The coevolution of play and the cortico-cerebellar system in primates.

Primates are some of the most playful animals in the natural world, yet the reason for this remains unclear. One hypothesis posits that primates are so playful because playful activity functions to help develop the sophisticated cognitive and behavioural abilities that they are also renowned for. If this hypothesis were true, then play might be expected to have coevolved with the neural substrates underlying these abilities in primates. Here, we tested this prediction by conducting phylogenetic comparative analyses to determine whether play has coevolved with the cortico-cerebellar system, a neural system known to be involved in complex cognition and the production of complex behaviour. We used phylogenetic generalised least squares analyses to compare the relative volume of the largest constituent parts of the primate cortico-cerebellar system (prefrontal cortex, non-prefrontal heteromodal cortical association areas, and posterior cerebellar hemispheres) to the mean percentage of time budget spent in play by a sample of primate species. Using a second categorical data set on play, we also used phylogenetic analysis of covariance to test for significant differences in the volume of the components of the cortico-cerebellar system among primate species exhibiting one of three different levels of adult-adult social play. Our results suggest that, in general, a positive association exists between the amount of play exhibited and the relative size of the main components of the cortico-cerebellar system in our sample of primate species. Although the explanatory power of this study is limited by the correlational nature of its analyses and by the quantity and quality of the data currently available, this finding nevertheless lends support to the hypothesis that play functions to aid the development of cognitive and behavioural abilities in primates

Resistance to antibiotics of clinical relevance in the fecal microbiota of Mexican wildlife.

There are a growing number of reports of antibiotic resistance (ATBR) in bacteria living in wildlife. This is a cause for concern as ATBR in wildlife represents a potential public health threat. However, little is known about the factors that might determine the presence, abundance and dispersion of ATBR bacteria in wildlife. Here, we used culture and molecular methods to assess ATBR in bacteria in fecal samples from howler monkeys (Alouatta palliata), spider monkeys (Ateles geoffroyi), tapirs (Tapirus bairdii) and felids (jaguars, Panthera onca; pumas, Puma concolor; jaguarundis, Puma yagouaroundi; and ocelots, Leopardus pardalis) living freely in two regions of the Mexican state of Veracruz under different degrees of human influence. Overall, our study shows that ATBR is commonplace in bacteria isolated from wildlife in southeast Mexico. Most of the resistances were towards old and naturally occurring antibiotics, but we also observed resistances of potential clinical significance. We found that proximity to humans positively affected the presence of ATBR and that ATBR was higher in terrestrial than arboreal species. We also found evidence suggesting different terrestrial and aerial routes for the transmission of ATBR between humans and wildlife. The prevalence and potential ATBR transfer mechanisms between humans and wildlife observed in this study highlight the need for further studies to identify the factors that might determine ATBR presence, abundance and distribution.The authors acknowledge the National Council of Science of Technology (CONACYT) in Mexico and the Veracruz State Government for providing partial financial support to JCA (Grant Number 108990). JCD was supported by grants from the Isaac Newton Trust and The Cambridge Humanities Research Grant Scheme. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.This is the final published version. It originally appeared in PLOS One at http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0107719

Acoustic allometry revisited: morphological determinants of fundamental frequency in primate vocal production

A fundamental issue in the evolution of communication is the degree to which signals convey accurate (“honest”) information about the signaler. In bioacoustics, the assumption that fundamental frequency (fo) should correlate with the body size of the caller is widespread, but this belief has been challenged by various studies, possibly because larynx size and body size can vary independently. In the present comparative study, we conducted excised larynx experiments to investigate this hypothesis rigorously and explore the determinants of fo. Using specimens from eleven primate species, we carried out an inter-specific investigation, examining correlations between the minimum fo produced by the sound source, body size and vocal fold length (VFL). We found that, across species, VFL predicted minimum fo much better than body size, clearly demonstrating the potential for decoupling between larynx size and body size in primates. These findings shed new light on the diversity of primate vocalizations and vocal morphology, highlighting the importance of vocal physiology in understanding the evolution of mammal vocal communication

The Ranging Costs of a Fallback Food: Liana Consumption Supplements Diet but Increases Foraging Effort in Howler Monkeys

Lianas are important components in the dynamics of tropical forests and represent fallback foods for some primates, yet little is known about their impact on primate ecology, behavior or fitness. Using 2 yr of field data, we investigated liana consumption and foraging effort in four groups of howler monkeys (two in bigger, more conserved forest fragments and two in smaller, less conserved fragments) to assess whether howler monkeys use lianas when and where food availability is scarce, and how liana consumption is related to foraging effort. Howler monkeys in smaller fragments spent more time consuming lianas and liana consumption was negatively related to the consumption of preferred food resources (fruit and Ficus spp.). Further, travel time was positively related to liana feeding time, but not to tree feeding time, and howler monkeys visited a greater number of food patches when feeding from liana leaves than when feeding from tree leaves. Our results suggest that these increases in foraging effort were related to the fact that lianas are mainly a source of leaves, and that liana patch size was probably smaller than tree patch size. While these results were clear when analyzing all four groups combined, however, they were not always significant in each of the groups individually. We suggest that this may be related to the differences in group size, patch size and the availability of resources among groups. Further studies are necessary to assess whether these dietary and behavioral adjustments negatively impact on the fitness and conservation of primates in fragments

The evolutionary drivers of primate scleral coloration

The drivers of divergent scleral morphologies in primates are currently unclear, though white sclerae are often assumed to underlie human hyper-cooperative behaviours. Humans are unusual in possessing depigmented sclerae whereas many other extant primates, including the closely-related chimpanzee, possess dark scleral pigment. Here, we use phylogenetic generalized least squares (PGLS) analyses with previously generated species-level scores of proactive prosociality, social tolerance (both n = 15 primate species), and conspecific lethal aggression (n = 108 primate species) to provide the first quantitative, comparative test of three existing hypotheses. The ‘self-domestication’ and ‘cooperative eye’ explanations predict white sclerae to be associated with cooperative, rather than competitive, environments. The ‘gaze camouflage’ hypothesis predicts that dark scleral pigment functions as gaze direction camouflage in competitive social environments. Notably, the experimental evidence that non-human primates draw social information from conspecific eye movements is unclear, with the latter two hypotheses having recently been challenged. Here, we show that white sclerae in primates are associated with increased cooperative behaviours whereas dark sclerae are associated with reduced cooperative behaviours and increased conspecific lethal violence. These results are consistent with all three hypotheses of scleral evolution, suggesting that primate scleral morphologies evolve in relation to variation in social environment

Socioecological factors affecting range defensibility among howler monkeys

Range defensibility is defined as the ability of animals to efficiently move over an area to monitor and defend it. Therefore, range defensibility can help understand the spatial structure of animal territoriality. We used howler monkeys (Alouatta spp), a genus for which no agreement on the extent of their territoriality exists, to investigate the factors mediating range defensibility. We compared the defensibility index (D) across 63 groups of howler monkeys, representing 8 different species, based on a literature review. All species, except Alouatta palliata, were classified as potentially territorial according to D, although there was high variability within and among species. Group size had a positive effect on D, probably due to the greater ability of groups to defend a territory as they become larger. Study area had a negative effect on D, perhaps suggesting that unlike small areas, large areas allow groups to have territories that do not require significant defense from neighbours. However, population density was the factor with the strongest effect on D, with greater monitoring of home ranges under high levels of competition. Our results suggest that howler monkeys are theoretically capable of maintaining a territory and suggest that animals can show a gradient in territoriality, which can be mediated by the competitive context in which it occurs

Evolutionary trade-off between vocal tract and testes dimensions in howler monkeys.

Males often face a trade-off between investments in precopulatory and postcopulatory traits [1], particularly when male-male contest competition determines access to mates [2]. To date, studies of precopulatory strategies have largely focused on visual ornaments (e.g., coloration) or weapon morphology (e.g., antlers, horns, and canines). However, vocalizations can also play an important role in both male competition and female choice [3-5]. We investigated variation in vocal tract dimensions among male howler monkeys (Alouatta spp.), which produce loud roars using a highly specialized and greatly enlarged hyoid bone and larynx [6]. We examined the relative male investment in hyoids and testes among howler monkey species in relation to the level of male-male competition and analyzed the acoustic consequences of variation in hyoid morphology. Species characterized by single-male groups have large hyoids and small testes, suggesting high levels of vocally mediated competition. Larger hyoids lower formant frequencies, probably increasing the acoustic impression of male body size and playing a role analogous to investment in large body size or weaponry. Across species, as the number of males per group increases, testes volume also increases, indicating higher levels of postcopulatory sperm competition, while hyoid volume decreases. These results provide the first evidence of an evolutionary trade-off between investment in precopulatory vocal characteristics and postcopulatory sperm production.We are grateful to Alexander Sliwa, Catalina Gomez, Robert Wallace, Michael Plavkan, Zelinda Braga Hirano, and Julio Cesar de Souza, Jr. for sharing data, Andrew Kitchener (National Museums Scotland) for loaning whole animal specimens, Michaela Gumpenberger and Jaap Saers for support with CT and MRI, Carolyn M. Crockett, Mariana Raño, and La Senda Verde Animal Refuge Bolivia for providing photographs and videos, Nadja Kavcik for help with the figures, and Dieter Lukas for help with statistical analyses. J.C.D. was funded by a Cambridge Humanities Research Grant. W.T.F. acknowledges support of ERC Advanced Grant SOMACCA (#230604) and Austrian Science Fund (FWF) grant W1234-G17.This is the final version of the article. It was first available from Elsevier via http://dx.doi.org/10.1016/j.cub.2015.09.02

Western gorilla space use suggests territoriality.

Funder: Sabine Plattner African CharitiesThe evolutionary origins of how modern humans share and use space are often modelled on the territorial-based violence of chimpanzees, with limited comparison to other apes. Gorillas are widely assumed to be non-territorial due to their large home ranges, extensive range overlap, and limited inter-group aggression. Using large-scale camera trapping, we monitored western gorillas in Republic of Congo across 60 km2. Avoidance patterns between groups were consistent with an understanding of the "ownership" of specific regions, with greater avoidance of their neighbours the closer they were to their neighbours' home range centres. Groups also avoided larger groups' home ranges to a greater extent, consistent with stronger defensive responses from more dominant groups. Our results suggest that groups may show territoriality, defending core regions of their home ranges against neighbours, and mirror patterns common across human evolution, with core areas of resident dominance and larger zones of mutual tolerance. This implies western gorillas may be a key system for understanding how humans have evolved the capacity for extreme territorial-based violence and warfare, whilst also engaging in the strong affiliative inter-group relationships necessary for large-scale cooperation

Rapid evolution of the primate larynx?

Tissue vibrations in the larynx produce most sounds that comprise vocal communication in mammals. Larynx morphology is thus predicted to be a key target for selection, particularly in species with highly developed vocal communication systems. Here, we present a novel database of digitally modeled scanned larynges from 55 different mammalian species, representing a wide range of body sizes in the primate and carnivoran orders. Using phylogenetic comparative methods, we demonstrate that the primate larynx has evolved more rapidly than the carnivoran larynx, resulting in a pattern of larger size and increased deviation from expected allometry with body size. These results imply fundamental differences between primates and carnivorans in the balance of selective forces that constrain larynx size and highlight an evolutionary flexibility in primates that may help explain why we have developed complex and diverse uses of the vocal organ for communication

Exponential Distribution of Locomotion Activity in Cell Cultures

In vitro velocities of several cell types have been measured using computer controlled video microscopy, which allowed to record the cells' trajectories over several days. On the basis of our large data sets we show that the locomotion activity displays a universal exponential distribution. Thus, motion resulting from complex cellular processes can be well described by an unexpected, but very simple distribution function. A simple phenomenological model based on the interaction of various cellular processes and finite ATP production rate is proposed to explain these experimental results.Comment: 4 pages, 3 figure