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.

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.

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.

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.

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.

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.

Stepwise evolution of stable sociality in primates.

Although much attention has been focused on explaining and describing the diversity of social grouping patterns among primates, less effort has been devoted to understanding the evolutionary history of social living. This is partly because social behaviours do not fossilize, making it difficult to infer changes over evolutionary time. However, primate social behaviour shows strong evidence for phylogenetic inertia, permitting the use of Bayesian comparative methods to infer changes in social behaviour through time, thereby allowing us to evaluate alternative models of social evolution. Here we present a model of primate social evolution, whereby sociality progresses from solitary foraging individuals directly to large multi-male/multi-female aggregations (approximately 52 million years (Myr) ago), with pair-living (approximately 16 Myr ago) or single-male harem systems (approximately 16 Myr ago) derivative from this second stage. This model fits the data significantly better than the two widely accepted alternatives (an unstructured model implied by the socioecological hypothesis or a model that allows linear stepwise changes in social complexity through time). We also find strong support for the co-evolution of social living with a change from nocturnal to diurnal activity patterns, but not with sex-biased dispersal. This supports suggestions that social living may arise because of increased predation risk associated with diurnal activity. Sociality based on loose aggregation is followed by a second shift to stable or bonded groups. This structuring facilitates the evolution of cooperative behaviours and may provide the scaffold for other distinctive anthropoid traits including coalition formation, cooperative resource defence and large brains.

Phylogenetic reconstruction of Bantu kinship challenges Main Sequence Theory of human social evolution.

Kinship provides the fundamental structure of human society: descent determines the inheritance pattern between generations, whereas residence rules govern the location a couple moves to after they marry. In turn, descent and residence patterns determine other key relationships such as alliance, trade, and marriage partners. Hunter-gatherer kinship patterns are viewed as flexible, whereas agricultural societies are thought to have developed much more stable kinship patterns as they expanded during the Holocene. Among the Bantu farmers of sub-Saharan Africa, the ancestral kinship patterns present at the beginning of the expansion are hotly contested, with some arguing for matrilineal and matrilocal patterns, whereas others maintain that any kind of lineality or sex-biased dispersal only emerged much later. Here, we use Bayesian phylogenetic methods to uncover the history of Bantu kinship patterns and trace the interplay between descent and residence systems. The results suggest a number of switches in both descent and residence patterns as Bantu farming spread, but that the first Bantu populations were patrilocal with patrilineal descent. Across the phylogeny, a change in descent triggered a switch away from patrifocal kinship, whereas a change in residence triggered a switch back from matrifocal kinship. These results challenge "Main Sequence Theory," which maintains that changes in residence rules precede change in other social structures. We also indicate the trajectory of kinship change, shedding new light on how this fundamental structure of society developed as farming spread across the globe during the Neolithic.

Copy-when-uncertain: bumblebees rely on social information when rewards are highly variable.

To understand the relative benefits of social and personal information use in foraging decisions, we developed an agent-based model of social learning that predicts social information should be more adaptive where resources are highly variable and personal information where resources vary little. We tested our predictions with bumblebees and found that foragers relied more on social information when resources were variable than when they were not. We then investigated whether socially salient cues are used preferentially over non-social ones in variable environments. Although bees clearly used social cues in highly variable environments, under the same conditions they did not use non-social cues. These results suggest that bumblebees use a 'copy-when-uncertain' strategy.

Male infanticide leads to social monogamy in primates.

Although common in birds, social monogamy, or pair-living, is rare among mammals because internal gestation and lactation in mammals makes it advantageous for males to seek additional mating opportunities. A number of hypotheses have been proposed to explain the evolution of social monogamy among mammals: as a male mate-guarding strategy, because of the benefits of biparental care, or as a defense against infanticidal males. However, comparative analyses have been unable to resolve the root causes of monogamy. Primates are unusual among mammals because monogamy has evolved independently in all of the major clades. Here we combine trait data across 230 primate species with a Bayesian likelihood framework to test for correlated evolution between monogamy and a range of traits to evaluate the competing hypotheses. We find evidence of correlated evolution between social monogamy and both female ranging patterns and biparental care, but the most compelling explanation for the appearance of monogamy is male infanticide. It is only the presence of infanticide that reliably increases the probability of a shift to social monogamy, whereas monogamy allows the secondary adoption of paternal care and is associated with a shift to discrete ranges. The origin of social monogamy in primates is best explained by long lactation periods caused by altriciality, making primate infants particularly vulnerable to infanticidal males. We show that biparental care shortens relative lactation length, thereby reducing infanticide risk and increasing reproductive rates. These phylogenetic analyses support a key role for infanticide in the social evolution of primates, and potentially, humans.

Competition for resources can explain patterns of social and individual learning in nature.

In nature, animals often ignore socially available information despite the multiple theoretical benefits of social learning over individual trial-and-error learning. Using information filtered by others is quicker, more efficient and less risky than randomly sampling the environment. To explain the mix of social and individual learning used by animals in nature, most models penalize the quality of socially derived information as either out of date, of poor fidelity or costly to acquire. Competition for limited resources, a fundamental evolutionary force, provides a compelling, yet hitherto overlooked, explanation for the evolution of mixed-learning strategies. We present a novel model of social learning that incorporates competition and demonstrates that (i) social learning is favoured when competition is weak, but (ii) if competition is strong social learning is favoured only when resource quality is highly variable and there is low environmental turnover. The frequency of social learning in our model always evolves until it reduces the mean foraging success of the population. The results of our model are consistent with empirical studies showing that individuals rely less on social information where resources vary little in quality and where there is high within-patch competition. Our model provides a framework for understanding the evolution of social learning, a prerequisite for human cumulative culture.

Irregular ovarian activity, body condition and behavioural differences are associated with reproductive success in female eastern black rhinoceros (Diceros bicornis michaeli).

Ex situ populations of endangered species such as the black rhinoceros play an important role in global conservation strategies. However, the European captive population of eastern black rhinoceros is performing sub-optimally, with growth rates and genetic viability limited by low birth rates and high reproductive skew. We investigated several intrinsic differences between parous and nulliparous females that may underlie differences in reproductive success, including ovarian cyclicity, adrenal activity, behaviour and body condition. Faecal samples were collected from 39 females (17 parous, 15 nulliparous and 7 pre-reproductive) at 11 zoological institutions, every other day for between 4months and 6years. Progestagen metabolite concentration indicated that although all non-pregnant females exhibited ovarian activity, irregular cyclicity was common. Longer cycles (>40days) were more common in nulliparous females and periods of acyclicity observed more often in females that had not bred for at least 7years. Even when endocrine data indicated clear ovarian activity, overt behavioural signs of oestrus were not always apparent, particularly among nulliparous females. Faecal glucocorticoids did not differ between parous and nulliparous females, although did differ according to individual temperament. More unpredictable temperaments were associated with higher glucocorticoids, and nulliparous females tended to be rated as more unpredictable. Finally, nulliparous females had higher body condition scores than parous females. This is the first comprehensive survey of the reproductive physiology of this European captive population, and highlights a number of intrinsic differences related to parity, which may underlie differences in reproductive success among captive female black rhinoceros.

Male reproductive success is correlated with testosterone in the eastern black rhinoceros (Diceros bicornis michaeli).

Among natural populations of polygynous species, males often vary in their lifetime reproductive success. However, in managed populations of endangered species, either in situ or as part of captive breeding programmes, it is important to understand why differences in reproductive success occur. The European captive population of the critically endangered eastern black rhinoceros is currently under-performing relative to their wild counterparts, with low reproductive output and high reproductive skew limiting growth and genetic diversity. To investigate why over 40% of captive males fail to breed, faecal samples were collected weekly from 23 males at 12 institutions across Europe for 4-32 months. Testosterone metabolite concentration was compared between proven and non-proven males and a number of intrinsic and extrinsic factors that could influence reproductive success were also investigated. Males that sired within the last 3½ years had significantly higher androgen concentrations than non-proven males, and average testosterone was positively correlated with the number of offspring sired per year spent in the reproductive age class. Proven and non-proven males did not differ in their body condition, or in average faecal glucocorticoid concentration. Differences in individual temperament were associated with adrenal activity, but did not correlate with reproductive category. Highest testosterone concentrations were observed in proven males that were housed with females during oestrus, and lowest concentrations in non-proven females not housed with females at all during the study period. Further work is necessary to determine whether proven males had higher testosterone due to underlying differences associated with quality, or whether external stimuli such as access to females could influence testosterone concentration and increase a male's chances of becoming a successful breeder.

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.

Making sense of information in noisy networks: human communication, gossip, and distortion.

Information from others can be unreliable. Humans nevertheless act on such information, including gossip, to make various social calculations, thus raising the question of whether individuals can sort through social information to identify what is, in fact, true. Inspired by empirical literature on people's decision-making when considering gossip, we built an agent-based simulation model to examine how well simple decision rules could make sense of information as it propagated through a network. Our simulations revealed that a minimalistic decision-rule 'Bit-wise mode' - which compared information from multiple sources and then sought a consensus majority for each component bit within the message - was consistently the most successful at converging upon the truth. This decision rule attained high relative fitness even in maximally noisy networks, composed entirely of nodes that distorted the message. The rule was also superior to other decision rules regardless of its frequency in the population. Simulations carried out with variable agent memory constraints, different numbers of observers who initiated information propagation, and a variety of network types suggested that the single most important factor in making sense of information was the number of independent sources that agents could consult. Broadly, our model suggests that despite the distortion information is subject to in the real world, it is nevertheless possible to make sense of it based on simple Darwinian computations that integrate multiple sources.

Associations between social behaviour and adrenal activity in female Barbary macaques: consequences of study design.

Faecal glucocorticoid metabolite (fGCM) concentrations have been used to evaluate adrenal activity in a variety of species; including as an indicator of the physiological response to social stress. However, across studies, the relationships between dominance rank, social behaviours and adrenal responses can be inconsistent. Differences in the relationship between rank and glucocorticoids may be due to the relative costs of social status, and the relative frequencies of social stressors and potential coping mechanisms. However, the differences in observed relationships between specific social behaviours and glucocorticoids may be partly explained by sampling frequency, as studies often use average fGCM concentrations collected over a period of weeks or months, rather than fGCM concentrations that are temporally-matched with behavioural data. In this study, we directly compared long-term average and temporally-matched data to determine whether particular social behaviours were related to adrenal activity in female Barbary macaques (Macaca sylvanus) at Trentham Monkey Forest, UK; and whether observed relationships were consistent using these two approaches. Average rates of autogrooming were positively correlated with average fGCM; however, this relationship was not robust in temporally-matched samples. Instead, specific social behaviours associated with agonism were associated with fGCM in temporally-matched samples within individuals. These results indicate that analyses of relationships using long-term average fGCM and temporally-matched samples do not necessarily provide comparable results, highlighting that study design is critical in determining associations between an individual's social behaviour and the relative physiological costs involved.

Encephalization is not a universal macroevolutionary phenomenon in mammals but is associated with sociality.

Evolutionary encephalization, or increasing brain size relative to body size, is assumed to be a general phenomenon in mammals. However, despite extensive evidence for variation in both absolute and relative brain size in extant species, there have been no explicit tests of patterns of brain size change over evolutionary time. Instead, allometric relationships between brain size and body size have been used as a proxy for evolutionary change, despite the validity of this approach being widely questioned. Here we relate brain size to appearance time for 511 fossil and extant mammalian species to test for temporal changes in relative brain size over time. We show that there is wide variation across groups in encephalization slopes across groups and that encephalization is not universal in mammals. We also find that temporal changes in brain size are not associated with allometric relationships between brain and body size. Furthermore, encephalization trends are associated with sociality in extant species. These findings test a major underlying assumption about the pattern and process of mammalian brain evolution and highlight the role sociality may play in driving the evolution of large brains.

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.