how these factors contribute to individual variation in parental investment and lifetime reproductive success.

Additive genetic variance and developmental plasticity in growth trajectories in a wild cooperative mammal.

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 study exploits weekly sequences of body mass from birth to adulthood to investigate sources of variance in, and covariance between, early and later growth in wild meerkats (Suricata suricatta), a cooperative mongoose. Our results indicate that (i) the correlation between early growth (prior to nutritional independence) and adult mass is positive but weak, and there are frequent changes (compensatory growth) in post-independence growth trajectories; (ii) among parameters describing growth trajectories, those describing growth rate (prior to and at nutritional independence) show undetectable heritability while associated size parameters (mass at nutritional independence and asymptotic mass) are moderately heritable (0.09 ≤ h(2) < 0.3); and (iii) additive genetic effects, rather than early environmental effects, mediate the covariance between early growth and adult mass. These results reveal that meerkat growth trajectories remain plastic throughout development, rather than showing early and irreversible divergence, and that the weak effects of early growth on adult mass, an important determinant of breeding success, are partly genetic. In contrast to most cooperative invertebrates, the acquisition of breeding status is often determined after sexual maturity and strongly impacted by chance in many cooperative vertebrates, who may therefore retain the ability to adjust their morphology to environmental changes and social opportunities arising throughout their development, rather than specializing early.

Policing of reproduction by hidden threats in a cooperative mammal

The evolution of cooperation in animal and human societies is associated with mechanisms to suppress individual selfishness. In insect societies, queens and workers enforce cooperation by "policing" selfish reproduction by workers. Insect policing typically takes the form of damage limitation after individuals have carried out selfish acts (such as laying eggs). In contrast, human policing is based on the use of threats that deter individuals from acting selfishly in the first place, minimizing the need for damage limitation. Policing by threat could in principle be used to enforce reproductive suppression in animal societies, but testing this idea requires an experimental approach to simulate reproductive transgression and provoke out-of-equilibrium behavior. We carried out an experiment of this kind on a wild population of cooperatively breeding banded mongooses (Mungos mungo) in Uganda. In this species, each group contains multiple female breeders that give birth to a communal litter, usually on the same day. In a 7-y experiment we used contraceptive injections to manipulate the distribution of maternity within groups, triggering hidden threats of infanticide. Our data suggest that older, socially dominant females use the threat of infanticide to deter selfish reproduction by younger females, but that females can escape the threat of infanticide by synchronizing birth to the same day as older females. Our study shows that reproduction in animal societies can be profoundly influenced by threats that remain hidden until they are triggered experimentally. Coercion may thus extend well beyond the systems in which acts of infanticide are common.

Intra-sexual selection in cooperative mammals and birds: why are females not bigger and better armed?

In cooperatively breeding mammals and birds, intra-sexual reproductive competition among females may often render variance in reproductive success higher among females than males, leading to the prediction that intra-sexual selection in such species may have yielded the differential exaggeration of competitive traits among females. However, evidence to date suggests that female-biased reproductive variance in such species is rarely accompanied by female-biased sexual dimorphisms. We illustrate the problem with data from wild Damaraland mole-rat, Fukomys damarensis, societies: the variance in lifetime reproductive success among females appears to be higher than that among males, yet males grow faster, are much heavier as adults and sport larger skulls and incisors (the weapons used for fighting) for their body lengths than females, suggesting that intra-sexual selection has nevertheless acted more strongly on the competitive traits of males. We then consider potentially general mechanisms that could explain these disparities by tempering the relative intensity of selection for competitive trait exaggeration among females in cooperative breeders. Key among these may be interactions with kin selection that could nevertheless render the variance in inclusive fitness lower among females than males, and fundamental aspects of the reproductive biology of females that may leave reproductive conflict among females more readily resolved without overt physical contests.

Maternal, social and abiotic environmental effects on growth vary across life stages in a cooperative mammal.

Resource availability plays a key role in driving variation in somatic growth and body condition, and the factors determining access to resources vary considerably across life stages. Parents and carers may exert important influences in early life, when individuals are nutritionally dependent, with abiotic environmental effects having stronger influences later in development as individuals forage independently.Most studies have measured specific factors influencing growth across development or have compared relative influences of different factors within specific life stages. Such studies may not capture whether early-life factors continue to have delayed effects at later stages, or whether social factors change when individuals become nutritionally independent and adults become competitors for, rather than providers of, food.Here, we examined variation in the influence of the abiotic, social and maternal environment on growth across life stages in a wild population of cooperatively breeding meerkats. Cooperatively breeding vertebrates are ideal for investigating environmental influences on growth. In addition to experiencing highly variable abiotic conditions, cooperative breeders are typified by heterogeneity both among breeders, with mothers varying in age and social status, and in the number of carers present.Recent rainfall had a consistently marked effect on growth across life stages, yet other seasonal terms only influenced growth during stages when individuals were growing fastest. Group size and maternal dominance status had positive effects on growth during the period of nutritional dependence on carers, but did not influence mass at emergence (at 1 month) or growth at independent stages (>4 months). Pups born to older mothers were lighter at 1 month of age and subsequently grew faster as subadults. Males grew faster than females during the juvenile and subadult stage only.Our findings demonstrate the complex ways in which the external environment influences development in a cooperative mammal. Individuals are most sensitive to social and maternal factors during the period of nutritional dependence on carers, whereas direct environmental effects are relatively more important later in development. Understanding the way in which environmental sensitivity varies across life stages is likely to be an important consideration in predicting trait responses to environmental change.

Individual recognition in a wild cooperative mammal using contact calls

Many of the mechanisms advanced to explain the evolution of intraspecific cooperative behaviour, such as reciprocity or social prestige, hinge on an animal's ability to recognize individual group members. However, ‘true’ individual recognition, between adult group members, has never been demonstrated in a cooperatively breeding bird or mammal species. We tested whether a wild cooperative mammal, the dwarf mongoose, Helogale parvula, could recognize individual group members from their vocalizations. We provided test subjects with a large, desirable food item and then simulated the approach of another group member using playbacks of its contact calls. Mongooses were more vigilant after hearing the calls of individuals of higher rank than themselves (that could steal their food) compared with individuals of lower rank than themselves (that could not). We showed that the mongooses were not simply responding to age-related cues that conveyed potential information on rank, and provide some evidence that they were associating the unique characteristics of the call with an individually specific characteristic of the caller (i.e. its relative rank). We conclude that dwarf mongooses exhibit ‘true’ individual recognition, and this finding supports the potential validity of mechanisms that rely on individuals monitoring the behaviour of others to explain the evolution of cooperative behaviour.

Energetic Benefits of Sociality Offset the Costs of Parasitism in a Cooperative Mammal

Sociality and particularly advanced forms of sociality such as cooperative breeding (living in permanent groups with reproductive division of labour) is relatively rare among vertebrates. A suggested constraint on the evolution of sociality is the elevated transmission rate of parasites between group members. Despite such apparent costs, sociality has evolved independently in a number of vertebrate taxa including humans. However, how the costs of parasitism are overcome in such cases remains uncertain. We evaluated the potential role of parasites in the evolution of sociality in a member of the African mole-rats, the only mammal family that exhibits the entire range of social systems from solitary to eusocial. Here we show that resting metabolic rates decrease whilst daily energy expenditure and energy stores (i.e. body fat) increase with group size in social Natal mole rats (Cryptomys hottentotus natalensis). Critically, larger groups also had reduced parasite abundance and infested individuals only showed measurable increases in energy metabolism at high parasite abundance. Thus, in some circumstances, sociality appears to provide energetic benefits that may be diverted into parasite defence. This mechanism is likely to be self-reinforcing and an important factor in the evolution of sociality.

Inbreeding and inbreeding depression of early life traits in a cooperative mammal

Mating between relatives often results in negative fitness consequences or inbreeding depression. However, the expression of inbreeding in populations of wild cooperative mammals and the effects of environmental, maternal and social factors on inbreeding depression in these systems are currently not well understood. This study uses pedigree-based inbreeding coefficients from a long-term study of meerkats (Suricata suricatta) in South Africa to reveal that 44% of the population have detectably non-zero (F > 0) inbreeding coefficients. 15% of these inbred individuals were the result of moderate inbreeding (F ≥ 0.125), although such inbreeding events almost solely occurred when mating individuals had no prior experience of each other. Inbreeding depression was evident for a range of traits: pup mass at emergence from the natal burrow, hind-foot length, growth until independence and juvenile survival. However, we found no evidence of significant inbreeding depression for skull and forearm length or for pup survival. This research provides a rare investigation into inbreeding in a cooperative mammal, revealing high levels of inbreeding, considerable negative consequences and complex interactions with the social environment.

The Role of Host Traits, Season and Group Size on Parasite Burdens in a Cooperative Mammal

The distribution of parasites among hosts is often characterised by a high degree of heterogeneity with a small number of hosts harbouring the majority of parasites. Such patterns of aggregation have been linked to variation in host exposure and susceptibility as well as parasite traits and environmental factors. Host exposure and susceptibility may differ with sexes, reproductive effort and group size. Furthermore, environmental factors may affect both the host and parasite directly and contribute to temporal heterogeneities in parasite loads. We investigated the contributions of host and parasite traits as well as season on parasite loads in highveld mole-rats (Cryptomys hottentotus pretoriae). This cooperative breeder exhibits a reproductive division of labour and animals live in colonies of varying sizes that procreate seasonally. Mole-rats were parasitised by lice, mites, cestodes and nematodes with mites (Androlaelaps sp.) and cestodes (Mathevotaenia sp.) being the dominant ecto- and endoparasites, respectively. Sex and reproductive status contributed little to the observed parasite prevalence and abundances possibly as a result of the shared burrow system. Clear seasonal patterns of parasite prevalence and abundance emerged with peaks in summer for mites and in winter for cestodes. Group size correlated negatively with mite abundance while it had no effect on cestode burdens and group membership affected infestation with both parasites. We propose that the mode of transmission as well as social factors constrain parasite propagation generating parasite patterns deviating from those commonly predicted.