Brief communication: Hair density and body mass in mammals and the evolution of human hairlessness

Humans are unusual among mammals in appearing hairless. Several hypotheses propose explanations for this phenotype, but few data are available to test these hypotheses. To elucidate the evolutionary history of human “hairlessness,” a comparative approach is needed. One previous study on primate hair density concluded that great apes have systematically less dense hair than smaller primates. While there is a negative correlation between body size and hair density, it remains unclear whether great apes have less dense hair than is expected for their body size. To revisit the scaling relationship between hair density and body size in mammals, I compiled data from the literature on 23 primates and 29 nonprimate mammals and conducted Phylogenetic Generalized Least Squares regressions. Among anthropoids, there is a significant negative correlation between hair density and body mass. Chimpanzees display the largest residuals, exhibiting less dense hair than is expected for their body size. There is a negative correlation between hair density and body mass among the broader mammalian sample, although the functional significance of this scaling relationship remains to be tested. Results indicate that all primates, and chimpanzees in particular, are relatively hairless compared to other mammals. This suggests that there may have been selective pressures acting on the ancestor of humans and chimpanzees that led to an initial reduction in hair density. To further understand the evolution of human hairlessness, a systematic study of hair density and physiology in a wide range of species is necessary. Am J Phys Anthropol 152:145–150, 2013. © 2013 Wiley Periodicals, Inc.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/99654/1/ajpa22333.pd

The evolution of self-control

This work was supported by the National Evolutionary Synthesis Center (NESCent) through support of a working group led by C.L.N. and B.H. NESCent is supported by the National Science Foundation (NSF) EF-0905606. For training in phylogenetic comparative methods, we thank the AnthroTree Workshop (supported by NSF BCS-0923791). Y.S. thanks the National Natural Science Foundation of China (Project 31170995) and National Basic Research Program (973 Program: 2010CB833904). E.E.B. thanks the Duke Vertical Integration Program and the Duke Undergraduate Research Support Office. J.M.P. was supported by a Newton International Fellowship from the Royal Society and the British Academy. L.R.S. thanks the James S. McDonnell Foundation for Award 220020242. L.J.N.B. and M.L.P. acknowledge the National Institutes of Mental Health (R01-MH096875 and R01-MH089484), a Duke Institute for Brain Sciences Incubator Award (to M.L.P.), and a Duke Center for Interdisciplinary Decision Sciences Fellowship (to L.J.N.B.). E.V. and E.A. thank the Programma Nazionale per la Ricerca–Consiglio Nazionale delle Ricerche (CNR) Aging Program 2012–2014 for financial support, Roma Capitale–Museo Civico di Zoologia and Fondazione Bioparco for hosting the Istituto di Scienze e Tecnologie della Cognizione–CNR Unit of Cognitive Primatology and Primate Centre, and Massimiliano Bianchi and Simone Catarinacci for assistance with capuchin monkeys. K.F. thanks the Japan Society for the Promotion of Science (JSPS) for Grant-in-Aid for Scientific Research 20220004. F. Aureli thanks the Stages in the Evolution and Development of Sign Use project (Contract 012-984 NESTPathfinder) and the Integrating Cooperation Research Across Europe project (Contract 043318), both funded by the European Community’s Sixth Framework Programme (FP6/2002–2006). F. Amici was supported by Humboldt Research Fellowship for Postdoctoral Researchers (Humboldt ID 1138999). L.F.J. and M.M.D. acknowledge NSF Electrical, Communications, and Cyber Systems Grant 1028319 (to L.F.J.) and an NSF Graduate Fellowship (to M.M.D.). C.H. thanks Grant-in-Aid for JSPS Fellows (10J04395). A.T. thanks Research Fellowships of the JSPS for Young Scientists (21264). F.R. and Z.V. acknowledge Austrian Science Fund (FWF) Project P21244-B17, the European Research Council (ERC) under the European Union’s Seventh Framework Programme (FP/2007–2013)/ERC Grant Agreement 311870 (to F.R.), Vienna Science and Technology Fund Project CS11-026 (to Z.V.), and many private sponsors, including Royal Canin for financial support and the Game Park Ernstbrunn for hosting the Wolf Science Center. S.M.R. thanks the Natural Sciences and Engineering Research Council (Canada). J.K.Y. thanks the US Department of Agriculture–Wildlife Services–National Wildlife Research Center. J.F.C. thanks the James S. McDonnell Foundation and Alfred P. Sloan Foundation. E.L.M. and B.H. thank the Duke Lemur Center and acknowledge National Institutes of Health Grant 5 R03 HD070649-02 and NSF Grants DGE-1106401, NSF-BCS-27552, and NSF-BCS-25172. This is Publication 1265 of the Duke Lemur Center.Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.PostprintPeer reviewe

Puberty initiates a unique stage of social learning and development prior to adulthood: Insights from studies of adolescence in wild chimpanzees

In humans, puberty initiates a period of rapid growth, change, and formative neurobehavioral development. Brain and behavior changes during this maturational window contribute to opportunities for social learning. Here we provide new insights into adolescence as a unique period of social learning and development by describing field studies of our closest living relatives, chimpanzees. Like humans, chimpanzees have a multiyear juvenile life stage between weaning and puberty onset followed by a multiyear adolescent life stage after pubertal onset but prior to socially-recognized adulthood. As they develop increasing autonomy from caregivers, adolescent chimpanzees explore and develop many different types of social relationships with a wide range of individuals in a highly flexible social environment. We describe how adolescent social motivations and experiences differ from those of juveniles and adults and expose adolescents to high levels of uncertainty, risk, and vulnerability, as well as opportunities for adaptive social learning. We discuss how these adolescent learning experiences may be shaped by early life and in turn shape varied adult social outcomes. We outline how future chimpanzee field research can contribute in new ways to a more integrative interdisciplinary understanding of adolescence as a developmental window of adaptive social learning and resilience

Parallel lasers and digital photography to estimate limb size of chimpanzees (Pan troglodytes) at Ngogo, Kibale National Park, Uganda

How animals grow and when they stop growing are key variables for understanding life history evolution. Although theoretically straightforward, it is logistically difficult to take body size measurements of wild animals, especially endangered and arboreal primates. Here we employ a method that has gained popularity over the past decade: digital photography combined with parallel lasers. Two laser pointers are set at a known distance apart and then projected on the animal to act as a scale in the photograph. We used this method to estimate limb length and width in a large, cross-sectional sample of mid- to late-adolescent and young adult male chimpanzees at Ngogo in Kibale National Park, Uganda. After several years of modifying our methods, we present a protocol for estimating limb length and width in wild chimpanzees. We found that by mid- to late-adolescence, male chimpanzees have reached adult height, as chimpanzees between 12 and 20 years of age did not differ in their forearm or lower leg lengths. However, mid- to late-adolescent male chimpanzees appear to continue gaining mass, as we found a weak but positive correlation between age and limb width for both forearms and lower legs. Although our method proved relatively precise, we encountered several sources of error throughout this study, such as ensuring that the lasers were indeed parallel and in identifying anatomical landmarks in the photographs. We discuss these challenges with the hope of increasing transparency and collaboration in future studies of primate body size

Assessing sources of error in comparative analyses of primate behavior: Intraspecific variation in group size and the social brain hypothesis

Phylogenetic comparative methods have become standard for investigating evolutionary hypotheses, including in studies of human evolution. While these methods account for the non-independence of trait data due to phylogeny, they often fail to consider intraspecific variation, which may lead to biased or erroneous results. We assessed the degree to which intraspecific variation impacts the results of comparative analyses by investigating the >social brain> hypothesis, which has provided a framework for explaining complex cognition and large brains in humans. This hypothesis suggests that group life imposes a cognitive challenge, with species living in larger social groups having comparably larger neocortex ratios than those living in smaller groups. Primates, however, vary considerably in group size within species, a fact that has been ignored in previous analyses. When within-species variation in group size is high, the common practice of using a mean value to represent the species may be inappropriate. We conducted regression and resampling analyses to ascertain whether the relationship between neocortex ratio and group size across primate species persists after controlling for within-species variation in group size. We found that in a sample of 23 primates, 70% of the variation in group size was due to between-species variation. Controlling for within-species variation in group size did not affect the results of phylogenetic analyses, which continued to show a positive relationship between neocortex ratio and group size. Analyses restricted to non-monogamous primates revealed considerable intraspecific variation in group size, but the positive association between neocortex ratio and group size remained even after controlling for within-species variation in group size. Our findings suggest that the relationship between neocortex size and group size in primates is robust. In addition, our methods and associated computer code provide a way to assess and account for intraspecific variation in other comparative analyses of primate evolution.For training in phylogenetic comparative methods, we thank the AnthroTree Workshop that is supported by the National Science Foundation (BCS-0923791) and the National Evolutionary Synthesis Center (NSF grant EF-0905606). A.A. Sandel was supported by the National Science Foundation Graduate Research Fellowship under Grant No. F031543. J.A. Miller was supported by a department grant from the National Science Foundation (DGE-0801634). J.C. Mitani is currently supported by National Institutes of Health RO1AG049395. C.L. Nunn was supported by Duke University and the National Science Foundation (BCS-1355902). S.K. Patterson was supported by the National Science Foundation Graduate Research Fellowship under Grant No. DGE-1311230. L.Z. Garamszegi was supported by funds from the Spanish Government within the frame of the “Plan Nacional” program (ref. no. CGL2012- 38262 and CGL2012-40026-C02-01) and the National Research, Development and Innovation Office, Hungary (NKFIH, K-115970)

Group Size Predicts Social but Not Nonsocial Cognition in Lemurs

<div><p>The social intelligence hypothesis suggests that living in large social networks was the primary selective pressure for the evolution of complex cognition in primates. This hypothesis is supported by comparative studies demonstrating a positive relationship between social group size and relative brain size across primates. However, the relationship between brain size and cognition remains equivocal. Moreover, there have been no experimental studies directly testing the association between group size and cognition across primates. We tested the social intelligence hypothesis by comparing 6 primate species (total N = 96) characterized by different group sizes on two cognitive tasks. Here, we show that a species’ typical social group size predicts performance on cognitive measures of social cognition, but not a nonsocial measure of inhibitory control. We also show that a species’ mean brain size (in absolute or relative terms) does not predict performance on either task in these species. These data provide evidence for a relationship between group size and social cognition in primates, and reveal the potential for cognitive evolution without concomitant changes in brain size. Furthermore our results underscore the need for more empirical studies of animal cognition, which have the power to reveal species differences in cognition not detectable by proxy variables, such as brain size.</p></div

Species’ performance on the social cognition and inhibitory control tasks.

<p>The tree structure at the bottom of the figure represents the phylogenetic relationships between the species. Error bars reflect the standard error of the mean.</p

Performance in the cognitive tasks as a function of social group size and residual endocranial volume (ECV), a measure of relative brain size.

<p>We tested the hypotheses that social group size and relative brain size would predict species performance. A) As predicted by the social intelligence hypothesis, species characterized by larger social groups performed better in the social cognition task. Relative brain size did not explain species’ performance, and the slope of the relationship was negative. B) Group size did not predict performance on the non-social inhibitory control task. As in the social task, relative brain size was not a predictor of performance on the inhibitory control task.</p

Scores (percent correct) from the social cognition task.

<p>Performance in each condition was compared to chance expectation (50%) using one-sample Wilcoxon tests to evaluate the hypothesis that subjects would attempt to steal the food that their competitor could not see.</p