Dominance loss and tenure maintenance in Kalahari meerkats.

In many social species, both the acquisition of dominance and the duration that individuals maintain their status are important determinants of breeding tenure and lifetime reproductive success. However, few studies have yet examined the extent and causes of variation in dominance tenure and the duration of breeding lifespans. Here, we investigate the processes that terminate dominance tenures and examine how they differ between the sexes in wild Kalahari meerkats (Suricata suricatta), a cooperative breeder where a dominant breeding pair produces most of the young recruited into each group. Mortality and displacement by resident subordinate competitors were important forms of dominance loss for both sexes. However, dominant males (but rarely females) were also at risk of takeovers by extra-group invading males. Dominant males also differed from dominant females in that they abandoned their group after the death of their breeding partner, when no other breeding opportunities were present, whereas dominant females that lost their partner remained and continued to breed in the same group. We show that a larger number of processes can terminate dominance tenure in males with the result that the average male tenure of breeding positions was shorter than that of females, which contributes to the reduced variance in the lifetime reproductive success in males compared to females. Our analysis suggests that sex differences in emigration and immigration may often have downstream consequences for sex differences in reproductive variance and for the selection pressures operating on females and males.

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.

Damaraland mole-rats do not rely on helpers for reproduction or survival.

In eusocial invertebrates and obligate cooperative breeders, successful reproduction is dependent on assistance from non-breeding group members. Although naked (Heterocephalus glaber) and Damaraland mole-rats (Fukomys damarensis) are often described as eusocial and their groups are suggested to resemble those of eusocial insects more closely than groups of any other vertebrate, the extent to which breeding individuals benefit from the assistance of non-breeding group members is unclear. Here we show that, in wild Damaraland mole-rats, prospective female breeders usually disperse and settle alone in new burrow systems where they show high survival rates and remain in good body condition-often for several years-before being joined by males. In contrast to many obligate cooperative vertebrates, pairs reproduced successfully without non-breeding helpers, and the breeding success of experimentally formed pairs was similar to that of larger, established groups. Though larger breeding groups recruited slightly more pups than smaller groups, adult survival was independent of group size and group size had mixed effects on the growth of non-breeders. Our results suggest that Damaraland mole-rats do not need groups to survive and that cooperative breeding in the species is not obligate as pairs can-and frequently do-reproduce without the assistance of helpers. While re-emphasizing the importance of ecological constraints on dispersal in social mole-rats, the mixed effects of group size in our study suggest that indirect benefits accrued through cooperative behavior may have played a less prominent role in the evolution of mole-rat group-living than previously thought.

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.

Turnover in male dominance offsets the positive effect of polygyny on within-group relatedness.

Evidence of an association between cooperative breeding systems and average coefficients of relatedness between group members in vertebrates have led to increased interest in the social and ecological factors affecting average kinship within groups. Previous studies have suggested that polygynous mating systems and high degrees of male reproductive skew increase average relatedness because they increase the proportion of offspring born in each group that are paternal siblings. Although this may be the case in semelparous organisms, in many multiparous polygynous animals, intense competition between males shortens the breeding tenure of males and leads to their frequent replacement by competitors which reduces paternal relatedness and average kinship between members of multigenerational groups. Here, we explore the interaction between male reproductive skew and the frequency of turnover in breeding males and its effects on within-group relatedness. Our theoretical model shows that increases in rates of dominance turnover in polygynous systems can offset the positive effect of male skew on relatedness between group members within seasons, showing that polygynous mating systems will not necessarily lead to significant increases in average relatedness, especially in species where there is extensive overlap between generations among group members.

Demographic consequences of changes in environmental periodicity.

The fate of natural populations is mediated by complex interactions among vital rates, which can vary within and among years. Although the effects of random, among-year variation in vital rates have been studied extensively, relatively little is known about how periodic, nonrandom variation in vital rates affects populations. This knowledge gap is potentially alarming as global environmental change is projected to alter common periodic variations, such as seasonality. We investigated the effects of changes in vital-rate periodicity on populations of three species representing different forms of adaptation to periodic environments: the yellow-bellied marmot (Marmota flaviventer), adapted to strong seasonality in snowfall; the meerkat (Suricata suricatta), adapted to inter-annual stochasticity as well as seasonal patterns in rainfall; and the dewy pine (Drosophyllum lusitanicum), adapted to fire regimes and periodic post-fire habitat succession. To assess how changes in periodicity affect population growth, we parameterized periodic matrix population models and projected population dynamics under different scenarios of perturbations in the strength of vital-rate periodicity. We assessed the effects of such perturbations on various metrics describing population dynamics, including the stochastic growth rate, log λS . Overall, perturbing the strength of periodicity had strong effects on population dynamics in all three study species. For the marmots, log λS decreased with increased seasonal differences in adult survival. For the meerkats, density dependence buffered the effects of perturbations of periodicity on log λS . Finally, dewy pines were negatively affected by changes in natural post-fire succession under stochastic or periodic fire regimes with fires occurring every 30 years, but were buffered by density dependence from such changes under presumed more frequent fires or large-scale disturbances. We show that changes in the strength of vital-rate periodicity can have diverse but strong effects on population dynamics across different life histories. Populations buffered from inter-annual vital-rate variation can be affected substantially by changes in environmentally driven vital-rate periodic patterns; however, the effects of such changes can be masked in analyses focusing on inter-annual variation. As most ecosystems are affected by periodic variations in the environment such as seasonality, assessing their contributions to population viability for future global-change research is crucial.

Two decades of tuberculosis surveillance reveal disease spread, high levels of exposure and mortality and marked variation in disease progression in wild meerkats.

Infections with tuberculosis (TB)-causing agents of the Mycobacterium tuberculosis complex threaten human, livestock and wildlife health globally due to the high capacity to cross trans-species boundaries. Tuberculosis is a cryptic disease characterized by prolonged, sometimes lifelong subclinical infections, complicating disease monitoring. Consequently, our understanding of infection risk, disease progression, and mortality across species affected by TB remains limited. The TB agent Mycobacterium suricattae was first recorded in the late 1990s in a wild population of meerkats inhabiting the Kalahari in South Africa and has since spread considerably, becoming a common cause of meerkat mortality. This offers an opportunity to document the epidemiology of naturally spreading TB in a wild population. Here, we synthesize more than 25 years' worth of TB reporting and social interaction data across 3420 individuals to track disease spread, and quantify rates of TB social exposure, progression, and mortality. We found that most meerkats had been exposed to the pathogen within eight years of first detection in the study area, with exposure reaching up to 95% of the population. Approximately one quarter of exposed individuals progressed to clinical TB stages, followed by physical deterioration and death within a few months. Since emergence, 11.6% of deaths were attributed to TB, although the true toll of TB-related mortality is likely higher. Lastly, we observed marked variation in disease progression among individuals, suggesting inter-individual differences in both TB susceptibility and resistance. Our results highlight that TB prevalence and mortality could be higher than previously reported, particularly in species or populations with complex social group dynamics. Long-term studies, such as the present one, allow us to assess temporal variation in disease prevalence and progression and quantify exposure, which is rarely measured in wildlife. Long-term studies are highly valuable tools to explore disease emergence and ecology and study host-pathogen co-evolutionary dynamics in general, and its impact on social mammals.

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.

Ageing red deer alter their spatial behaviour and become less social.

Social relationships are important to many aspects of animals' lives, and an individual's connections may change over the course of their lifespan. Currently, it is unclear whether social connectedness declines within individuals as they age, and what the underlying mechanisms might be, so the role of age in structuring animal social systems remains unresolved, particularly in non-primates. Here we describe senescent declines in social connectedness using 46 years of data in a wild, individually monitored population of a long-lived mammal (European red deer, Cervus elaphus). Applying a series of spatial and social network analyses, we demonstrate that these declines occur because of within-individual changes in social behaviour, with correlated changes in spatial behaviour (smaller home ranges and movements to lower-density, lower-quality areas). These findings demonstrate that within-individual socio-spatial behavioural changes can lead older animals in fission-fusion societies to become less socially connected, shedding light on the ecological and evolutionary processes structuring wild animal populations.

Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals.

The rate of adaptive evolution, the contribution of selection to genetic changes that increase mean fitness, is determined by the additive genetic variance in individual relative fitness. To date, there are few robust estimates of this parameter for natural populations, and it is therefore unclear whether adaptive evolution can play a meaningful role in short-term population dynamics. We developed and applied quantitative genetic methods to long-term datasets from 19 wild bird and mammal populations and found that, while estimates vary between populations, additive genetic variance in relative fitness is often substantial and, on average, twice that of previous estimates. We show that these rates of contemporary adaptive evolution can affect population dynamics and hence that natural selection has the potential to partly mitigate effects of current environmental change.

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.

Strategic growth in social vertebrates.

Individual differences in growth and size of vertebrates often represent adaptive, plastic responses to contrasts in ecological conditions. Recent studies show that vertebrates can also modify their growth and size in an adaptive fashion in response to fine-grain changes in social conditions (which we refer to as strategic growth). Here, we review experimental evidence for strategic growth in social vertebrates. We describe a set of conditions under which strategic growth commonly occurs, and highlight potential examples of convergent evolution of strategic growth across the tree of life. This synthesis has implications for the way we think about organismal growth and size, because it underscores that the size of individuals can often be fine-tuned to their social environment.

CHARACTERIZING TUBERCULOSIS PROGRESSION IN WILD MEERKATS (SURICATA SURICATTA) FROM FECAL SAMPLES AND CLINICAL SIGNS.

Tuberculosis (TB) is an increasing threat to wildlife, yet tracking its spread is challenging because infections often appear to be asymptomatic, and diagnostic tools such as blood tests can be invasive and resource intensive. Our understanding of TB biology in wildlife is therefore limited to a small number of well-studied species. Testing of fecal samples using PCR is a noninvasive method that has been used to detect Mycobacterium bovis shedding amongst badgers, yet its utility more broadly for TB monitoring in wildlife is unclear. We combined observation data of clinical signs with PCR testing of 388 fecal samples to characterize longitudinal dynamics of TB progression in 66 wild meerkats (Suricata suricatta) socially exposed to Mycobacterium suricattae between 2000 and 2018. Our specific objectives were 1) to test whether meerkat fecal samples can be used to monitor TB; 2) to characterize TB progression between three infection states (PCR-negative exposed, PCR-positive asymptomatic, and PCR positive with clinical signs); and 3) estimate individual heterogeneity in TB susceptibility, defined here as the time between TB exposure and detection, and survival after TB detection. We found that the TB detection probability once meerkats developed clinical signs was 13% (95% confidence interval 3-46%). Nevertheless, with an adapted test protocol of 10 PCR replicates per sample we detected hidden TB infections in 59% of meerkats before the onset of clinical signs. Meerkats became PCR positive approximately 14 mo after initial exposure, developed clinical signs approximately 1 yr after becoming PCR positive, and died within 5 mo of developing clinical signs. Individual variation in disease progression was high, with meerkats developing clinical signs from immediately after exposure to 3.4 yr later. Overall, our study generates novel insights into wildlife TB progression, and may help guide adapted management strategies for TB-susceptible wildlife populations.

Trait-Based Vaccination of Individual Meerkats (Suricata suricatta) against Tuberculosis Provides Evidence to Support Targeted Disease Control.

Individuals vary in their potential to acquire and transmit infections, but this fact is currently underexploited in disease control strategies. We trialled a trait-based vaccination strategy to reduce tuberculosis in free-living meerkats by targeting high-contact meerkats (socially dominant individuals) in one study arm, and high-susceptibility individuals (young subordinates) in a second arm. We monitored infection within vaccinated groups over two years comparing the results with untreated control groups. Being a member of a high-contact group had a protective effect on individuals' survival times (Hazard Ratio = 0.5, 95% Confidence Interval, CI: 0.29-0.88, p = 0.02) compared to control groups. Over the study, odds of testing positive for tuberculosis increased more than five-fold in control groups (Odds Ratio = 5.40, 95% CI = 0.94-30.98, p = 0.058); however, no increases were observed in either of the treatment arms. Targeted disease control approaches, such as the one described in this study, allow for reduced numbers of interventions. Here, trait-based vaccination was associated with reduced infection rates and thus has the potential to offer more efficient alternatives to traditional mass-vaccination policies. Such improvements in efficiency warrant further study and could make infectious disease control more practically achievable in both animal (particularly wildlife) and human populations.

Combining Analytical Approaches and Multiple Sources of Information to Improve Interpretation of Diagnostic Test Results for Tuberculosis in Wild Meerkats.

Diagnostic tests are used to classify individual animals' infection statuses. However, validating test performance in wild animals without gold standard tests is extremely challenging, and the issue is further complicated in chronic conditions where measured immune parameters vary over time. Here, we demonstrate the value of combining evidence from different diagnostic approaches to aid interpretation in the absence of gold standards, large sample sizes, and controlled environments. Over a two-year period, we sampled 268 free-living meerkats (Suricata suricatta) longitudinally for Mycobacterium suricattae (a causative agent of tuberculosis), using three ante-mortem diagnostic tests based on mycobacterial culture, and antigen-specific humoral and cell-mediated immune responses, interpreting results both independently and in combination. Post-mortem cultures confirmed M. suricattae infection in 22 animals, which had prior ante-mortem information, 59% (13/22) of which were test-positive on a parallel test interpretation (PTI) of the three ante-mortem diagnostic assays (95% confidence interval: 37-79%). A similar ability to detect infection, 65.7% (95% credible interval: 42.7-84.7%), was estimated using a Bayesian approach to examine PTI. Strong evidence was found for a near doubling of the hazard of death (Hazard Ratio 1.75, CI: 1.14-2.67, p = 0.01), associated with a positive PTI result, thus demonstrating that these test results are related to disease outcomes. For individual tests, small sample sizes led to wide confidence intervals, but replication of conclusions, using different methods, increased our confidence in these results. This study demonstrates that combining multiple methodologies to evaluate diagnostic tests in free-ranging wildlife populations can be a useful approach for exploiting such valuable datasets.

An intergenerational androgenic mechanism of female intrasexual competition in the cooperatively breeding meerkat.

Female intrasexual competition can be intense in cooperatively breeding species, with some dominant breeders (matriarchs) limiting reproduction in subordinates via aggression, eviction or infanticide. In males, such tendencies bidirectionally link to testosterone, but in females, there has been little systematic investigation of androgen-mediated behaviour within and across generations. In 22 clans of wild meerkats (Suricata suricatta), we show that matriarchs 1) express peak androgen concentrations during late gestation, 2) when displaying peak feeding competition, dominance behaviour, and evictions, and 3) relative to subordinates, produce offspring that are more aggressive in early development. Late-gestation antiandrogen treatment of matriarchs 4) specifically reduces dominance behaviour, is associated with infrequent evictions, decreases social centrality within the clan, 5) increases aggression in cohabiting subordinate dams, and 6) reduces offspring aggression. These effects implicate androgen-mediated aggression in the operation of female sexual selection, and intergenerational transmission of masculinised phenotypes in the evolution of meerkat cooperative breeding.

Decline and fall: The causes of group failure in cooperatively breeding meerkats.

In many social vertebrates, variation in group persistence exerts an important effect on individual fitness and population demography. However, few studies have been able to investigate the failure of groups or the causes of the variation in their longevity. We use data from a long-term study of cooperatively breeding meerkats, Suricata suricatta, to investigate the different causes of group failure and the factors that drive these processes. Many newly formed groups failed within a year of formation, and smaller groups were more likely to fail. Groups that bred successfully and increased their size could persist for several years, even decades. Long-lived groups principally failed in association with the development of clinical tuberculosis, Mycobacterium suricattae, a disease that can spread throughout the group and be fatal for group members. Clinical tuberculosis was more likely to occur in groups that had smaller group sizes and that had experienced immigration.

Diurnal oscillations in gut bacterial load and composition eclipse seasonal and lifetime dynamics in wild meerkats.

Circadian rhythms in gut microbiota composition are crucial for metabolic function, yet the extent to which they govern microbial dynamics compared to seasonal and lifetime processes remains unknown. Here, we investigate gut bacterial dynamics in wild meerkats (Suricata suricatta) over a 20-year period to compare diurnal, seasonal, and lifetime processes in concert, applying ratios of absolute abundance. We found that diurnal oscillations in bacterial load and composition eclipsed seasonal and lifetime dynamics. Diurnal oscillations were characterised by a peak in Clostridium abundance at dawn, were associated with temperature-constrained foraging schedules, and did not decay with age. Some genera exhibited seasonal fluctuations, whilst others developed with age, although we found little support for microbial senescence in very old meerkats. Strong microbial circadian rhythms in this species may reflect the extreme daily temperature fluctuations typical of arid-zone climates. Our findings demonstrate that accounting for circadian rhythms is essential for future gut microbiome research.

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.