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.

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.

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.

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.

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.

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.

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.

Signalling adjustments to direct and indirect environmental effects on signal perception in meerkats.

The efficiency of communication between animals is determined by the perception range of signals. With changes in the environment, signal transmission between a sender and a receiver can be influenced both directly, where the signal's propagation quality itself is affected, and indirectly where the senders or receivers' behaviour is impaired, impacting for example the distance between them. Here we investigated how meerkats (Suricata suricatta) in the Kalahari Desert adjust to these challenges in the context of maintaining group cohesion through contact calls. We found that meerkats changed their calling rate when signal transmission was affected indirectly due to increased dispersion of group members as during a drought, but not under typical wet conditions, when signal transmission was directly affected due to higher vegetation density. Instead under these wetter conditions, meerkats remained within proximity to each other. Overall, both direct and indirect environmental effects on signal perception resulted in an increased probability of groups splitting. In conclusion, we provide evidence that social animals can flexibly adjust their vocal coordination behaviour to cope with direct and indirect effects of the environment on signal perception, but these adjustments have limitations.

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.

Consistent within-individual plasticity is sufficient to explain temperature responses in red deer reproductive traits.

Warming global temperatures are affecting a range of aspects of wild populations, but the exact mechanisms driving associations between temperature and phenotypic traits may be difficult to identify. Here, we use a 36-year data set on a wild population of red deer to investigate the causes of associations between temperature and two important components of female reproduction: timing of breeding and offspring size. By separating within- versus between-individual associations with temperature for each trait, we show that within-individual phenotypic plasticity (changes within a female's lifetime) was entirely sufficient to generate the observed population-level association with temperature at key times of year. However, despite apparently adequate statistical power, we found no evidence of any variation between females in their responses (i.e. no "IxE" interactions). Our results suggest that female deer show plasticity in reproductive traits in response to temperatures in the year leading up to calving and that this response is consistent across individuals, implying no potential for either selection or heritability of plasticity. We estimate that the plastic response to rising temperatures explained 24% of the observed advance in mean calving date over the study period. We highlight the need for comparable analyses of other systems to determine the contribution of within-individual plasticity to population-level responses to climate change.

The development of individual differences in cooperative behaviour: maternal glucocorticoid hormones alter helping behaviour of offspring in wild meerkats.

The phenotype of parents can have long-lasting effects on the development of offspring as well as on their behaviour, physiology and morphology as adults. In some cases, these changes may increase offspring fitness but, in others, they can elevate parental fitness at a cost to the fitness of their offspring. We show that in Kalahari meerkats ( Suricata suricatta), the circulating glucocorticoid (GC) hormones of pregnant females affect the growth and cooperative behaviour of their offspring. We performed a 3-year experiment in wild meerkats to test the hypothesis that GC-mediated maternal effects reduce the potential for offspring to reproduce directly and therefore cause them to exhibit more cooperative behaviour. Daughters (but not sons) born to mothers treated with cortisol during pregnancy grew more slowly early in life and exhibited significantly more of two types of cooperative behaviour (pup rearing and feeding) once they were adults compared to offspring from control mothers. They also had lower measures of GCs as they aged, which could explain the observed increases in cooperative behaviour. Because early life growth is a crucial determinant of fitness in female meerkats, our results indicate that GC-mediated maternal effects may reduce the fitness of offspring, but may elevate parental fitness as a consequence of increasing the cooperative behaviour of their daughters. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

Male immigration triggers increased growth in subordinate female meerkats.

There is increasing evidence that some vertebrates can adjust their growth rate in relation to changes in the social context that affect their probability of breeding. Here, we show that, in meerkats (Suricata suricatta), which are singular cooperative breeders, subordinate females increase in body mass after their father is replaced as the dominant male in their natal group by an immigrant male, giving them regular access to an unfamiliar and unrelated mating partner, while their brothers showed no similar increase nor did subordinate females living in other stable groups (where male immigration did not occur did) in this time period. Moreover, subordinate females showed a greater increase in growth rate when their father was succeeded by an unfamiliar immigrant male than when he was replaced by a familiar male who was already resident. These results suggest that female meerkats can adjust their rate of growth to changes in the kinship composition of their groups that provide them with increased access to unrelated breeding partners, which may occur in other mammals as well when breeding opportunities change.

Social and endocrine correlates of immune function in meerkats: implications for the immunocompetence handicap hypothesis.

Social status can mediate effects on the immune system, with profound consequences for individual health; nevertheless, most investigators of status-related disparities in free-ranging animals have used faecal parasite burdens to proxy immune function in the males of male-dominant species. We instead use direct measures of innate immune function (complement and natural antibodies) to examine status-related immunocompetence in both sexes of a female-dominant species. The meerkat is a unique model for such a study because it is a cooperatively breeding species in which status-related differences are extreme, evident in reproductive skew, morphology, behaviour, communication and physiology, including that dominant females naturally express the greatest total androgen (androstenedione plus testosterone) concentrations. We found that, relative to subordinates, dominant animals had reduced serum bacteria-killing abilities; also, relative to subordinate females, dominant females had reduced haemolytic complement activities. Irrespective of an individual's sex or social status, androstenedione concentrations (but not body condition, age or reproductive activity) negatively predicted concurrent immunocompetence. Thus, dominant meerkats of both sexes are immunocompromised. Moreover, in female meerkats, androstenedione perhaps acting directly or via local conversion, may exert a double-edged effect of promoting dominance and reproductive success at the cost of increased parasitism and reduced immune function. Given the prominent signalling of dominance in female meerkats, these findings may relate to the immunocompetence handicap hypothesis (ICHH); however, our data would suggest that the endocrine mechanism underlying the ICHH need not be mediated solely by testosterone and might explain trade-offs in females, as well as in males.

Matrix Models of Hierarchical Demography: Linking Group- and Population-Level Dynamics in Cooperative Breeders.

For highly social species, population dynamics depend on hierarchical demography that links local processes, group dynamics, and population growth. Here, we describe a stage-structured matrix model of hierarchical demography, which provides a framework for understanding social influences on population change. Our approach accounts for dispersal and affords insight into population dynamics at multiple scales. The method has close parallels to integral projection models but focuses on a discrete characteristic (group size). Using detailed long-term records for meerkats (Suricata suricatta), we apply our model to explore patterns of local density dependence and implications of group size for group and population growth. Taking into account dispersers, the model predicts a per capita growth rate for social groups that declines with group size. It predicts that larger social groups should produce a greater number of new breeding groups; thus, dominant breeding females (responsible for most reproduction) are likely to be more productive in larger groups. Considering the potential for future population growth, larger groups have the highest reproductive value, but per capita reproductive value is maximized for individuals in smaller groups. Across a plausible range of dispersal conditions, meerkats' long-run population growth rate is maximized when individuals form groups of intermediate size.

Declining home range area predicts reduced late-life survival in two wild ungulate populations.

Demographic senescence is increasingly recognised as an important force shaping the dynamics of wild vertebrate populations. However, our understanding of the processes that underpin these declines in survival and fertility in old age remains limited. Evidence for age-related changes in foraging behaviour and habitat use is emerging from wild vertebrate studies, but the extent to which these are driven by within-individual changes, and the consequences for fitness, remain unclear. Using longitudinal census observations collected over four decades from two long-term individual-based studies of unmanaged ungulates, we demonstrate consistent within-individual declines in home range area with age in adult females. In both systems, we found that within-individual decreases in home range area were associated with increased risk of mortality the following year. Our results provide the first evidence from the wild that age-related changes in space use are predictive of adult mortality.