The size of the neocortex in relation to ecology and social structure in monkeys and apes.

In an attempt to reveal factors associated with neocortical development in monkeys and apes (anthropoids), relationships between the relative size of the neocortex and differences in ecology and social structure were examined for 24 genera of 11 subfamilies. Relative sizes of the neocortex (RSNs) in a given group were assessed as the difference between actual neocortical volume and the volume expected from an allometric relationship between neocortical volume and the volume of the rest of the brain. We found that RSNs are related to diet and social structure: frugivorous anthropoids had higher values of RSNs than folivorous anthropoids, and polygynous anthropoids had significantly higher values of RSNs than monogynous anthropoids. Furthermore, RSNs were positively correlated with the size of the troop. These results suggest that development of the neocortex is associated with both diet and social structure in anthropoids.     

Relative brain size,stratification, and social structure in anthropoids

The relationships between relative brain size and both stratification and social structure were examined in a total of 82 species of anthropoids. The species were divided into a total of 42 congeneric groups which consisted of congeneric species with similar ecologies and social structures. The relative brain size (RBS) was calculated for each congeneric group in each superfamily, based on an allometric equation describing the relationship between brain weight and body weight for each superfamily. Among congeneric groups with a common category of diet, RBS was significantly greater for terrestrial groups than for arboreal groups, and for polygynous (i.e. multi-female) groups than for monogynous (single-female) groups. Furthermore, RBS was significantly and positively correlated with the size of the home range per individual for the Cercopithecoidea, and with troop size for frugivorous groups of the Ceboidea. The results obtained suggest that factors associated with terrestriality and polygyny have been involved in the increases in relative brain size of anthropoids.     

Diets of fossil primates from the Fayum Depression of Egypt: a quantitative analysis of molar shearing

Over the last 90 years, Eocene and Oligocene aged sediments in the Fayum Depression of Egypt have yielded at least 17 genera of fossil primates. However, of this diverse sample the diets of only four early Oligocene anthropoid genera have been previously studied using quantitative methods. Here we present dietary assessments for 11 additional Fayum primate genera based on the analysis of body mass and molar shearing crest development. These studies reveal that all late Eocene Fayum anthropoids were probably frugivorous despite marked subfamilial differences in dental morphology. By contrast, late Eocene Fayum prosimians demonstrated remarkable dietary diversity, including specialized insectivory (Anchomomys), generalized frugivory (Plesiopithecus), frugivory+insectivory (Wadilemur), and strict folivory (Aframonius). This evidence that sympatric prosimians and early anthropoids jointly occupied frugivorous niches during the late Eocene reinforces the hypothesis that changes in diet did not form the primary ecological impetus for the origin of the Anthropoidea. Early Oligocene Fayum localities differ from late Eocene Fayum localities in lacking large-bodied frugivorous and folivorous prosimians, and may document the first appearance of primate communities with trophic structures like those of extant primate communities in continental Africa. A similar change in primate community structure during the Eocene-Oligocene transition is not evident in the Asian fossil record. Putative large anthropoids from the Eocene of Asia, such as Amphipithecus mogaungensis, Pondaungia cotteri, and Siamopithecus eocaenus, share with early Oligocene Fayum anthropoids derived features of molar anatomy related to an emphasis on crushing and grinding during mastication. However, these dental specializations are not seen in late Eocene Fayum anthropoids that are broadly ancestral to the later-occurring anthropoids of the Fayum's upper sequence. This lack of resemblance to undisputed Eocene African anthropoids suggests that the "progressive" anthropoid-like dental features of some large-bodied Eocene Asian primates may be the result of dietary convergence rather than close phyletic affinity with the Anthropoidea.     

Body Mass Estimates for Eocene Eosimiid and Amphipithecid Primates Using Prosimian and Anthropoid Scaling Models

We estimated body masses for middle to late Eocene East Asian eosimiids and amphipithecids from the crown areas of cheek teeth. First, we calculated body mass estimate equations via an extant primate sample of 11 prosimian and 30 anthropoid species, and compared the reliability of the resulting body mass estimate regressions. M ^1–2 and M _1–2 are better body mass estimators, especially for fossils with few samples, because of their low intraspecific variations in dimensions. Moreover, body masses derived from M _1–2 tend to indicate lower estimate error than those from other cheek teeth. The relationships between tooth crown areas and body mass differ between prosimians and anthropoids; the estimated body mass from crown area of P ⁴ or any molar will be larger if anthropoids, instead of prosimians, are used as a reference taxon. Second, We applied the regressions to the fossil primates. The estimated body masses in kg are as follows: Eosimias centennicus, 0.16; E. sinensis, 0.14; Eosimiidae indet. from the Pondaung Formation, 0.41; Bahinia pondaungensis, 0.57; Myanmarpithecus yarshensis, 1.8; Amphipithecus mogaungensis, 6.8; Pondaungia cotteri, 5.9; Pondaungia savagei, 8.8; Siamopithecus eocaenus, 5.9. Eosimiids fit the prosimian model better than the anthropoid model. Amphipithecids do not fit one model particularly better than the other, as the estimates vary considerably according to the tooth used and the reference taxon. The anthropoid model gives smaller differences between upper- and lower-molar-based body mass estimates, but premolars are relatively much smaller in amphipithecids than in extant prosimians and anthropoids.     

New primate first metatarsals from the Paleogene of Egypt and the origin of the anthropoid big toe

The specialized grasping feet of primates, and in particular the nature of the hallucal grasping capabilities of living strepsirrhines and tarsiers (i.e., ‘prosimians’), have played central roles in the study of primate origins. Prior comparative studies of first metatarsal (Mt1) morphology have documented specialized characters in living prosimians that are indicative of a more abducted hallux, which in turn is often inferred to be related to an increased ability for powerful grasping. These include a well-developed peroneal process and a greater angle of the proximal articular surface relative to the long axis of the diaphysis. Although known Mt1s of fossil prosimians share these characters with living non-anthropoid primates, Mt1 morphology in the earliest crown group anthropoids is not well known. Here we describe two Mt1s from the Fayum Depression of Egypt - one from the latest Eocene (from the ∼34 Ma Quarry L-41), and one from the later early Oligocene (from the ∼29-30 Ma Quarry M) - and compare them with a sample of extant and fossil primate Mt1s. Multivariate analyses of Mt1 shape variables indicate that the Fayum specimens are most similar to those of crown group anthropoids, and likely belong to the stem catarrhines Catopithecus and Aegyptopithecus specifically, based on analyses of size. Also, phylogenetic analyses with 16 newly defined Mt1 characters support the hypotheses that “prosimian”-like Mt1 features evolved along the primate stem lineage, while crown anthropoid Mt1 morphology and function is derived among primates, and likely differed from that of basal stem anthropoids. The derived loss of powerful hallucal grasping as reflected in the Mt1 morphology of crown anthropoids may reflect long-term selection for improved navigation of large-diameter, more horizontal branches at the expense of movement in smaller, more variably inclined branches in the arboreal environment.     

Morphometry and allometry of the primate humerus

The primate distal humerus has been used both in phylogenetic reconstruction and in assessing locomotor and postural adaptations. This study uses an allometric approach to predict locomotor patterns of extant primates regardless of phylogenetic position. By showing the relationship between form and function in living primate taxa it will be possible to use this data set to predict locomotor behavior of extinct primates. Several linear measurements were taken from the distal humerus of 71 extant primate species (anthropoids and prosimians). Allometric regressions of each measurement were performed with mandibular M₂ area as a surrogate for body size. These measurements were used to determine if significant differences in distal humerus morphology exist among locomotor groups. The results were then used to test several hypotheses about the relationship between humeral form and function. For example, the hypothesis that suspensory primates have a large medial epicondyle is confirmed; the hypothesis that terrestrial quadrupeds have a deep olecranon fossa could not be confirmed with quantitative data. In addition to this hypothesis testing, the residuals from the allometric regressions of the humeral measurements were used in a discriminant functions analysis to estimate locomotor behavior from distal humerus morphology. The discriminant functions analysis correctly reclassified 64/71 (90%) species.     

Population genetics of Japanese monkeys: I. Estimation of the effective troop size

In order to estimate the genetically effective troop size of Japanese monkeys, we have to know the pattern of distribution of the numbers of gametes contributed by the individual members of the parental population to the next generation. The author inspected the observation records of macaque troops made by a number of socio-ecologists and found that the relationship between sexual rank and sexual activity of adult males could be approximately expressed by the law of geometrical series. Assuming that the genetic contribution of male parents to the next generation was proportional to their sexual activity and that the numbers of gametes contributed by the female parents formed thePoisson distribution, the author derived a formula for estimating effective troop size (N), namely, whereN _c was the census number andN _m andN _f the numbers of male and female parents, respectively, of the troop. Moreover, assumingN _m =0.2N _c andN _f =0.3N _c as an average, the effective size could be estimated as 36% or less of the census number.     

Interspecific perspective on mechanical and nonmechanical models of primate circumorbital morphology.

Linear dimensions and angular orientations of the browridge, postorbital bar, and postorbital septum were obtained from a representative series of primates and compared with variables associated with several nonmechanical and biomechanical/mechanical models put forward to explain the form and function of the circumorbital region. Analyses of the results indicate that face size is the primary determinant of variation in primate circumorbital morphology. Anteroposterior browridge thickness is correlated with neural-orbital disjunction among anthropoid primates, but not among prosimians. This difference appears related to differences in the construction of the upper face and anterior cranial fossa between prosimians and anthropoids. Little support is demonstrated for the anterior dental loading model of browridge development. Mediolateral postorbital bar width and (to a lesser degree) browridge height are correlated with neurofacial torsion during mastication and variation in masticatory muscle size. These analyses further suggest that since circumorbital structures (especially the browridges) are located the farthest away from the chewing apparatus, they are least affected by masticatory stresses.     

New early Eocene anaptomorphine primate (Omomyidae) from the Washakie Basin,Wyoming, with comments on the phylogeny and paleobiology of anaptomorphines

Recent paleontological collecting in the Washakie Basin, southcentral Wyoming, has resulted in the recovery of over 100 specimens of omomyid primates from the lower Eocene Wasatch Formation. Much of what is known about anaptomorphine omomyids is based upon work in the Bighorn and Wind River Basins of Wyoming. This new sample documents greater taxonomic diversity of omomyids during the early Eocene and contributes to our understanding of the phylogeny and adaptations of some of these earliest North American primates. A new middle Wasatchian (Lysitean) anaptomorphine, Anemorhysis savagei, n. sp., is structurally intermediate between Teilhardina americana and other species of Anemorhysis and may be a sister group of other Anemorhysis and Trogolemur. Body size estimates for Anemorhysis, Tetonoides, Trogolemur, and Teilhardina americana indicate that these animals were extremely small, probably less than 50 grams. Analysis of relative shearing potential of lower molars of these taxa indicates that some were primarily insectivorous, some primarily frugivorous, and some may have been more mixed feeders. Anaptomorphines did not develop the extremes of molar specialization for frugivory or insectivory seen in extant prosimians. Incisor enlargement does not appear to be associated with specialization in either fruits or insects but may have been an adaptation for specialized grooming or food manipulation. © 1994 Wiley-Liss, Inc.     

Paleobiology of the oligopithecines,the earliest known anthropoid primates

Anthropoid primates of the subfamily Oligopithecinae are late Eocene in age, and have a known distribution of Northeast Africa and the Arabian Peninsula. Body sizes of the three known oligopithecine species are estimated from allometric molar size regressions to be 700–1000 g forOligopithecus savagei, 600–900 g forCatopithecus browni, and 500 g for the least well-known and smallest species,Proteopithecus sylviae. Occlusal features of the molar teeth, considered in conjunction with body size, suggest that all three species were frugivorous and insectivorous. The orbital size ofCatopithecus indicates a diurnal activity cycle. A relatively broad interobital region in this species may indicate prosimian-like or callitrichid-like olfactory adaptations. Structural features of the crushed skull suggest thatCatopithecus had a smaller cranial capacity than those of extant anthropoids with a similar body size. Fossil plants and birds from localities yielding oligopithecines suggest a wet, warm, tropical, forested, swampy environment. These paleobiological inferences about the extinct oligopithecines are discussed in relation to questions about primate adaptations near the prosimian-anthropoid transition.     

Primate cranial diversity

Many studies in primate and human evolution focus on aspects of cranial morphology to address issues of systematics, phylogeny, and functional anatomy. However, broad analyses of cranial diversity within Primates as an Order are notably absent. In this study, we present a 3D geometric morphometric analysis of primate cranial morphology, providing a multivariate comparison of the major patterns of cranial shape change during primate evolution and quantitative assessments of cranial diversity among different clades. We digitized a set of 18 landmarks designed to capture overall cranial shape on male and female crania representing 66 genera of living primates. The landmark data were aligned using a Generalized Procrustes Analysis and then subjected to a principal components analysis to identify the major axes of cranial variation. Cranial diversity among clades was compared using multivariate measurements of variance. The first principal component axis reflects differences in cranial flexion, orbit size and orientation, and relative neurocranial volume. In general, it separates strepsirrhines from anthropoids. The second axis reflects differences in relative cranial height and snout length and primarily describes differences among anthropoids. Eulemur, Mandrillus, Pongo, and Homo are among the extremes in cranial shape. Anthropoids, catarrhines, and haplorhines show a higher variance than prosimians or strepsirrhines. Hominoids show the highest variance in cranial shape among extant primate clades, and much of this diversity is driven by the unique cranium of Homo sapiens. Am J Phys Anthropol 142:565–578, 2010. © 2010 Wiley‐Liss, Inc.     

The ecology of oligocene African anthropoidea

African anthropoids are first recorded in Early Oligocene deposits of the Fayum Province, Egypt. Six genera and nine species are recognized. Estimated body weights for these taxa are based on the regression equation log ₁₀(B) = 2.86log ₁₀(L) + 1.37, whereB is the bodyweight in grams, and Lis the M ₂ length in millimeters. The equation is derived from 106 species of living primates. Fayum species range in body weight from about 600 g (Apidium moustafai)to about 6000 g (Aegyptopithecus zeuxis).A similar range of body weight is found among extant Cebidae. The Fayum primates are larger than any extant insectivorous primates;this fact probably rules out a predominantly insectivorous diet. Extant frugivorous hominoids can be separated from folivorous hominoids on the basis of molar morphology. Folivorous apes (gorilla and siamang) have proportionately more shearing on their molars than do frugivorous species. Based on the hominoid analogy, the molar morphology of the Fayum species is consistent with a frugivorous diet. Parapithecus grangeristands apart from other Fayum species in having better developed molar shearing, possibly indicating that it had more fiber in its diet. Terrestrial species of Old World monkeys tend to have significantly higher molar crowns than do more arboreal species. This difference may relate to an increased amount of grit in the diet of the more terrestrial species, selecting for greater resistance to wear. Oligocene primates have molar crown heights consistent with a primarily arboreal mode of existence. However, the particularly high molar crowns of Parapithecus grangerisuggest that this species may have foraged on the ground to a considerable degree. Other evidence is advanced suggesting that Apidiummay have had a diurnal activity pattern.     

A volumetric comparison of the vestibular nuclei in primates

The volumes of each of the four vestibular nuclei, superior, lateral, medial and descending, were measured in 80 brains from 2 species of Scandentia, 18 species of prosimians, and 26 species of anthropoids. Size indices were calculated by comparing species-specific points to the nucleus volume-body weight allometry in prosimians, where the average prosimian was set at 1.00. The indices range from 1.78 in Saimiri to 0.48 in Gorilla, and the distributions by families overlap partially or completely. The observed trend in size indices is independent of changes in the neocortex and the ventral pons; average indices are 1.35 in New World monkeys, 1.20 in Old World monkeys, 0.74 in apes, 0.82 in man. Among prosimians, Galago, Galagoides and Tarsius (leaping locomotion) show significantly higher indices than Nycticebus, Loris and Perodicticus (slow movement without leaping). The lateral vestibular nuclear indices in Pongidae and man are extremely low, about half of those of the average prosimians. Correlation coefficients of size indices between the vestibular nuclei and other motor nuclei, such as the cerebellar nuclei, ventral pons and striatum, are analysed. The ratio of the vestibular nuclear volumes to the total brain volumes and the distribution of percentages of each vestibular nuclear volume to the total complex are also obtained.     

Home-Range Use and Activity Patterns of the Red Langur (Presbytis rubicunda) in Sabangau Tropical Peat-Swamp Forest, Central Kalimantan, Indonesian Borneo

Knowledge of a species’ ranging patterns is vital for understanding its behavioral ecology and vulnerability to extinction. Given the abundance and even distribution of leaves in forested habitats, folivorous primates generally spend less time feeding; more time resting; have shorter day ranges; and require smaller home ranges than frugivorous primates. To test the influence of frugivory on ranging behavior, we established the activity budget and home-range size and use in a highly frugivorous population of the Borneo-endemic colobine, Presbytis rubicunda, within Sabangau tropical peat-swamp forest, Central Kalimantan, and examined relationships between fruit availability and ranging patterns. We collected 6848 GPS locations and 10,702 instantaneous focal behavioral scans on a single group between January and December 2011. The group had the largest home-range size recorded in genus Presbytis (kernel density estimates: mean = 108.3 ± SD 3.8 ha, N = 4 bandwidths). The annual activity budget comprised 48 ± SD 4.0% resting; 29.3 ± SD 3.9% feeding, 14.2 ± SD 2.5% traveling, and 0.4 ± SD 0.4% social behaviors. Mean monthly day-range length was the highest recorded for any folivorous primate (1645 ± SD 220.5 m/d). No significant relationships existed between ranging variables and fruit availability, and ranging behaviors did not vary significantly across seasons, potentially owing to low fluctuations in fruit availability. Our results suggest that colobine monkeys maintain larger than average ranges when high-quality food resources are available. Their extensive range requirements imply that protecting large, contiguous tracts of habitat is crucial in future conservation planning for Presbytis rubicunda.     

Relationship of incisor size to diet and anterior tooth use in sympatric sumatran anthropoids

Researchers often relate anthropoid incisor size to diet and ingestive behaviors. It is suggested that primates that frequently consume large, tough foods (i.e., fruits) require large incisors to process these items. This idea has been difficult to test because of a lack of data on anterior tooth use in wild primates, and a lack of understanding concerning the relationships between food properties and ingestive behaviors. The first field study of primate ingestive behaviors has recently been completed for four species of Sumatran anthropoids: Hylobates lar, Macaca fascicularis, Pongo pygmaeus, and Presbytis thomasi [Ungar, American Journal of Physical Anthropology 95:197–219, 1994; International Journal of Primatology 16:221–245, 1995]. This paper documents both relative and absolute incisor row width differences among these taxa, and evaluates the relationships between incisor size and feeding behaviors for specific taxa. Results indicate that differences in incisor size among these species cannot all be explained by degree of frugivory, food item size, or even degree of incisor use in ingestion alone. It is therefore suggested that inferences of dietary differences based on largely or solely on differences in incisor sizes of specific fossil anthropoid taxa should be approached with caution. © 1996 Wiley-Liss, Inc.     

The fossil evidence of anthropoid brain evolution

The endocast of Aegyptopithecus, a 27 million year old ape, reveals that its brain was advanced over that of prosimians and comparable to that of modern anthropoids in relative size and in having expanded visual cortex, reduced olfactory bulbs, and a central sulcus separating primary somatic sensory and motor cortex. The early appearance of those features suggests that they may have been among the adaptations responsible for the evolution of anthropoids from prosimian ancestors. The frontal lobe was relatively smaller in Aegyptopithecus than in modern anthropoids. An endocast of Dolichocebus, one of the oldest known New World monkeys (25–30 million years old), reveals visual cortex expanded as in modern anthropoids. The 19 million year old Napak frontal bone displays a hominoid rather than cercopithecoid sulcal pattern. An 18 million year old endocast of the ape Dryopithecus (Proconsul) was neither monkey-like nor primitive, as originally described, but rather apelike and essentially modern in all observable features. The oldest undoubted Old World monkey endocast, from nine million year old Mesopithecus, reveals that the brain was modern in sulcal pattern and proportions. The sulcal pattern was like that of modern colobines, but that appears to be the more primitive condition, from which features characteristic of modern cercopithecine brains have evolved. The brain of six million year old Libypithecus was similar to that of Mesopithecus. A two million year old endocast of “Dolichopithecus” arvernensis displays a modern cercopithecine sulcal pattern.     

Time Constraints Limit Group Sizes and Distribution in Red and Black-and-White Colobus

Researchers have shown that, in frugivorous primates, a major constraint on group size is intra group feeding competition. The relationship is less obvious in folivorous primates. We investigated whether colobine group sizes are constrained by time limitations as a result of their low energy diet and ruminant-like digestive system. We used climate as an easy to obtain proxy for the productivity of a habitat. Using the relationships between climate, group size, and time budget components for populations of Colobus and Piliocolobus at different research sites, we created 2 taxon-specific models. In both genera, feeding time increased with group size or biomass. The models for Colobus and Piliocolobus correctly predicted the presence or absence of the genera at, respectively, 86% of 148 and 84% of 156 African primate sites. Median predicted group sizes where the respective genera were present are 19 for Colobus and 53 for Piliocolobus. We show that the differences between the 2 genera are due mainly to intrinsic differences in the way each taxon’s digestive physiology interacts with climatic variables to influence resting time requirements. The models may help us explore their responses to climatic change in both the past and the future.     

Frontal White Matter Volume Is Associated with Brain Enlargement and Higher Structural Connectivity in Anthropoid Primates

Previous research has indicated the importance of the frontal lobe and its ‘executive’ connections to other brain structures as crucial in explaining primate neocortical adaptations. However, a representative sample of volumetric measurements of frontal connective tissue (white matter) has not been available. In this study, we present new volumetric measurements of white and grey matter in the frontal and non-frontal neocortical lobes from 18 anthropoid species. We analyze this data in the context of existing theories of neocortex, frontal lobe and white versus grey matter hyperscaling. Results indicate that the ‘universal scaling law’ of neocortical white to grey matter applies separately for frontal and non-frontal lobes; that hyperscaling of both neocortex and frontal lobe to rest of brain is mainly due to frontal white matter; and that changes in frontal (but not non-frontal) white matter volume are associated with changes in rest of brain and basal ganglia, a group of subcortical nuclei functionally linked to ‘executive control’. Results suggest a central role for frontal white matter in explaining neocortex and frontal lobe hyperscaling, brain size variation and higher neural structural connectivity in anthropoids.     

Patterns of growth in primates

A model is developed which demonstrates the pattern of the relationship between growth rate. body weight, proportion of adult weight attained, and time taken to mature in animals. The relationships of growth rate and time taken to mature, to body weight in primates are examined in relation to this model. Within each of the taxonomic groups: prosimians, New World monkeys, Old World monkeys and great apes, growth rate quite closely parallels the three-quarter power of weight. After accounting for size, growth rate clearly decreases through this taxonomic list. Man has the slowest growth rate of all primates in relation to his size. The model predicts that, after accounting for differences in size, the daily energy intake during growth may, like growth rate, decrease considerably through the taxonomic groups from prosimians to man. The results form a basis from which to account for the differences due to size and taxonomic position when using monkeys as models for human physiology or disease during growth.