Determinants of microbiome composition: Insights from free-ranging hybrid zebras (Equus quagga × grevyi).

The composition of mammalian gut microbiomes is highly conserved within species, yet the mechanisms by which microbiome composition is transmitted and maintained within lineages of wild animals remain unclear. Mutually compatible hypotheses exist, including that microbiome fidelity results from inherited dietary habits, shared environmental exposure, morphophysiological filtering and/or maternal effects. Interspecific hybrids are a promising system in which to interrogate the determinants of microbiome composition because hybrids can decouple traits and processes that are otherwise co-inherited in their parent species. We used a population of free-living hybrid zebras (Equus quagga × grevyi) in Kenya to evaluate the roles of these four mechanisms in regulating microbiome composition. We analysed faecal DNA for both the trnL-P6 and the 16S rRNA V4 region to characterize the diets and microbiomes of the hybrid zebra and of their parent species, plains zebra (E. quagga) and Grevy's zebra (E. grevyi). We found that both diet and microbiome composition clustered by species, and that hybrid diets and microbiomes were largely nested within those of the maternal species, plains zebra. Hybrid microbiomes were less variable than those of either parent species where they co-occurred. Diet and microbiome composition were strongly correlated, although the strength of this correlation varied between species. These patterns are most consistent with the maternal-effects hypothesis, somewhat consistent with the diet hypothesis, and largely inconsistent with the environmental-sourcing and morphophysiological-filtering hypotheses. Maternal transmittance likely operates in conjunction with inherited feeding habits to conserve microbiome composition within species.

New estimates indicate that males are not larger than females in most mammal species.

Sexual size dimorphism has motivated a large body of research on mammalian mating strategies and sexual selection. Despite some contrary evidence, the narrative that larger males are the norm in mammals-upheld since Darwin's Descent of Man-still dominates today, supported by meta-analyses that use coarse measures of dimorphism and taxonomically-biased sampling. With newly-available datasets and primary sources reporting sex-segregated means and variances in adult body mass, we estimate statistically-determined rates of sexual size dimorphism in mammals, sampling taxa by their species richness at the family level. Our analyses of wild, non-provisioned populations representing >400 species indicate that although males tend to be larger than females when dimorphism occurs, males are not larger in most mammal species, suggesting a need to revisit other assumptions in sexual selection research.

Zebras of all stripes repel biting flies at close range.

The best-supported hypothesis for why zebras have stripes is that stripes repel biting flies. While this effect is well-established, the mechanism behind it remains elusive. Myriad hypotheses have been suggested, but few experiments have helped narrow the field of possible explanations. In addition, the complex visual features of real zebra pelage and the natural range of stripe widths have been largely left out of experimental designs. In paired-choice field experiments in a Kenyan savannah, we found that hungry Stomoxys flies released in an enclosure strongly preferred to land on uniform tan impala pelts over striped zebra pelts but exhibited no preference between the pelts of the zebra species with the widest stripes and the narrowest stripes. Our findings confirm that zebra stripes repel biting flies under naturalistic conditions and do so at close range (suggesting that several of the mechanisms hypothesized to operate at a distance are unnecessary for the fly-repulsion effect) but indicate that interspecific variation in stripe width is associated with selection pressures other than biting flies.

Social dilemmas of sociality due to beneficial and costly contagion.

Levels of sociality in nature vary widely. Some species are solitary; others live in family groups; some form complex multi-family societies. Increased levels of social interaction can allow for the spread of useful innovations and beneficial information, but can also facilitate the spread of harmful contagions, such as infectious diseases. It is natural to assume that these contagion processes shape the evolution of complex social systems, but an explicit account of the dynamics of sociality under selection pressure imposed by contagion remains elusive. We consider a model for the evolution of sociality strategies in the presence of both a beneficial and costly contagion. We study the dynamics of this model at three timescales: using a susceptible-infectious-susceptible (SIS) model to describe contagion spread for given sociality strategies, a replicator equation to study the changing fractions of two different levels of sociality, and an adaptive dynamics approach to study the long-time evolution of the population level of sociality. For a wide range of assumptions about the benefits and costs of infection, we identify a social dilemma: the evolutionarily-stable sociality strategy (ESS) is distinct from the collective optimum-the level of sociality that would be best for all individuals. In particular, the ESS level of social interaction is greater (respectively less) than the social optimum when the good contagion spreads more (respectively less) readily than the bad contagion. Our results shed light on how contagion shapes the evolution of social interaction, but reveals that evolution may not necessarily lead populations to social structures that are good for any or all.

Interacting with others while reacting to the environment.

Here, we revise Pietraszewski's model of groups by assigning participant pairs with two triplets, denoting: (1) the type of game that models the interaction, (2) its critical switching point between alternatives (i.e., the game's similarity threshold), and (3) the perception of strategic similarity with the opponent. These triplets provide a set of primitives that accounts for individuals' strategic motivations and observed behaviors.

Both prey and predator features predict the individual predation risk and survival of schooling prey.

Predation is one of the main evolutionary drivers of social grouping. While it is well appreciated that predation risk is likely not shared equally among individuals within groups, its detailed quantification has remained difficult due to the speed of attacks and the highly dynamic nature of collective prey response. Here, using high-resolution tracking of solitary predators (Northern pike) hunting schooling fish (golden shiners), we not only provide insights into predator decision-making, but show which key spatial and kinematic features of predator and prey predict the risk of individuals to be targeted and to survive attacks. We found that pike tended to stealthily approach the largest groups, and were often already inside the school when launching their attack, making prey in this frontal 'strike zone' the most vulnerable to be targeted. From the prey's perspective, those fish in central locations, but relatively far from, and less aligned with, neighbours, were most likely to be targeted. While the majority of attacks were successful (70%), targeted individuals that did manage to avoid being captured exhibited a higher maximum acceleration response just before the attack and were further away from the pike's head. Our results highlight the crucial interplay between predators' attack strategy and response of prey underlying the predation risk within mobile animal groups.

Vaccination-hesitancy and global warming: distinct social challenges with similar behavioural solutions.

Although the COVID-19 vaccine has dramatically changed the fight against the pandemic, many exhibit vaccination-hesitancy. At the same time, continued human-induced emissions of greenhouse gases pose an alarming threat to humanity. Based on the theory of Subjective Expected Relative Similarity (SERS) and a recent international study that drastically modified COVID-19 health-related attitudes, we explain why a similar approach and a corresponding public policy are expected to help resolve both behavioural issues: reduce vaccination hesitancy and motivate climate actions.

Divergent water requirements partition exposure risk to parasites in wild equids.

For grazing herbivores, dung density in feeding areas is an important determinant of exposure risk to fecal-orally transmitted parasites. When host species share the same parasite species, a nonrandom distribution of their cumulative dung density and/or nonrandom ranging and feeding behavior may skew exposure risk and the relative selection pressure parasites impose on each host. The arid-adapted Grevy's zebra (Equus grevyi) can range more widely than the water-dependent plains zebra (Equus quagga), with which it shares the same species of gastrointestinal nematodes. We studied how the spatial distribution of zebra dung relates to ranging and feeding behavior to assess parasite exposure risk in Grevy's and plains zebras at a site inhabited by both zebra species. We found that zebra dung density declined with distance from water, Grevy's zebra home ranges (excluding those of territorial males) were farther from water than those of plains zebras, and plains zebra grazing areas had higher dung density than random points while Grevy's zebra grazing areas did not, suggesting a greater exposure risk in plains zebras associated with their water dependence. Fecal egg counts increased with home range proximity to water for both species, but the response was stronger in plains zebras, indicating that this host species may be particularly vulnerable to the elevated exposure risk close to water. We further ran experiments on microclimatic effects on dung infectivity and showed that fewer nematode eggs embryonated in dung in the sun than in the shade. However, only 5% of the zebra dung on the landscape was in shade, indicating that the microclimatic effects of shade on the density of infective larvae is not a major influence on exposure risk dynamics. Ranging constraints based on water requirements appear to be key mediators of nematode parasite exposure in free-ranging equids.

The gastrointestinal nematodes of plains and Grevy's zebras: Phylogenetic relationships and host specificity.

Equids are chronically infected with parasitic strongyle nematodes. There is a rich literature on horse strongyles, but they are difficult to identify morphologically and genetic studies on strongyles infecting other equid species are few, hampering studies of host specificity. We sequenced expelled worms from two sympatric zebra species in central Kenya to expand the strongyle phylogeny and used DNA metabarcoding on faecal samples to genetically characterize zebra nemabiomes for the first time. We generated sequences for several species new to public genetic reference databases, all of which are typical strongyles in wild zebras (i.e., the three species of Cylindropharynx and Cyathostomum montgomeryi), and identified their closest relatives. We also discovered an apparent fungus infecting a quarter of the expelled Crossocephalus viviparus worms, a hyperabundant nematode species in the family Atractidae, hinting at the possibility that zebra host-parasite dynamics may involve a zebra-fungus mutualism. The two zebra species had similar nemabiomes; we found a complete overlap in the list of nematode species they carry and very similar prevalence (i.e., proportion of hosts infected) for the different nematode species. Our study suggests limited host-specificity in zebra strongyles and high potential for transmission between the plains zebra and the endangered Grevy's zebra.

Body size and digestive system shape resource selection by ungulates: A cross-taxa test of the forage maturation hypothesis.

The forage maturation hypothesis (FMH) states that energy intake for ungulates is maximised when forage biomass is at intermediate levels. Nevertheless, metabolic allometry and different digestive systems suggest that resource selection should vary across ungulate species. By combining GPS relocations with remotely sensed data on forage characteristics and surface water, we quantified the effect of body size and digestive system in determining movements of 30 populations of hindgut fermenters (equids) and ruminants across biomes. Selection for intermediate forage biomass was negatively related to body size, regardless of digestive system. Selection for proximity to surface water was stronger for equids relative to ruminants, regardless of body size. To be more generalisable, we suggest that the FMH explicitly incorporate contingencies in body size and digestive system, with small-bodied ruminants selecting more strongly for potential energy intake, and hindgut fermenters selecting more strongly for surface water.

Stewardship of global collective behavior.

Collective behavior provides a framework for understanding how the actions and properties of groups emerge from the way individuals generate and share information. In humans, information flows were initially shaped by natural selection yet are increasingly structured by emerging communication technologies. Our larger, more complex social networks now transfer high-fidelity information over vast distances at low cost. The digital age and the rise of social media have accelerated changes to our social systems, with poorly understood functional consequences. This gap in our knowledge represents a principal challenge to scientific progress, democracy, and actions to address global crises. We argue that the study of collective behavior must rise to a "crisis discipline" just as medicine, conservation, and climate science have, with a focus on providing actionable insight to policymakers and regulators for the stewardship of social systems.

Population structure, inbreeding and stripe pattern abnormalities in plains zebras.

One of the most iconic wild equids, the plains zebra occupies a broad region of sub-Saharan Africa and exhibits a wide range of phenotypic diversity in stripe patterns that have been used to classify multiple subspecies. After decades of relative stability, albeit with a loss of at least one recognized subspecies, the total population of plains zebras has undergone an approximate 25% decline since 2002. Individuals with abnormal stripe patterns have been recognized in recent years but the extent to which their appearance is related to demography and/or genetics is unclear. Investigating population genetic health and genetic structure are essential for developing effective strategies for plains zebra conservation. We collected DNA from 140 plains zebra, including seven with abnormal stripe patterns, from nine locations across the range of plains zebra, and analyzed data from restriction site-associated and whole genome sequencing (RAD-seq, WGS) libraries to better understand the relationships between population structure, genetic diversity, inbreeding, and abnormal phenotypes. We found that genetic structure did not coincide with described subspecific variation, but did distinguish geographic regions in which anthropogenic habitat fragmentation is associated with reduced gene flow and increased evidence of inbreeding, especially in certain parts of East Africa. Further, zebras with abnormal striping exhibited increased levels of inbreeding relative to normally striped individuals from the same populations. Our results point to a genetic cause of stripe pattern abnormalities, and dramatic evidence of the consequences of habitat fragmentation.

Multilevel Organisation of Animal Sociality.

Multilevel societies (MLSs), stable nuclear social units within a larger collective encompassing multiple nested social levels, occur in several mammalian lineages. Their architectural complexity and size impose specific demands on their members requiring adaptive solutions in multiple domains. The functional significance of MLSs lies in their members being equipped to reap the benefits of multiple group sizes. Here, we propose a unifying terminology and operational definition of MLS. To identify new avenues for integrative research, we synthesise current literature on the selective pressures underlying the evolution of MLSs and their implications for cognition, intersexual conflict, and sexual selection. Mapping the drivers and consequences of MLS provides a reference point for the social evolution of many taxa, including our own species.

The non-invasive measurement of faecal immunoglobulin in African equids.

Eco-immunological research is encumbered by a lack of basic research in a wild context and by the availability of few non-invasive tools to measure the internal state of wild animals. The recent development of an enzyme-linked immunosorbent assay for measuring immunoglobulins in faecal samples from Soay sheep prompted us to optimize such an assay to measure immunoglobulin A (IgA: an antibody associated with parasitic nematode fecundity) in faecal samples from equids. We measured total IgA in domestic donkeys, wild plains zebras, and wild Grevy's zebras sharing the same landscape in central Kenya over two field seasons. Attempts to measure anti-nematode IgA more specifically, using a homogenized extract from a mixture of excreted nematodes, failed to clear background. However, we found that total IgA positively correlated with strongyle nematode faecal egg counts (FECs) in donkeys sampled during the wetter field season - a time when the donkeys were in good condition. Further, this relationship appeared among donkeys with high body condition but not among those with low body condition. Time lags of 1-4 days introduced between IgA and FEC measurements in repeatedly sampled donkeys did not yield correlations, suggesting that IgA and FEC roughly tracked one another without much delay in the wet field season. Such a direct IgA-FEC relationship did not appear for zebras in either the wet or dry field season, possibly due to higher interindividual variation in body condition among the free-roaming zebras than in the donkeys. However, Grevy's zebras had higher overall levels of IgA than either plains zebras or donkeys, potentially associated with their reportedly lower FECs at the population level. Our results suggest that equids may mount an IgA response to nematode egg production when the host is in good condition and that equid species may differ in baseline levels of mucosal IgA.

Communication is key: Mother-offspring signaling can affect behavioral responses and offspring survival in feral horses (Equus caballus).

Acoustic signaling plays an important role in mother-offspring recognition and subsequent bond-formation. It remains unclear, however, if mothers and offspring use acoustic signaling in the same ways and for the same reasons throughout the juvenile stage, particularly after mutual recognition has been adequately established. Moreover, despite its critical role in mother-offspring bond formation, research explicitly linking mother-infant communication strategies to offspring survival are lacking. We examined the communicative patterns of mothers and offspring in the feral horse (Equus caballus) to better understand 1) the nature of mother-offspring communication throughout the first year of development; 2) the function(s) of mother- vs. offspring-initiated communication and; 3) the importance of mare and foal communication to offspring survival. We found that 1) mares and foals differ in when and how they initiate communication; 2) the outcomes of mare- vs. foal-initiated communication events consistently differ; and 3) the communicative patterns between mares and their foals can be important for offspring survival to one year of age. Moreover, given the importance of maternal activity to offspring behavior and subsequent survival, we submit that our data are uniquely positioned to address the long-debated question: do the behaviors exhibited during the juvenile stage (by both mothers and their young) confer delayed or immediate benefits to offspring? In summary, we aimed to better understand 1) the dynamics of mother-offspring communication, 2) whether mother-offspring communicative patterns were important to offspring survival, and 3) the implications of our research regarding the function of the mammalian juvenile stage. Our results demonstrate that we have achieved those aims.

Knowledgeable Lemurs Become More Central in Social Networks.

Strong relationships exist between social connections and information transmission [1-9], where individuals' network position plays a key role in whether or not they acquire novel information [2, 3, 5, 6]. The relationships between social connections and information acquisition may be bidirectional if learning novel information, in addition to being influenced by it, influences network position. Individuals who acquire information quickly and use it frequently may receive more affiliative behaviors [10, 11] and may thus have a central network position. However, the potential influence of learning on network centrality has not been theoretically or empirically addressed. To bridge this epistemic gap, we investigated whether ring-tailed lemurs' (Lemur catta) centrality in affiliation networks changed after they learned how to solve a novel foraging task. Lemurs who had frequently initiated interactions and approached conspecifics before the learning experiment were more likely to observe and learn the task solution. Comparing social networks before and after the learning experiment revealed that the frequently observed lemurs received more affiliative behaviors than they did before-they became more central after the experiment. This change persisted even after the task was removed and was not caused by the observed lemurs initiating more affiliative behaviors. Consequently, quantifying received and initiated interactions separately provides unique insights into the relationships between learning and centrality. While the factors that influence network position are not fully understood, our results suggest that individual differences in learning and becoming successful can play a major role in social centrality, especially when learning from others is advantageous.

How ecology shapes exploitation: a framework to predict the behavioural response of human and animal foragers along exploration-exploitation trade-offs.

Understanding how humans and other animals behave in response to changes in their environments is vital for predicting population dynamics and the trajectory of coupled social-ecological systems. Here, we present a novel framework for identifying emergent social behaviours in foragers (including humans engaged in fishing or hunting) in predator-prey contexts based on the exploration difficulty and exploitation potential of a renewable natural resource. A qualitative framework is introduced that predicts when foragers should behave territorially, search collectively, act independently or switch among these states. To validate it, we derived quantitative predictions from two models of different structure: a generic mathematical model, and a lattice-based evolutionary model emphasising exploitation and exclusion costs. These models independently identified that the exploration difficulty and exploitation potential of the natural resource controls the social behaviour of resource exploiters. Our theoretical predictions were finally compared to a diverse set of empirical cases focusing on fisheries and aquatic organisms across a range of taxa, substantiating the framework's predictions. Understanding social behaviour for given social-ecological characteristics has important implications, particularly for the design of governance structures and regulations to move exploited systems, such as fisheries, towards sustainability. Our framework provides concrete steps in this direction.