Brain organization of gorillas reflects species differences in ecology

Gorillas include separate eastern (Gorilla beringei) and western (Gorilla gorilla) African species that diverged from each other approximately 2 million years ago. Although anatomical, genetic, behavioral, and socioecological differences have been noted among gorilla populations, little is known about variation in their brain structure. This study examines neuroanatomical variation between gorilla species using structural neuroimaging. Postmortem magnetic resonance images were obtained of brains from 18 captive western lowland gorillas (Gorilla gorilla gorilla), 15 wild mountain gorillas (Gorilla beringei beringei), and 3 Grauer's gorillas (Gorilla beringei graueri) (both wild and captive). Stereologic methods were used to measure volumes of brain structures, including left and right frontal lobe gray and white matter, temporal lobe gray and white matter, parietal and occipital lobes gray and white matter, insular gray matter, hippocampus, striatum, thalamus, each hemisphere and the vermis of the cerebellum, and the external and extreme capsules together with the claustrum. Among the species differences, the volumes of the hippocampus and cerebellum were significantly larger in G. gorilla than G. beringei. These anatomical differences may relate to divergent ecological adaptations of the two species. Specifically, G. gorilla engages in more arboreal locomotion and thus may rely more on cerebellar circuits. In addition, they tend to eat more fruit and have larger home ranges and consequently might depend more on spatial mapping functions of the hippocampus. Am J Phys Anthropol 156:252–262, 2015. © 2014 Wiley Periodicals, Inc.     

Extreme primates: Ecology and evolution of Asian lorises

Asia's slow and slender lorises (Nycticebus and Loris) are among nature's most extreme primates. Until recently, it was not understood why lorises have such huge forward‐facing eyes, strange steady climbing locomotion, tiny dependent babies, and a bite that potentially can kill a human! Indeed, early studies described them as slow, solitary, and boring. Twenty years of field research now indicate that lorises are among the most intriguing mammal species.     

The evolution of social philopatry in female primates

The transition from solitary life to sociality is considered one of the major transitions in evolution. In primates, this transition is currently not well understood. Traditional verbal models appear insufficient to unravel the complex interplay of environmental and demographic factors involved in the evolution of primate sociality, and recent phylogenetic reconstructions have produced conflicting results. We therefore analyze a theoretical model for the evolution of female social philopatry that sheds new light on the question why most primates live in groups. In individual-based simulations, we study the evolution of dispersal strategies of both resident females and their offspring. The model reveals that social philopatry can evolve through kin selection, even if retention of offspring is costly in terms of within-group resource competition and provides no direct benefits. Our model supports the role of predator avoidance as a selective pressure for group-living in primates, but it also suggests that a second benefit of group-living, communal resource defense, might be required to trigger the evolution of sizable groups. Lastly, our model reveals that seemingly small differences in demographic parameters can have profound effects on primate social evolution.     

The crown joules: energetics,ecology, and evolution in humans and other primates

Biological diversity is metabolic diversity: Differences in anatomy, physiology, life history, and activity reflect differences in energy allocation and expenditure among traits and tasks. Traditional frameworks in primatology, human ecology, public health, and paleoanthropology view daily energy expenditure as being more variable within than between species, changing with activity level but essentially fixed for a given body size. Growing evidence turns this view on its head. Total energy expenditure (kcal/d), varies relatively little within species, despite variation in physical activity; it varies considerably among species even after controlling for the effect of body size. Embracing this emerging paradigm requires rethinking potential trade‐offs in energy allocation within and between species, assessing evidence of metabolic acceleration within lineages, and abandoning activity‐based estimates of total energy expenditure. Difficult and exciting work lies ahead in the effort to untangle the ecological and evolutionary pressures shaping primate metabolic diversity.     

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.     

The coevolution of innovation and technical intelligence in primates

In birds and primates, the frequency of behavioural innovation has been shown to covary with absolute and relative brain size, leading to the suggestion that large brains allow animals to innovate, and/or that selection for innovativeness, together with social learning, may have driven brain enlargement. We examined the relationship between primate brain size and both technical (i.e. tool using) and non-technical innovation, deploying a combination of phylogenetically informed regression and exploratory causal graph analyses. Regression analyses revealed that absolute and relative brain size correlated positively with technical innovation, and exhibited consistently weaker, but still positive, relationships with non-technical innovation. These findings mirror similar results in birds. Our exploratory causal graph analyses suggested that technical innovation shares strong direct relationships with brain size, body size, social learning rate and social group size, whereas non-technical innovation did not exhibit a direct relationship with brain size. Nonetheless, non-technical innovation was linked to brain size indirectly via diet and life-history variables. Our findings support ‘technical intelligence’ hypotheses in linking technical innovation to encephalization in the restricted set of primate lineages where technical innovation has been reported. Our findings also provide support for a broad co-evolving complex of brain, behaviour, life-history, social and dietary variables, providing secondary support for social and ecological intelligence hypotheses. The ability to gain access to difficult-to-extract, but potentially nutrient-rich, resources through tool use may have conferred on some primates adaptive advantages, leading to selection for brain circuitry that underlies technical proficiency.     

Cranial capacity and performance on delay-response task correlated with principal sulcus length in monkeys

During the process of evolution, a selective advantage may have been gained by organisms that had the ability to utilize mentally stored information of a stimulus rather than the stimulus itself. The ability to temporarily store and mentally operate on stimulus information is often termed “working memory.” Within the neocortex of primates, the functional anatomic subdivision surrounding the principal (rectus) sulcus plays an important role in modulating the performance of delay-response tasks in monkeys (representing working memory). However, it appears that no study has investigated the direct relationship between the length of the principal sulcus and performance on a delay-response task. Therefore, this paper investigates the relationships between principal sulcus length and performance on delay-response tasks. However, to control for the effect of overall brain size on this relationship, cranial capacity is analyzed with both principal sulcus length and delay-response performance. Results support a consistent and significant correlation between principal sulcus length and performance on delayed-response tasks in a variety of Old World and New World monkeys. Principal sulcus length is also significantly correlated with cranial capacity; however, cranial capacity is not significantly correlated with performance on delayed-response tasks. The results of this investigation provide a method for analyzing cranial capacity and working-memory abilities in select primates based on principal sulcus length, and may prove useful for interpreting endocasts in the primate fossil record. Am J Phys Anthropol 109:33–40. © 1999 Wiley-Liss, Inc.     

Problems of body-weight estimation in fossil primates

Body-weight estimates of fossil primates are commonly used to infer many important aspects of primate paleobiology, including diet, ecology, and relative encephalization. It is important to examine carefully the methodologies and problems associated with such estimates and the degree to which one can have confidence in them. New regression equations for predicting body weight in fossil primates are given which provide body-weight estimates for most nonhominid primate species in the fossil record. The consequences of using different subgroups (evolutionary “grades”) of primate species to estimate fossil-primate body weights are explored and the implications of these results for interpreting the primate fossil record are discussed. All species (fossil and extant) were separated into the following “grades”: prosimian grade, monkey grade, ape grade, anthropoid grade, and all-primates grade. Regression equations relating lower molar size to body weight for each of these grades were then calculated. In addition, a female-anthropoid grade regression was also calculated for predicting body weight infernales of extinct, sexually dimorphic anthropoid species. These equations were then used to generate the fossil-primate body weights. In many instances, the predicted fossil-primate body weights differ substantially from previous estimates.     

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.     

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.     

Co‐evolution of cerebral and cerebellar expansion in cetaceans

Cetaceans possess brains that rank among the largest to have ever evolved, either in terms of absolute mass or relative to body size. Cetaceans have evolved these huge brains under relatively unique environmental conditions, making them a fascinating case study to investigate the constraints and selection pressures that shape how brains evolve. Indeed, cetaceans have some unusual neuroanatomical features, including a thin but highly folded cerebrum with low cortical neuron density, as well as many structural adaptations associated with acoustic communication. Previous reports also suggest that at least some cetaceans have an expanded cerebellum, a brain structure with wide‐ranging functions in adaptive filtering of sensory information, the control of motor actions, and cognition. Here, we report that, relative to the size of the rest of the brain, both the cerebrum and cerebellum are dramatically enlarged in cetaceans and show evidence of co‐evolution, a pattern of brain evolution that is convergent with primates. However, we also highlight several branches where cortico‐cerebellar co‐evolution may be partially decoupled, suggesting these structures can respond to independent selection pressures. Across cetaceans, we find no evidence of a simple linear relationship between either cerebrum and cerebellum size and the complexity of social ecology or acoustic communication, but do find evidence that their expansion may be associated with dietary breadth. In addition, our results suggest that major increases in both cerebrum and cerebellum size occurred early in cetacean evolution, prior to the origin of the major extant clades, and predate the evolution of echolocation.     

Abundance, diversity, and patterns of distribution of primates on the Tapiche River in Amazonian Peru

This work presents data on the relative diversity, abundance, and distribution patterns of primates in a 20 km2 area of the Tapiche River in the Peruvian Amazon. Population data were collected while the study area was both inundated and dry (March to September 1997) using conventional line-transect census techniques. Survey results reflected the presence of 11 primate species, but population parameters on only eight of the species will be presented, including saddleback tamarins (Saguinus fuscicollis), Bolivian squirrel monkeys (Saimiri boliviensis), brown capuchins (Cebus apella), white-fronted capuchins (Cebus albifrons), monk sakis (Pithecia monachus), red titi monkeys (Callicebus cupreus), red uakaris (Cacajao calvus), and red howler monkeys (Alouatta seniculus). Woolly monkeys (Lagothrix lagotricha), night monkeys (Aotus nancymaae), and pygmy marmosets (Callithrix pygmaea) were also seen in the area. The data for the smaller-bodied primates is similar to that reported almost 18 years earlier, but the data for the larger-bodied primates reflect a loss in the number of animals present in the area. Pressure from hunters and the timber industry may account for declining numbers of large-bodied primates, while it appears that natural features peculiar to the conservation area contribute to the patchy pattern of distribution.     

Compliant walking in primates: elbow and knee yield in primates compared to other mammals

It has been suggested that primates utilize a compliant gait to help reduce peak locomotor stresses on their limbs (Schmitt [1994] J. Hum. Evol. 26:441-458; Schmitt [ 1998] Primate Locomotion, p. 175-200; Schmitt [ 1999] J. Zool. Lond. 248:149-160). However, the components of such a gait, i.e., increased step length, prolonged contact time, and substantial limb yield, have only been documented on a handful of primate species. In order to explore the generality of this claim, elbow and knee angles during walking were documented at touchdown, midstance, and liftoff in a sample of primates, carnivores, marsupials, rodents, and artiodactyls, all under 25 kg. Limb yield was calculated as the change in angle from touchdown to midstance, and re-extension as the change in angle from midstance to liftoff for both forelimbs and hind limbs. Use of a compliant gait (as reflected in significant limb yield) in primates was confirmed for both forelimbs and hind limbs. However, there was variability within primates in the degree of either elbow or knee yield. Surprisingly, marsupials were found to exhibit almost as much elbow yield and even greater knee yield than primates. Carnivores and rodents display a modest amount of limb yield during walking, while artiodactyls appear to display a relatively stiff gait. These data are consistent with the suggestion that the use of a compliant gait to attenuate peak substrate reaction forces may have facilitated the primate invasion of a small-branch niche. However, limb compliance (as reflected by elbow or knee yield) does not appear to be exclusive to the primate order.     

Vertical clinging and leaping revisited: vertical support use as the ancestral condition of strepsirrhine primates

A re-examination of primate foot and knee anatomy suggests that strepsirrhine primates (adapiforms and lemuriforms) possess a unique and derived hindlimb related to their use of vertical supports. In contrast, leaping adaptations are older and shared by both major euprimate clades, Strepsirrhini and Haplorhini. Combining this derived hindlimb anatomy with leaping suggests that ancestral strepsirrhines were at least frequent vertical support users and leapers, and perhaps vertical clingers and leapers. These initial strepsirrhine adaptations were preadaptive for later lemuriform vertical clingers and leapers. In contrast, haplorhine vertical clingers and leapers require additional foot and leg modifications to accommodate a vertical clinging and leaping lifestyle. The movement pattern called vertical clinging and leaping evolved independently among different primate lineages throughout primate evolutionary history for several different ecological reasons.     

The social organizations of squirrel monkeys: Implications for ecological models of social evolution

“Squirrel-monkeys occur in a considerable number of slightly different forms, but all are built upon a similar body plan and have a basic color scheme. One of the larger races—from inner Perú—is also the most colorful and one of the brightest colored of all mammals. It may be taken as a point of departure. The top of the head and the upper and outer parts of the body and the upper side of the basal half of the tail are a vivid green, with a pepper and salt effect of yellow and gray. The face is pure white except for black spectacles, muzzle and chin; the throat, chest, underside, insides of limbs, and the underside of the basal half of the tail are brilliant daffodil yellow. The terminal half of the tail is jet black and rather bushy. The flesh of the hands is pale pink. Other races vary in the intensity of the green and yellow, so that some may be olive brown above and white below, and in the amount and arrangement of the black areas on the face and the tip of the tail. Some have almost naked ears, others have these organs clothed in short fur, and still others bear thereupon long tufts or fringes. All these variations seem to blend into the other geographically . . . some of these pure color variations may constitute valid regional subspecies or even species. . . .” I. T. Sanderson¹ (p. 77).     

Built to last: The structure,function, and evolution of primate dental enamel

The teeth of every primate, living and extinct, are covered by a hard, durable layer of enamel. This is not unique: Almost all mammals have enamel-covered teeth. In addition, all of the variations in enamel structure that occur in primates are also found in other groups of mammals. Nevertheless, the very complexity of enamel and the variation we see in it on the teeth of living and fossil primates raise questions about its evolutionary significance. Is the complex structure of primate enamel adaptive? What, if anything, does enamel structure tell us about primate phylogeny? To answer these questions, we need to look more closely at the characteristics of prismatic enamel in primates and at the distribution of those characteristics, both in relation to our knowledge of primate dental function and feeding ecology and from a phylogenetic perspective.