The adaptive immune response to Trichuris in wild versus laboratory mice: An established model system in context.

Laboratory model organisms have provided a window into how the immune system functions. An increasing body of evidence, however, suggests that the immune responses of naive laboratory animals may differ substantially to those of their wild counterparts. Past exposure, environmental challenges and physiological condition may all impact on immune responsiveness. Chronic infections of soil-transmitted helminths, which we define as establishment of adult, fecund worms, impose significant health burdens on humans, livestock and wildlife, with limited treatment success. In laboratory mice, Th1 versus Th2 immune polarisation is the major determinant of helminth infection outcome. Here we compared antigen-specific immune responses to the soil-transmitted whipworm Trichuris muris between controlled laboratory and wild free-ranging populations of house mice (Mus musculus domesticus). Wild mice harbouring chronic, low-level infections produced lower levels of cytokines in response to Trichuris antigen than laboratory-housed C57BL/6 mice. Wild mouse effector/memory CD4+ T cell phenotype reflected the antigen-specific cytokine response across the Th1/Th2 spectrum. Increasing egg shedding was associated with body condition loss. However, local Trichuris-specific Th1/Th2 balance was positively associated with worm burden only in older wild mice. Thus, although the fundamental relationships between the CD4+ T helper cell response and resistance to T. muris infection are similar in both laboratory and wild M. m. domesticus, there are quantitative differences and age-specific effects that are analogous to human immune responses. These context-dependent immune responses demonstrate the fundamental importance of understanding the differences between model and natural systems for translating mechanistic models to 'real world' immune function.

Linking diet switching to reproductive performance across populations of two critically endangered mammalian herbivores.

Optimal foraging theory predicts that animals maximise energy intake by consuming the most valuable foods available. When resources are limited, they may include lower-quality fallback foods in their diets. As seasonal herbivore diet switching is understudied, we evaluate its extent and effects across three Kenyan reserves each for Critically Endangered eastern black rhino (Diceros bicornis michaeli) and Grevy's zebra (Equus grevyi), and its associations with habitat quality, microbiome variation, and reproductive performance. Black rhino diet breadth increases with vegetation productivity (NDVI), whereas zebra diet breadth peaks at intermediate NDVI. Black rhino diets associated with higher vegetation productivity have less acacia (Fabaceae: Vachellia and Senegalia spp.) and more grass suggesting that acacia are fallback foods, upending conventional assumptions. Larger dietary shifts are associated with longer calving intervals. Grevy's zebra diets in high rainfall areas are consistently grass-dominated, whereas in arid areas they primarily consume legumes during low vegetation productivity periods. Whilst microbiome composition between individuals is affected by the environment, and diet composition in black rhino, seasonal dietary shifts do not drive commensurate microbiome shifts. Documenting diet shifts across ecological gradients can increase the effectiveness of conservation by informing habitat suitability models and improving understanding of responses to resource limitation.

The paradox of spring: Thyroid and glucocorticoid responses to cold temperatures and food availability in free living Carneddau ponies.

In seasonal environments, maintaining a constant body temperature poses challenges for endotherms. Cold winters at high latitudes, with limited food availability, create opposing demands on metabolism: upregulation preserves body temperature but depletes energy reserves. Examining endocrine profiles, such as thyroid hormone triiodothyronine (T3) and glucocorticoids (GCs), proxies for changes in metabolic rate and acute stressors, offer insights into physiological trade-offs. We evaluated how environmental conditions and gestation impact on faecal hormone metabolites (fT3Ms and fGCMs) from late winter to spring in a free-living population of Carneddau ponies. Faecal T3Ms were highest in late February and March, when temperatures were lowest. Then, fT3Ms concentrations decreased throughout April and were at the lowest in May before increasing towards the end of the study. The decline in fT3M levels in April and May was associated with warmer weather but poor food availability, diet diversity and diet composition. On the other hand, fGCM levels did not display a clear temporal pattern but were associated with reproductive status, where pregnant and lactating females had higher fGCM levels as compared to adult males and non-reproductive females. The temporal profile of fT3Ms levels highlights metabolic trade-offs in a changing environment. In contrast, the ephemeral but synchronous increase in fGCM concentrations across the population suggest a shared experience of acute stressors (i.e., weather, disturbance or social). This multi-biomarker approach can evaluate the role of acute stressors versus energy budgets in the context of interventions, reproduction, seasonality and environmental change, or across multiple scales from individuals to populations.

Four errors and a fallacy: pitfalls for the unwary in comparative brain analyses.

Comparative analyses are the backbone of evolutionary analysis. However, their record in producing a consensus has not always been good. This is especially true of attempts to understand the factors responsible for the evolution of large brains, which have been embroiled in an increasingly polarised debate over the past three decades. We argue that most of these disputes arise from a number of conceptual errors and associated logical fallacies that are the result of a failure to adopt a biological systems-based approach to hypothesis-testing. We identify four principal classes of error: a failure to heed Tinbergen's Four Questions when testing biological hypotheses, misapplying Dobzhansky's Dictum when testing hypotheses of evolutionary adaptation, poorly chosen behavioural proxies for underlying hypotheses, and the use of inappropriate statistical methods. In the interests of progress, we urge a more careful and considered approach to comparative analyses, and the adoption of a broader, rather than a narrower, taxonomic perspective.

Ecological marginalization is widespread and increases extinction risk in mammals.

Human land-use results in widespread range change across taxa. Anthropogenic pressures can result in species' realized niches expanding, shifting, or contracting. Marginalization occurs when contraction constrains species to the geographic or ecological extremes of their historic niche. Using 4,785 terrestrial mammal species, we show that range contraction results in niche space and habitat diversity loss. Additionally, ecological marginalization is a common consequence of range contraction caused by human land use change. Remnant populations become located in the climatic and topographic extremes of their historic niche that are more likely to be at the periphery of their historic niche at greater distances from historic niche centroids. This ecological marginalization is associated with poor performance and increased extinction risk independent of geographic range loss. Range loss and marginalization may create a "double whammy" in vulnerable groups, such as large-bodied species and species with small geographical range size. Our results reveal a hitherto unrecognized conservation threat that is vital to incorporate into conservation assessment and management.

Socioecological complexity in primate groups and its cognitive correlates.

Characterizing non-human primate social complexity and its cognitive bases has proved challenging. Using principal component analyses, we show that primate social, ecological and reproductive behaviours condense into two components: socioecological complexity (including most social and ecological variables) and reproductive cooperation (comprising mainly a suite of behaviours associated with pairbonded monogamy). We contextualize these results using a meta-analysis of 44 published analyses of primate brain evolution. These studies yield two main consistent results: cognition, sociality and cooperative behaviours are associated with absolute brain volume, neocortex size and neocortex ratio, whereas diet composition and life history are consistently associated with relative brain size. We use a path analysis to evaluate the causal relationships among these variables, demonstrating that social group size is predicted by the neocortex, whereas ecological traits are predicted by the volume of brain structures other than the neocortex. That a range of social and technical behaviours covary, and are correlated with social group size and brain size, suggests that primate cognition has evolved along a continuum resulting in an increasingly flexible, domain-general capacity to solve a range of socioecological challenges culminating in a capacity for, and reliance on, innovation and social information use in the great apes and humans. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Female reproductive skew exacerbates the extinction risk from poaching in the eastern black rhino.

Variation in individual demographic rates can have large consequences for populations. Female reproductive skew is an example of structured demographic heterogeneity where females have intrinsic qualities that make them more or less likely to breed. The consequences of reproductive skew for population dynamics are poorly understood in non-cooperatively breeding mammals, especially when coupled with other drivers such as poaching. We address this knowledge gap with population viability analyses using an age-specific, female-only, individual-based, stochastic population model built with long-term data for three Kenyan populations of the Critically Endangered eastern black rhino (Diceros bicornis michaeli). There was substantial reproductive skew, with a high proportion of females not breeding or doing so at very low rates. This had a large impact on the projected population growth rate for the smaller population on Ol Jogi. Moreover, including female reproductive skew exacerbates the effects of poaching, increasing the probability of extinction by approximately 70% under a simulated poaching pressure of 5% offtake per year. Tackling the effects of reproductive skew depends on whether it is mediated by habitat or social factors, with potential strategies including habitat and biological management respectively. Investigating and tackling reproductive skew in other species requires long-term, individual-level data collection.

Untapped potential of physiology, behaviour and immune markers to predict range dynamics and marginality.

Linking environmental conditions to the modulators of individual fitness is necessary to predict long-term population dynamics, viability, and resilience. Functional physiological, behavioral, and reproductive markers can provide this mechanistic insight into how individuals perceive physiological, psychological, chemical, and physical environmental challenges through physiological and behavioral responses that are fitness proxies. We propose a Functional Marginality framework where relative changes in allostatic load, reproductive health, and behavior can be scaled up to evidence and establish causation of macroecological processes such as local extirpation, colonization, population dynamics, and range dynamics. To fully exploit functional traits, we need to move beyond single biomarker studies to develop an integrative approach that models the interactions between extrinsic challenges, physiological, and behavioral pathways and their modulators. In addition to providing mechanistic markers of range dynamics, this approach can also serve as a valuable conservation tool for evaluating individual- and population-level health, predicting responses to future environmental change and measuring the impact of interventions. We highlight specific studies that have used complementary biomarkers to link extrinsic challenges to population performance. These frameworks of integrated biomarkers have untapped potential to identify causes of decline, predict future changes, and mitigate against future biodiversity loss.

Fecal Bacterial Community of Allopatric Przewalski's Gazelles and Their Sympatric Relatives.

Mammal gastrointestinal tracts harbor diverse bacterial communities that play important roles in digestion, development, behavior, and immune function. Although, there is an increasing understanding of the factors that affect microbial community composition in laboratory populations, the impact of environment and host community composition on microbiomes in wild populations is less understood. Given that the composition of bacterial communities can be shaped by ecological factors, particularly exposure to the microbiome of other individuals, inter-specific interactions should impact on microbiome community composition. Here, we evaluated inter-population and inter-specific similarity in the fecal microbiota of Przewalski's gazelle (Procapra przewalskii), an endangered endemic ruminant around Qinghai Lake in China. We compared the fecal bacterial communities of three Przewalski's gazelle populations, with those of two sympatric ruminants, Tibetan gazelle (Procapra picticaudata) and Tibetan sheep (Ovis aries). The fecal bacterial community richness (Chao1, ACE) did not vary across the three Przewalski's gazelle populations, nor did the composition vary between species. In contrast, the managed Przewalski's gazelle population had higher bacterial diversity (Shannon and Simpson) and was more similar to its sympatric Tibetan sheep in beta diversity than the wild Przewalski's gazelle populations. These results suggest that ecological factors like host community composition or diet affect Przewalski's gazelle's gastrointestinal bacterial community. The role of bacterial community composition in maintaining gastrointestinal health should be assessed to improve conservation management of endangered Przewalski's gazelle. More broadly, captive breeding and reintroduction efforts may be impeded, where captive management results in dysbiosis and introduction of pathogenic bacteria. In free ranging populations, where wildlife and livestock co-occur, infection by domestic pathogens and diseases may be an underappreciated threat to wild animals.

Fungal microbiomes are determined by host phylogeny and exhibit widespread associations with the bacterial microbiome.

Interactions between hosts and their resident microbial communities are a fundamental component of fitness for both agents. Though recent research has highlighted the importance of interactions between animals and their bacterial communities, comparative evidence for fungi is lacking, especially in natural populations. Using data from 49 species, we present novel evidence of strong covariation between fungal and bacterial communities across the host phylogeny, indicative of recruitment by hosts for specific suites of microbes. Using co-occurrence networks, we demonstrate marked variation across host taxonomy in patterns of covariation between bacterial and fungal abundances. Host phylogeny drives differences in the overall richness of bacterial and fungal communities, but the effect of diet on richness was only evident in the mammalian gut microbiome. Sample type, tissue storage and DNA extraction method also affected bacterial and fungal community composition, and future studies would benefit from standardized approaches to sample processing. Collectively these data indicate fungal microbiomes may play a key role in host fitness and suggest an urgent need to study multiple agents of the animal microbiome to accurately determine the strength and ecological significance of host-microbe interactions.

Reproductive males are effective at managing conflict in captive Sulawesi crested macaques (Macaca nigra).

Group size, density, and composition significantly influence the expression of agonism and, as demography is frequently manipulated in captivity, natural mechanisms of conflict management may be disrupted. Here, we examine how changes to the social and physical environment of a captive group of Sulawesi crested macaques, Macaca nigra, influenced mechanisms of conflict management. The initial group was comprised of females, juveniles, and castrated males; under a series of management interventions, the group was moved to a new enclosure, 75% of the castrated adult males were removed, 67% of the females were contracepted, a novel, intact male was introduced, and the group was allowed access to an outdoor enclosure. Despite a decreasing trend in aggression following the changes to the social group, we found no significant differences in aggression or intervention behavior in the 5-week periods immediately following changes to the social group, apart from a significant decrease in aggression following the introduction of the novel male. This decrease in the frequency of aggression was still evident 10 weeks after the interventions occurred, and was coupled with a decrease in the intensity of aggression. Moreover, the intensity of aggression as well as the frequency of aggression and intervention were significantly lower under low-density conditions. Our results highlight how management changes to the social and physical environment can influence aggressive behavior, albeit following a period of acclimation. We discuss the relative impacts of social group composition, social density, and individual reproductive status on the management of conflict behavior in a captive setting.

Social complexity and the fractal structure of group size in primate social evolution.

Compared to most other mammals and birds, anthropoid primates have unusually complex societies characterised by bonded social groups. Among primates, this effect is encapsulated in the social brain hypothesis: the robust correlation between various indices of social complexity (social group size, grooming clique size, tactical behaviour, coalition formation) and brain size. Hitherto, this has always been interpreted as a simple, unitary relationship. Using data for five different indices of brain volume from four independent brain databases, we show that the distribution of group size plotted against brain size is best described as a set of four distinct, very narrowly defined grades which are unrelated to phylogeny. The allocation of genera to these grades is highly consistent across the different data sets and brain indices. We show that these grades correspond to the progressive evolution of bonded social groups. In addition, we show, for those species that live in multilevel social systems, that the typical sizes of the different grouping levels in each case coincide with different grades. This suggests that the grades correspond to demographic attractors that are especially stable. Using five different cognitive indices, we show that the grades correlate with increasing social cognitive skills, suggesting that the cognitive demands of managing group cohesion increase progressively across grades. We argue that the grades themselves represent glass ceilings on animals' capacity to maintain social and spatial coherence during foraging and that, in order to evolve more highly bonded groups, species have to be able to invest in costly forms of cognition.

Learning performance is influenced by the social environment in cichlid fishes.

It has been hypothesised that some specialised cognitive abilities may have evolved because of the challenges of living in complex social environments. Therefore, more-social species might be able to learn faster than less-social species. The aim of this study was to develop a learning framework to test how more- and less-social Lamprologine cichlid fishes perform across associative learning tasks. These cichlids are a group of closely related species with similar ecologies and life histories but varying degrees of sociality, making them an ideal group for comparative learning studies. We found that three nongrouping cichlids (Telmatochromis temporalis, Lamprologus meleagris, and Neolamprologus tretocephalus) outperformed three closely related highly social, cooperatively breeding cichlids (N. pulcher, N. multifasciatus, and Julidochromis dickfeldi) on an associative learning task based on food rewards. However, we hypothesised that these differences may be caused by the social environment during testing and might not reflect true cognitive differences. Indeed, when we drilled down and compared just two species across four different social conditions, we found that the social environment during learning trials affected the performance of the highly social N. pulcher and the less-social T. temporalis differently. We then performed further experiments with both N. pulcher and T. temporalis under more natural social settings. Under these more natural social conditions, we found that N. pulcher learned to differentiate accessible and inaccessible shelters faster than T. temporalis. These findings highlight the potential for expanding comparative experiments investigating the relationship between sociality and cognition and emphasise the crucial role social environment plays in learning outcomes. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Reproductive skew affects social information use.

Individuals vary in their propensity to use social learning, the engine of cultural evolution, to acquire information about their environment. The causes of those differences, however, remain largely unclear. Using an agent-based model, we tested the hypothesis that as a result of reproductive skew differences in energetic requirements for reproduction affect the value of social information. We found that social learning is associated with lower variance in yield and is more likely to evolve in risk-averse low-skew populations than in high-skew populations. Reproductive skew may also result in sex differences in social information use, as empirical data suggest that females are often more risk-averse than males. To explore how risk may affect sex differences in learning strategies, we simulated learning in sexually reproducing populations where one sex experiences more reproductive skew than the other. When both sexes compete for the same resources, they tend to adopt extreme strategies: the sex with greater reproductive skew approaches pure individual learning and the other approaches pure social learning. These results provide insight into the conditions that promote individual and species level variation in social learning and so may affect cultural evolution.

Author Correction: Direct benefits and evolutionary transitions to complex societies.

In the version of this Article originally published, references were missing from the column "Source(s) for mating and parental care system data" in Supplementary Table 1. The following references have now been added to the relevant species: Brichard 1989 has been added to Chalinochromis popelini, Chalinochromis brichardi and Julidochromis dickfeldi; Clabaut et al. 2007 to Altolamprologus calvus and Julidochromis regani; Konings 1998 to Neolamprologus hecqui; and Kuwamura 1997 to Chalinochromis popelini.

Rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino.

BACKGROUND: Host microbiomes play a role in hormone production and subsequent fertility in humans, but this is less well understood in non-model organisms. This is of particular relevance to species in zoo-based conservation breeding programmes, as relationships between host microbiome composition and reproductive output may allow for the development of microbial augmentation strategies to improve success. Here, we characterise faecal bacterial communities of breeding and non-breeding eastern black rhino (Diceros bicornis michaeli) using 16S rRNA gene amplicon sequencing and quantify progestagen and glucocorticoid metabolite concentrations through enzyme immunoassays to identify such relationships. RESULTS: We identified significant differences in black rhino gut microbiome composition according to ID, institution, breeding success and ovarian cycle phase. In particular, the gut microbiome during pregnancy and post-parturition was significantly altered. Around a third of bacterial genera showed more than ± 10% correlation with either progestagen and/or glucocorticoid concentration, and in general, microbial genera correlated with both hormones in the same direction. Through a combination of analyses, we identified four genera (Aerococcaceae, Atopostipes, Carnobacteriaceae and Solobacterium) that were significantly associated with breeding success, pregnancy and/or post-parturition, and higher faecal progestagen metabolite concentrations. These genera had a lower-than-average relative abundance in the gut microbiome. CONCLUSION: Our results indicate that many members of the gut microbiome of black rhino are associated with hormone production and breeding success, and some members of the rare microbiota appear to be particularly important. Although the directionality of the relationship is unclear, the variation in gut microbiome communities represents a potential biomarker of reproductive health. We identified four genera that were associated with multiple indicators of reproductive output; these could be candidate probiotics to improve the breeding success of black rhino in zoo-based conservation breeding programmes. Further work is required to understand the efficacy and feasibility of this, either directly through microbial augmentation (e.g. probiotics) or indirectly via dietary manipulation or prebiotics.

Gut microbiome composition is associated with spatial structuring and social interactions in semi-feral Welsh Mountain ponies.

BACKGROUND: Microbiome composition is linked to host functional traits including metabolism and immune function. Drivers of microbiome composition are increasingly well-characterised; however, evidence of group-level microbiome convergence is limited and may represent a multi-level trait (i.e. across individuals and groups), whereby heritable phenotypes are influenced by social interactions. Here, we investigate the influence of spatial structuring and social interactions on the gut microbiome composition of Welsh mountain ponies. RESULTS: We show that semi-feral ponies exhibit variation in microbiome composition according to band (group) membership, in addition to considerable within-individual variation. Spatial structuring was also identified within bands, suggesting that despite communal living, social behaviours still influence microbiome composition. Indeed, we show that specific interactions (i.e. mother-offspring and stallion-mare) lead to more similar microbiomes, further supporting the notion that individuals influence the microbiome composition of one another and ultimately the group. Foals exhibited different microbiome composition to sub-adults and adults, most likely related to differences in diet. CONCLUSIONS: We provide novel evidence that microbiome composition is structured at multiple levels within populations of social mammals and thus may form a unit on which selection can act. High levels of within-individual variation in microbiome composition, combined with the potential for social interactions to influence microbiome composition, suggest the direction of microbiome selection may be influenced by the individual members present in the group. Although the functional implications of this require further research, these results lend support to the idea that multi-level selection can act on microbiomes.

Primate social group sizes exhibit a regular scaling pattern with natural attractors.

Primate groups vary considerably in size across species. Nonetheless, the distribution of mean species group size has a regular scaling pattern with preferred sizes approximating 2.5, 5, 15, 30 and 50 individuals (although strepsirrhines lack the latter two), with a scaling ratio of approximately 2.5 similar to that observed in human social networks. These clusters appear to form distinct social grades that are associated with rapid evolutionary change, presumably in response to intense environmental selection pressures. These findings may have wider implications for other highly social mammal taxa.