The evolution of intergroup tolerance in nonhuman primates and humans

Primate individuals use a variety of strategies in intergroup encounters, from aggression to tolerance; however, recent focus on the evolution of either warfare or peace has come at the cost of characterizing this variability. We identify evolutionary advantages that may incentivize tolerance toward extra‐group individuals in humans and nonhuman primates, including enhanced benefits in the domains of transfer, mating, and food acquisition. We highlight the role these factors play in the flexibility of gorilla, chimpanzee, bonobo, and human behavior. Given humans have an especially broad range of intergroup behavior, we explore how the human foraging ecology, especially large spatial and temporal fluctuations in resource availability, may have selected for a greater reliance on tolerant between‐community relationships—relationships reinforced by status acquisition and cultural institutions. We conclude by urging careful, theoretically motivated study of behavioral flexibility in intergroup encounters in humans and the nonhuman great apes.     

Lateralization in feeding is food type specific and impacts feeding success in wild birds

Current research suggests that hemispheric lateralization has significant fitness consequences. Foraging, as a basic survival function, is a perfect research model to test the fitness impact of lateralization. However, our understanding of lateralized feeding behavior is based predominantly on laboratory studies, while the evidence from wild animals in natural settings is limited. Here we studied visual lateralization in yellow‐footed green pigeons (Treron phoenicoptera) feeding in the wild. We aimed to test whether different types of food objects requiring different searching strategies elicit different eye/hemisphere biases. When feeding on relatively large, uniformly colored food objects (mahua flowers) which can be present or absent in the viewed patch, the majority of pigeons relied mostly on the left eye–right hemisphere. In contrast, when feeding on smaller and more abundant food objects, with color cues signaling its ripeness (sacred figs), right‐eye (left‐hemisphere) preference prevailed. Our results demonstrate that oppositely directed visual biases previously found in different experimental tasks occur in natural feeding situations in the form of lateralized viewing strategies specific for different types of food. The results suggest that pigeons rely on the hemisphere providing more advantages for the consumption of the particular type of food objects, implying the relevance of brain lateralization as a plastic adaptation to ecological demands. We assessed the success of food discrimination and consumption to examine the link between lateralization and cognitive performance. The use of the preferred eye resulted in better discrimination of food items. Discrimination accuracy and feeding efficiency were significantly higher in lateralized individuals. The results showed that visual lateralization impacted pigeons’ feeding success, implicating important fitness benefits associated with lateralization.     

The importance of scale in comparative microbiome research: New insights from the gut and glands of captive and wild lemurs

Research on animal microbiomes is increasingly aimed at determining the evolutionary and ecological factors that govern host–microbiome dynamics, which are invariably intertwined and potentially synergistic. We present three empirical studies related to this topic, each of which relies on the diversity of Malagasy lemurs (representing a total of 19 species) and the comparative approach applied across scales of analysis. In Study 1, we compare gut microbial membership across 14 species in the wild to test the relative importance of host phylogeny and feeding strategy in mediating microbiome structure. Whereas host phylogeny strongly predicted community composition, the same feeding strategies shared by distant relatives did not produce convergent microbial consortia, but rather shaped microbiomes in host lineage‐specific ways, particularly in folivores. In Study 2, we compare 14 species of wild and captive folivores, frugivores, and omnivores, to highlight the importance of captive populations for advancing gut microbiome research. We show that the perturbational effect of captivity is mediated by host feeding strategy and can be mitigated, in part, by modified animal management. In Study 3, we examine various scent‐gland microbiomes across three species in the wild or captivity and show them to vary by host species, sex, body site, and a proxy of social status. These rare data provide support for the bacterial fermentation hypothesis in olfactory signal production and implicate steroid hormones as mediators of microbial community structure. We conclude by discussing the role of scale in comparative microbial studies, the links between feeding strategy and host–microbiome coadaptation, the underappreciated benefits of captive populations for advancing conservation research, and the need to consider the entirety of an animal's microbiota. Ultimately, these studies will help move the field from exploratory to hypothesis‐driven research.     

Coevolutionary relationship between striatum size and social play in nonhuman primates

The striatum is a region of the brain specifically tied to the experience and anticipation of pleasure, reward, appropriate behavioral sequencing, cognition, learning, and social modulation. Furthermore, the striatum is connected neurologically and functionally to other brain regions associated with the exhibition of social play, such as the neocortex, cerebellum, and limbic system. For these reasons, the striatum is especially interesting to researchers of play behavior. Moreover, the caudate-putamen area of the striatum has been specifically implicated in laboratory studies of social play behavior. This study uses the phylogenetic comparative method of independent contrasts to test for an evolutionary relationship between striatum volume and a measure of social play in nonhuman primates. Relative volume of the primate striatum correlates with rate of social, but not nonsocial, play behavior across species, suggesting a coevolution of traits. The pleasurable and procedural aspects of social play behavior may be mediated in part by the striatum and further to its connection to dopaminergic pathways in the primate brain.     

Basicranial flexion,relative brain size,and facial kyphosis in nonhuman primates

Numerous hypotheses explaining interspecific differences in the degree of basicranial flexion have been presented. Several authors have argued that an increase in relative brain size results in a spatial packing problem that is resolved by flexing the basicranium. Others attribute differences in the degree of basicranial flexion to different postural behaviors, suggesting that more orthograde animals require a ventrally flexed pre-sella basicranium in order to maintain the eyes in a correct forward-facing orientation. Less specific claims are made for a relationship between the degree of basicranial flexion and facial orientation. In order to evaluate these hypotheses, the degree of basicranial flexion (cranial base angle), palate orientation, and orbital axis orientation were measured from lateral radiographs of 68 primate species and combined with linear and volumetric measures as well as data on the size of the neocortex and telencephalon. Bivariate correlation and partial correlation analyses at several taxonomic levels revealed that, within haplorhines, the cranial base angle decreases with increasing neurocranial volume relative to basicranial length and is positively correlated with angles of facial kyphosis and orbital axis orientation. Strepsirhines show no significant correlations between the cranial base angle and any of the variables examined. It is argued that prior orbital approximation in the ancestral haplorhine integrated the medial orbital walls and pre-sella basicranium into a single structural network such that changes in the orientation of one necessarily affect the other. Gould's (“Ontogeny and Phylogeny.” Cambridge: Belknap Press, 1977) hypothesis, that the highly flexed basicranium of Homo may be due to a combination of a large brain and a relatively short basicranium, is corroborated. © 1993 Wiley-Liss, Inc.     

Muscle mass scaling in primates: an energetic and ecological perspective

Body composition is known to vary dramatically among mammals, even in closely related species, yet this issue has never been systematically investigated. Here, we examine differences in muscle mass scaling among mammals, and explore how primate body composition compares to that of nonprimate mammals. We use a literature-based sample of eutherian and metatherian mammals, and combine this with new dissection-based data on muscularity in a variety of strepsirrhine primates and the haplorhine, Tarsius syrichta. Our results indicate an isometric scaling relationship between total muscle mass and total body mass across mammals. However, we documented substantial variation in muscularity in mammals (21-61% of total body mass), which can be seen both within and between taxonomic groups. We also found that primates are under-muscled when compared to other mammals. This difference in body composition may in part reflect the functional consequences of arboreality, as arboreal species have significantly lower levels of muscularity than terrestrial species.     

Biological control: Premises,ecological input and Mimosa pigra in the wetlands of Australia's Top End

The adverse impacts of weeds on natural ecosystems, together with the inadequate outcomes from treating weeds as a symptom, have escalated interest in finding efficacious control methods. With the aim of protecting wetlands from invasive weeds, this contribution uses the woody shrub Mimosa pigra L. (mimosa) as a case history to examine the methodology of classical biological control and the reasons for the widely accepted 75% failure rate. Overall objectives are for all biocontrol agents to have the opportunity to fully express their potential and to insure that limited resources are spent wisely on attainable weed control. The three main conclusions were that (1) the premises on which biocontrol is based has restricted advancement of this method; (2) monitoring is the logical first step to improving the selection of agents and release sites; and (3) it may be more cost-effective to introduce fewer agents that have undergone agent/plant and host/home range pre- and post-release ecological studies. Weed control may remain elusive unless advantage is taken of every beneficial result. Innovative assistance to agents and the integration of different control methods may preserve a role for weed biological control and has the potential to be of great importance for future weed management. It is proposed that the climate in the Top End of the Northern Territory and the lack of competition on the floodplains has contributed to mimosa's invasiveness. Climate may also underly the difficulties faced by agents. Agents appear unable to impart effective control in the dry season because of low numbers which relates to mimosa's poor growth; nor in the wet season, when the impact from high numbers of agents is outstripped by mimosa's growth.     

不同生态恢复措施对草地样带食物消费的影响——以锡林郭勒盟为例

生态工程的实施对区域居民生产生活产生了重要影响。以锡林郭勒草地样带为例,利用2017年8月—2018年7月农牧户食物跟踪调查数据、农牧户问卷调查数据、生态恢复措施数据,结合土地利用数据和社会经济数据等,重点分析了不同生态恢复措施对锡林郭勒草地样带农牧户食物消费的影响。研究结果显示:(1)锡林郭勒草地样带生态恢复措施沿样带自北向南实施力度逐渐变弱,草地恢复措施由以草畜平衡、休牧和禁牧为主向休牧和围栏封育为主转变,草地恢复措施中对人类活动的限制也随之由弱变强;(2)沿草地样带自北向南居民食物消费形成了三种模式,在食物消费数量和消费结构上呈显出由牧区特征向农区特征的转变,即人均食物消费量沿样带递减,食物消费由肉蛋奶和蔬菜水果为主向粮食和蔬菜水果为主转变;(3)食物消费模式受到草地供给、收入及其结构、文化习俗和职业分布等生态、经济和社会多方面因素的影响。研究为实现区域生态、经济和社会的协调发展相关政策的制定提供参考。     

Individual variation in winter supplementary food consumption and its consequences for reproduction in wild birds

The provision of wild birds with supplementary food has increased substantially over recent decades. While it is assumed that provisioning birds is beneficial, supplementary feeding can have detrimental ‘carry‐over’ effects on reproductive traits. Due to difficulties in monitoring individual feeding behaviour, assessing how individuals within a population vary in their exploitation of supplementary food resources has been limited. Quantifying individual consumption of supplementary food is necessary to understand the operation of carry‐over effects at the individual level. We used Radio Frequency Identification (RFID) technology and automated feeders to estimate individual consumption of supplementary winter food in a large wild population of great tits Parus major and blue tits Cyanistes caeruleus. Using these data, we identified demographic factors that explained individual variation in levels of supplementary food consumption. We also tested for carry‐over effects of supplementary food consumption on recruitment, reproductive success and a measure of survival. Individual variation in consumption of supplementary food was explained by differences between species, ages, sexes and years. Individuals were consistent across time in their usage of supplementary resources. We found no strong evidence that the extent of supplementary food consumption directly influenced subsequent fitness parameters. Such effects may instead result from supplementary food influencing population demographics by enhancing the survival and subsequent breeding of less competitive individuals, which reduce average breeding parameters and increase density‐dependent competition. Carry‐over effects of supplementary feeding are not universal and may depend upon the temporal availability of the food provided. Our study demonstrates how RFID systems can be used to examine individual‐level behaviour with minimal effects on fitness.     

Adrenal androgen production in catarrhine primates and the evolution of adrenarche

Adrenarche is a developmental event involving differentiation of the adrenal gland and production of adrenal androgens, and has been hypothesized to play a role in the extension of the preadolescent phase of human ontogeny. It remains unclear whether any nonhuman primate species shows a similar suite of endocrine, biochemical, and morphological changes as are encompassed by human adrenarche. Here, we report serum concentrations of the adrenal androgens dehydroepiandrosterone (DHEA) and dehydroepiandrosterone sulfate (DHEAS) measured in 698 cross-sectional and mixed longitudinal serum samples from catarrhine primates ranging from 0.6 to 47 years of age. DHEAS in Pan is most similar to that of humans in both age-related pattern and absolute levels, and a transient early increase appears to be present in Gorilla. DHEA levels are highest in Cercocebus, Cercopithecus, and Macaca. We also tested for evidence of adaptive evolution in six genes that code for proteins involved in DHEA/S synthesis. Our genetic analyses demonstrate the protein-coding regions of these genes are highly conserved among sampled primates. We describe a tandem gene duplication event probably mediated by a retrotransposon that resulted in two 3-β-hydroxysteroid dehydrogenase/Delta 5-Delta 4 genes (HSD3B1 and HSD3B2) with tissue specific functions in catarrhines. In humans, HSD3B2 is expressed primarily in the adrenals, ovary, and testis, while HSD3B1 is expressed in the placenta. Taken together, our findings suggest that while adrenarche has been suggested to be unique to hominoids, the evolutionary roots for this developmental stage are more ancient.     

Study of dentition in lizards from Gran Ganaria Island (Canary Islands) and its ecological and evolutionary significance

The dentition of Gallotia stehlini from one extant and two subfossil populations dated as 4000 and 2000 years before present was studied. Body measurements were similar in the two subfossil populations, but much greater than the largest sizes observed today in G. stehlini. The morphology of the dental cusps in this G. stehlini differs greatly from that of other Lacertidae, including other congeneric Canarian species; this has been connected with a vegetarian diet. A decrease in heterodonty with size of the animal is also seen which contrasts strongly with the models observed in the Mediterranean lacertid lizards.     

Ecological significance of hypometabolism in nonhuman primates: allometry, adaptation, and deviant diets

The "Kleiber relationship" describes the interspecific allometry between body size and metabolism. Like other allometric relationships, the Kleiber relationship not only summarizes scaling effects across species but also provides a standard by which species can be compared. One well-noted deviation from the Kleiber relationship is "hypometabolism": metabolic rates below that expected for a given size. It has been suggested in the literature that hypometabolism may be a primitive mammalian trait, a thermoregulatory adaptation, an adaptation to arboreal folivory, or an adaptation to a diet that is deviant for body size. Data on primate physiology and behavior are used to evaluate these hypotheses. Only the deviant-diet hypothesis is supported by the data on nonhuman primates. Indeed, the Jarman-Bell relationship, which is the basis for this hypothesis, provides a more coherent explanation of correlated features of animal physiology and behavior than do the alternative models. Hypometabolism may be an energy-conserving adaptation to a variety of nutritional stresses. The present analysis underscores the point that metabolic rate, like foraging behavior, should be thought of as evolutionarily labile.     

Primates and pandemics: A biocultural approach to understanding disease transmission in human and nonhuman primates

Investigations into zoonotic disease outbreaks have been largely epidemiological and microbiological, with the primary focus being one of disease control and management. Increasingly though, the human–animal interface has proven to be an important driver for the acquisition and transmission of pathogens in humans, and this requires syncretic bio-socio-cultural enquiries into the origins of disease emergence, for more efficacious interventions. A biocultural lens is imperative for the examination of primate-related zoonoses, for the human-primate interface is broad and multitudinous, involving both physical and indirect interactions that occur due to shared spaces and ecologies. I use the case example of a viral zoonotic epidemic that is currently endemic to India, the Kysanaur Forest Disease, to show how biocultural anthropology provides a broad and integrative perspective into infectious disease ecology and presents new insights into the determinants of disease outbreaks. Drawing on insights from epidemiology, political ecology, primate behavioral ecology and ethnoprimatology, this paper demonstrates how human-primate interactions and shared ecologies impact infectious disease spread between human and nonhuman primate groups.     

Experimental evidence for ecological selection on genome variation in the wild

Understanding natural selection's effect on genetic variation is a major goal in biology, but the genome‐scale consequences of contemporary selection are not well known. In a release and recapture field experiment we transplanted stick insects to native and novel host plants and directly measured allele frequency changes within a generation at 186 576 genetic loci. We observed substantial, genome‐wide allele frequency changes during the experiment, most of which could be attributed to random mortality (genetic drift). However, we also documented that selection affected multiple genetic loci distributed across the genome, particularly in transplants to the novel host. Host‐associated selection affecting the genome acted on both a known colour‐pattern trait as well as other (unmeasured) phenotypes. We also found evidence that selection associated with elevation affected genome variation, although our experiment was not designed to test this. Our results illustrate how genomic data can identify previously underappreciated ecological sources and phenotypic targets of selection.     

Diet of the gracile mouse opossum (Gracilinanus microtarsus) (Didelphimorphia: Didelphidae) in a Brazilian cerrado: patterns of food consumption and intrapopulation variation

The diet of the gracile mouse opossum Gracilinanus microtarsus was studied in a cerrado remnant in south-eastern Brazil through the analysis of faeces sampled from adult individuals. Patterns of food resource consumption were assessed using the statistics of per cent occurrence. Intrapopulation variation in the number of food items detected in faeces as a function of relevant factors was inferred using generalized linear models. The latter statistical formalism also allowed variation in the number of food items detected in faeces to be interpreted in terms of rate ratios among levels of significant factors. Insects, spiders, snails and fruits were detected in the faeces of G. microtarsus , with insects, particularly termites, beetles and ants, being the most frequently detected food resource. These food resources were consumed in proportion to their relative abundance in the cerrado, suggesting that G . microtarsus is an opportunistic forager feeding primarily on insects. The generalized linear model identified sex, season and food resource as significant factors affecting the number of food items detected in faeces, as well as interactions between sex and season and season and food resource. Rate ratios calculated between sexes within seasons showed that the number of food items detected in the faeces of males was larger than that detected in the faeces of females in the warm-wet and cool-dry seasons. Rate ratios calculated between seasons within sexes showed different trends in the number of food items detected in faeces for each significant food resource. It is suggested that differences in the number of food items detected in faeces between sexes within season and between seasons within sexes are related to energetic requirements associated with reproduction.