A female-biased gene expression signature of dominance in cooperatively breeding meerkats.

Dominance is a primary determinant of social dynamics and resource access in social animals. Recent studies show that dominance is also reflected in the gene regulatory profiles of peripheral immune cells. However, the strength and direction of this relationship differs across the species and sex combinations investigated, potentially due to variation in the predictors and energetic consequences of dominance status. Here, we investigated the association between social status and gene expression in the blood of wild meerkats (Suricata suricatta; n = 113 individuals), including in response to lipopolysaccharide, Gardiquimod (an agonist of TLR7, which detects single-stranded RNA in vivo) and glucocorticoid stimulation. Meerkats are cooperatively breeding social carnivores in which breeding females physically outcompete other females to suppress reproduction, resulting in high reproductive skew. They therefore present an opportunity to disentangle the effects of social dominance from those of sex per se. We identify a sex-specific signature of dominance, including 1045 differentially expressed genes in females but none in males. Dominant females exhibit elevated activity in innate immune pathways and a larger fold-change response to LPS challenge. Based on these results and a preliminary comparison to other mammals, we speculate that the gene regulatory signature of social status in the immune system depends on the determinants and energetic costs of social dominance, such that it is most pronounced in hierarchies where physical competition is important and reproductive skew is large. Such a pattern has the potential to mediate life history trade-offs between investment in reproduction versus somatic maintenance.

Climate change drives loss of bacterial gut mutualists at the expense of host survival in wild meerkats.

Climate change and climate-driven increases in infectious disease threaten wildlife populations globally. Gut microbial responses are predicted to either buffer or exacerbate the negative impacts of these twin pressures on host populations. However, examples that document how gut microbial communities respond to long-term shifts in climate and associated disease risk, and the consequences for host survival, are rare. Over the past two decades, wild meerkats inhabiting the Kalahari have experienced rapidly rising temperatures, which is linked to the spread of tuberculosis (TB). We show that over the same period, the faecal microbiota of this population has become enriched in Bacteroidia and impoverished in lactic acid bacteria (LAB), a group of bacteria including Lactococcus and Lactobacillus that are considered gut mutualists. These shifts occurred within individuals yet were compounded over generations, and were better explained by mean maximum temperatures than mean rainfall over the previous year. Enriched Bacteroidia were additionally associated with TB exposure and disease, the dry season and poorer body condition, factors that were all directly linked to reduced future survival. Lastly, abundances of LAB taxa were independently and positively linked to future survival, while enriched taxa did not predict survival. Together, these results point towards extreme temperatures driving an expansion of a disease-associated pathobiome and loss of beneficial taxa. Our study provides the first evidence from a longitudinally sampled population that climate change is restructuring wildlife gut microbiota, and that these changes may amplify the negative impacts of climate change through the loss of gut mutualists. While the plastic response of host-associated microbiotas is key for host adaptation under normal environmental fluctuations, extreme temperature increases might lead to a breakdown of coevolved host-mutualist relationships.

Pregnancy reduces concurrent pup care behaviour in meerkats, generating differences between dominant and subordinate females.

In some mammals, and particularly in cooperative breeding ones, successive bouts of reproduction can overlap so that a female is often pregnant while still nurturing dependent young from her previous litter. Such an overlap requires females to divide their energetic budget between two reproductive activities, and pregnancy costs would consequently be expected to reduce investment in concurrent offspring care. However, explicit evidence for such reductions is scarce, and the potential effects they may have on work division in cooperative breeders have not been explored. Using 25 years of data on reproduction and cooperative behaviour in wild Kalahari meerkats, supplemented with field experiments, we investigated whether pregnancy reduces contributions to cooperative pup care behaviours, including babysitting, provisioning and raised guarding. We also explored whether pregnancy, which is more frequent in dominants than subordinates, could account for the reduced contributions of dominants to the cooperative pup care behaviours. We found that pregnancy, particularly at late stages of gestation, reduces contributions to cooperative pup care; that these reductions are eliminated when the food available to pregnant females is experimentally supplemented; and that pregnancy effects accounted for differences between dominants and subordinates in two of the three cooperative behaviours examined (pup provisioning and raised guarding but not babysitting). By linking pregnancy costs with reductions in concurrent pup care, our findings illuminate a trade-off between investment in successive, overlapping bouts of reproduction. They also suggest that some of the differences in cooperative behaviour between dominant and subordinate females in cooperative breeding mammals can be a direct consequence of differences in their breeding frequency.

Dispersal-induced social stress prolongs gestation in wild meerkats.

In the majority of mammals, gestation length is relatively consistent and seldom varies by more than 3%. In a few species, females can adjust gestation length by delaying the development of the embryo after implantation. Delays in embryonic development allow females to defer the rising energetic costs of gestation when conditions are unfavourable, reducing the risk of embryo loss. Dispersal in mammals that breed cooperatively is a period when food intake is likely to be suppressed and stress levels are likely to be high. Here, we show that pregnant dispersing meerkats (Suricata suricatta), which have been aggressively evicted from their natal group and experience weight loss and extended periods of social stress, prolong their gestation by means of delayed embryonic development. Repeated ultrasound scans of wild, unanaesthetized females throughout their pregnancies showed that pregnancies of dispersers were on average 6.3% longer and more variable in length (52-65 days) than those of residents (54-56 days). The variation in dispersers shows that, unlike most mammals, meerkats can adapt to stress by adjusting their pregnancy length by up to 25%. By doing so, they potentially rearrange the costs of gestation during adverse conditions of dispersal and enhance offspring survival.

Dispersal Decreases Survival but Increases Reproductive Opportunities for Subordinates in a Cooperative Breeder.

AbstractIn most socially structured populations, the formation of new groups depends on the survival and reproduction of dispersing individuals. Quantifying vital rates in dispersers, however, is difficult because of the logistic challenges of following wide-ranging animals. Here, using data from free-ranging meerkats (Suricata suricatta), we estimate survival and reproduction of dispersing females and compare these estimates to data for established residents. Meerkat groups consist of a dominant pair and several subordinate helpers. Female helpers are evicted from their resident groups by the dominant female, allowing her to monopolize reproduction, and evicted females may form small dispersing coalitions. We show that, as in established resident groups, one female is behaviorally dominant in parties of dispersing females. During dispersal and the first 4 months after new group formation, survival is lower for all females compared with established resident groups. At the same time, subordinates in disperser groups have higher birth rates than those in established groups, which rarely breed successfully. This may partly offset the survival costs of dispersal to subordinate females. Further studies of dispersal based on direct observation of dispersing animals are needed to explore the costs and benefits of dispersal in species with contrasting breeding systems.

Gut microbiota individuality is contingent on temporal scale and age in wild meerkats.

Inter-individual differences in gut microbiota composition are hypothesized to generate variation in host fitness-a premise for the evolution of host-gut microbe symbioses. However, recent evidence suggests that gut microbial communities are highly dynamic, challenging the notion that individuals harbour unique gut microbial phenotypes. Leveraging a long-term dataset of wild meerkats, we reconcile these concepts by demonstrating that the relative importance of identity for shaping gut microbiota phenotypes depends on the temporal scale. Across meerkat lifespan, year-to-year variation overshadowed the effects of identity and social group in predicting gut microbiota composition, with identity explaining on average less than 2% of variation. However, identity was the strongest predictor of microbial phenotypes over short sampling intervals (less than two months), predicting on average 20% of variation. The effect of identity was also dependent on meerkat age, with the gut microbiota becoming more individualized and stable as meerkats aged. Nevertheless, while the predictive power of identity was negligible after two months, gut microbiota composition remained weakly individualized compared to that of other meerkats for up to 1 year. These findings illuminate the degree to which individualized gut microbial signatures can be expected, with important implications for the time frames over which gut microbial phenotypes may mediate host physiology, behaviour and fitness in natural populations.

The role of selection and evolution in changing parturition date in a red deer population.

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 that evolutionary change underlies the most widely reported phenotypic response to climate change: the advancement of breeding times. In a wild population of red deer, average parturition date has advanced by nearly 2 weeks in 4 decades. Here, we quantify the contribution of plastic, demographic, and genetic components to this change. In particular, we quantify the role of direct phenotypic plasticity in response to increasing temperatures and the role of changes in the population structure. Importantly, we show that adaptive evolution likely played a role in the shift towards earlier parturition dates. The observed rate of evolution was consistent with a response to selection and was less likely to be due to genetic drift. Our study provides a rare example of observed rates of genetic change being consistent with theoretical predictions, although the consistency would not have been detected with a solely phenotypic analysis. It also provides, to our knowledge, the first evidence of both evolution and phenotypic plasticity contributing to advances in phenology in a changing climate.

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.

Phenological sensitivity to climate across taxa and trophic levels.

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 and aquatic phenological data sets, spatially matched to temperature and precipitation data, to quantify variation in climate sensitivity. The direction, magnitude and timing of climate sensitivity varied markedly among organisms within taxonomic and trophic groups. Despite this variability, we detected systematic variation in the direction and magnitude of phenological climate sensitivity. Secondary consumers showed consistently lower climate sensitivity than other groups. We used mid-century climate change projections to estimate that the timing of phenological events could change more for primary consumers than for species in other trophic levels (6.2 versus 2.5-2.9 days earlier on average), with substantial taxonomic variation (1.1-14.8 days earlier on average).

Multiple spatial behaviours govern social network positions in a wild ungulate.

The structure of wild animal social systems depends on a complex combination of intrinsic and extrinsic drivers. Population structuring and spatial behaviour are key determinants of individuals' observed social behaviour, but quantifying these spatial components alongside multiple other drivers remains difficult due to data scarcity and analytical complexity. We used a 43-year dataset detailing a wild red deer population to investigate how individuals' spatial behaviours drive social network positioning, while simultaneously assessing other potential contributing factors. Using Integrated Nested Laplace Approximation (INLA) multi-matrix animal models, we demonstrate that social network positions are shaped by two-dimensional landscape locations, pairwise space sharing, individual range size, and spatial and temporal variation in population density, alongside smaller but detectable impacts of a selection of individual-level phenotypic traits. These results indicate strong, multifaceted spatiotemporal structuring in this society, emphasising the importance of considering multiple spatial components when investigating the causes and consequences of sociality.

Group size increases inequality in cooperative behaviour.

In cooperatively breeding species where rearing effort is shared among multiple group members, increases in group size typically reduce average per capita contributions to offspring care by all group members (load-lightening) but it is not known how changes in group size affect the distribution of workload among group members. The socioeconomic collective action theory suggests that, in larger groups, the incentives for free riding are stronger, leading to greater inequalities in work division among group members. Here, we use the Gini index to measure inequality at the group level in the contributions of helpers to three different cooperative behaviours (babysitting, pup-provisioning and raised guarding) in groups of varying size in wild Kalahari meerkats (Suricata suricatta). In larger groups, inequality in helpers' contributions to cooperative activities and the frequency of free riding both increased. Elevated levels of inequality were generated partly as a result of increased differences in contributions to cooperative activities between helpers in different sex and age categories in larger groups. After controlling for the positive effect of group size on total provisioning, increasing levels of inequality in contributions were associated with reductions in total pup-provisioning conducted by the group. Reductions in total pup-provisioning were, in turn, associated with reductions in the growth and survival of pups (but pup growth and survival were not directly affected by inequality in provisioning). Our results support the prediction of collective action theory described above and show how the Gini index can be used to investigate the distribution of cooperative behaviour within the group.

Increases in glucocorticoids are sufficient but not necessary to increase cooperative burrowing in Damaraland mole-rats.

Despite widespread interest in the evolution of cooperative behaviour, the physiological mechanisms shaping their expression remain elusive. We tested the hypothesis that glucocorticoid (GC) hormones affect cooperative behaviour using captive Damaraland mole-rats (Fukomys damarensis), a cooperatively breeding mammal. Within groups, individuals routinely contribute to public goods that include foraging tunnels, which provide all group members access to the tubers of desert plants they feed on, communal food stores and nests. We found that experimental increases in glucocorticoid concentration (GCc) in non-breeding female helpers led them to be active for longer and to burrow more while active, raising their daily contributions to burrowing, but not food carrying or nest building. However, experimentally induced increases in burrowing did not lead to elevated GCc in helpers of both sexes. These results suggest that heightened GCc may stimulate some cooperative behaviours that are energetically demanding (a characteristic shared by many types of cooperative activities across species) but that the cooperative behaviours affected by GCc can also be regulated by other mechanisms.

Meerkat helpers buffer the detrimental effects of adverse environmental conditions on fecundity, growth and survival.

Recent comparative studies show that cooperative breeding is positively correlated with harsh and unpredictable environments and it is suggested that this association occurs because helpers buffer the negative effects of adverse ecological conditions on fitness. In the Kalahari, rainfall varies widely between- and within years, affecting primary production and the availability of the principal prey of cooperatively breeding Kalahari meerkats, Suricata suricatta. Our study aimed to establish whether the presence and number of helpers buffer the negative effects of variation in rainfall on the fecundity and body mass of breeding females, and the survival and growth of pups. We investigate the relationship between group size and variation in rainfall on dominant female fecundity, body mass, and offspring survival and growth using an additive modelling approach on 21 years of individual-based records of the life histories of individual meerkats. We show that breeding female fecundity is reduced during periods of low rainfall but that the effects of low rainfall are mitigated by increases in group size and body mass because heavier females and those in larger groups have increased fecundity and reduced interbirth intervals. Pup growth and survival are also reduced during periods of low rainfall, but only in smaller groups. Our results support the suggestion that cooperative breeding mitigates the detrimental effects of adverse environmental conditions and may enhance the capacity of species to occupy environments where food availability is low and unpredictable.

Behavioural change during dispersal and its relationship to survival and reproduction in a cooperative breeder.

The ability of dispersing individuals to adjust their behaviour to changing conditions is instrumental in overcoming challenges and reducing dispersal costs, consequently increasing overall dispersal success. Understanding how dispersers' behaviour and physiology change during the dispersal process, and how they differ from resident individuals, can shed light on the mechanisms by which dispersers increase survival and maximise reproduction. By analysing individual behaviour and concentrations of faecal glucocorticoid metabolites (fGCM), a stress-associated biomarker, we sought to identify the proximate causes behind differences in survival and reproduction between dispersing and resident meerkats Suricata suricatta. We used data collected on 67 dispersing and 108 resident females to investigate (a) which individual, social and environmental factors are correlated to foraging and vigilance, and whether the role of such factors differs among dispersal phases, and between dispersers and residents; (b) how time allocated to either foraging or vigilance correlated to survival in dispersers and residents and (c) the link between aggression and change in fGCM concentration, and their relationship with reproductive rates in dispersing groups and resident groups with either long-established or newly established dominant females. Time allocated to foraging increased across dispersal phases, whereas time allocated to vigilance decreased. Time allocated to foraging and vigilance correlated positively and negatively, respectively, with dispersers' group size. We did not find a group size effect for residents. High proportions of time allocated to foraging correlated with high survival, and more so in dispersers, suggesting that maintaining good physical condition may reduce mortality during dispersal. Furthermore, while subordinate individuals rarely reproduced in resident groups, the conception rate of subordinates in newly formed dispersing groups was equal to that of their dominant individuals. Mirroring conception rates, in resident groups, fGCM concentrations were lower in subordinates than in dominants, whereas in disperser groups, fGCM concentrations did not differ between subordinates and dominants. Our results, which highlight the relationship between behavioural and physiological factors and demographic rates, provide insights into some of the mechanisms that individuals of a cooperative species can use to increase overall dispersal success.

Sex-independent senescence in a cooperatively breeding mammal.

Researchers studying mammals have frequently interpreted earlier or faster rates of ageing in males as resulting from polygyny and the associated higher costs of reproductive competition. Yet, few studies conducted on wild populations have compared sex-specific senescence trajectories outside of polygynous species, making it difficult to make generalized inferences on the role of reproductive competition in driving senescence, particularly when other differences between males and females might also contribute to sex-specific changes in performance across lifespan. Here, we examine age-related variation in body mass, reproductive output and survival in dominant male and female meerkats, Suricata suricatta. Meerkats are socially monogamous cooperative breeders where a single dominant pair virtually monopolizes reproduction in each group and subordinate group members help to rear offspring produced by breeders. In contrast to many polygynous societies, we find that neither the onset nor the rate of senescence in body mass or reproductive output shows clear differences between males and females. Both sexes also display similar patterns of age-related survival across lifespan, but unlike most wild vertebrates, survival senescence (increases in annual mortality with rising age) was absent in dominants of both sexes, and as a result, the fitness costs of senescence were entirely attributable to declines in reproductive output from mid- to late-life. We suggest that the potential for intrasexual competition to increase rates of senescence in females-who are hormonally masculinized and frequently aggressive-is offset by their ability to maintain longer tenures of dominance than males, and that these processes when combined lead to similar patterns of senescence in both sexes. Our results stress the need to consider the form and intensity of sexual competition as well as other sex-specific features of life history when investigating the operation of senescence in wild populations.

Long-term movements and home-range changes: Rapid territory shifts in meerkats.

Territoriality and stable home ranges are a common space-use pattern among animals. These ranges provide its inhabitants with important resources and thus favourable territories are associated with an increased fitness. While the role of territory quality and changes of territory ownership have often been investigated, the changes of territorial boundaries have been less studied. Here, we investigated space-use changes in a social mammal species, applying a novel analytical approach, calculating long-term dissimilarity in space use using distancematrices based on periodic utilization distributions. This approach makes it possible to identify different space-use patterns, which cannot be distinguished by only considering changes between consecutive time periods. We analysed meerkat (Suricata suricatta) movements of a total of 24 different groups over a 16-year period, resulting in 134 group years. We then correlated the identified home-range changes to life-history events and possible environmental drivers. Groups had stable territories for several years before they abandoned their home range mostly to move quickly to new areas where they again remained for several years. Of 26 identified sudden shifts, 22 occurred in the summer months and often involved distances larger than the original home-range size. Home-range movements that were close together in time were often also spatially clustered and moved in a similar direction. These shifts were often preceded by more frequent interactions between groups, but did not seem to be a product of direct displacements by other groups. The normalized difference vegetation index as a measure of food production and social factors such as dominance changes did not correlate to changes. Against our expectation space-use changes were not accumulations of small changes, but more often involved long-distance moves into unknown ranges. This means that the groups enter areas where they cannot profit from local knowledge. The methods used identify episodes of long stability alternated by sudden changes in meerkats and in general provides insight into long-term space use. Our methods can be used to analyse long-term space use, either within or across species.

Breeders are less active foragers than non-breeders in wild Damaraland mole-rats.

Eusocial societies are characterized by a clear division of labour between non-breeding workers and breeding queens, and queens often do not contribute to foraging, defence and other maintenance tasks. It has been suggested that the structure and organization of social mole-rat groups resembles that of eusocial insect societies. However, the division of labour has rarely been investigated in wild mole-rats, and it is unknown whether breeders show decreased foraging activity compared with non-breeding helpers in natural groups. Here, we show that, in wild Damaraland mole-rats (Fukomys damarensis), breeders show lower activity in foraging areas than non-breeding group members. Both breeders and non-breeders displayed variation in activity across the different seasons. Our results suggest that group living allows social mole-rat breeders to reduce their investment in energetically costly behaviour, or alternatively, that the high cost of reproduction in this species forces a behavioural trade-off against foraging investment.

The Evolution of Indiscriminate Altruism in a Cooperatively Breeding Mammal.

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. Here, we show that meerkats (Suricata suricatta) are largely indiscriminate altruists who do not alter the amount of help provided to pups or group mates in response to their relatedness to them. We present a model showing that indiscriminate altruism may yield greater fitness payoffs than kin discrimination where most group members are close relatives and errors occur in the estimation of relatedness. The presence of errors in the estimation of relatedness provides a feasible explanation for associations between kin discriminative helping and group relatedness in eusocial and cooperatively breeding animals.

Intergroup aggression in meerkats.

Violent conflicts between groups have been observed among many species of group living mammals and can have important fitness consequences, with individuals being injured or killed and with losing groups surrendering territory. Here, we explore between-group conflict among meerkats (Suricata suricatta), a highly social and cooperatively breeding mongoose. We show that interactions between meerkat groups are frequently aggressive and sometimes escalate to fighting and lethal violence and that these interactions have consequences for group territories, with losing groups moving to sleeping burrows closer to the centre of their territories following an intergroup interaction and with winning groups moving further away. We find that larger groups and groups with pups are significantly more likely to win contests, but that the location of the contest, adult sex ratio, and mean within-group genetic relatedness do not predict contest outcome. Our results suggest that intergroup competition may be a major selective force among meerkats, reinforcing the success of large groups and increasing the vulnerability of small groups to extinction. The presence of both within-group cooperation and between-group hostility in meerkats make them a valuable point of comparison in attempts to understand the ecological and evolutionary roots of human warfare.

Cost of dispersal in a social mammal: body mass loss and increased stress.

Dispersal is a key process influencing the dynamics of socially and spatially structured populations. Dispersal success is determined by the state of individuals at emigration and the costs incurred after emigration. However, quantification of such costs is often difficult, due to logistical constraints of following wide-ranging individuals. We investigated the effects of dispersal on individual body mass and stress hormone levels in a cooperative breeder, the meerkat ( Suricata suricatta). We measured body mass and faecal glucocorticoid metabolite (fGCM) concentrations from 95 dispersing females in 65 coalitions through the entire dispersal process. Females that successfully settled lost body mass, while females that did not settle but returned to their natal group after a short period of time did not. Furthermore, dispersing females had higher fGCM levels than resident females, and this was especially pronounced during the later stages of dispersal. By adding information on the transient stage of dispersal and by comparing dispersers that successfully settled to dispersers that returned to their natal group, we expand on previous studies focusing on the earlier stages of dispersal. We propose that body mass and stress hormone levels are good indicators to investigate dispersal costs, as these traits often play an important role in mediating the effects of the environment on other life-history events and individual fitness.