Primate Fossil Record Research Articles

Macaque fossils (Cercopithecidae: Papionini) from the Kumok Cave, Sungho County, North Hwanghae Province, the Democratic People's Republic of Korea

ABSTRACTThe recently discovered macaque fossils, including mandible, maxilla fragments and isolated teeth, from the Kumok Cave, Sungho County, the Democratic People's Republic of Korea can be identified as Macaca mulatta. They represent the first recognised occurrence of fossil M. mulatta in the Kumok Cave. The Kumok Cave sediments include seven layers, of which the macaque fossils were found only in the third layer. Thermoluminescence dating on a calcite sample from Layer 3 is about 86.1 ± 7.7 ka, and geochronology by the accompanying mammal fauna belongs to the Late Pleistocene, Thus, it indicates that Layer 3 was represented by a warm phase at the end of the pre‐Würm interglacial Epoch. The Kumok fossils also contribute to the growing primate fossil record in DPRK, and indicate the need for increased research into fossil primates in that country.

Liminal Light and Primate Evolution

The adaptive origins of primates and anthropoid primates are topics of enduring interest to biological anthropologists. A convention in these discussions is to treat the light environment as binary—night is dark, day is light—and to impute corresponding selective pressure on the visual systems and behaviors of primates. In consequence, debate has tended to focus on whether a given trait can be interpreted as evidence of nocturnal or diurnal behavior in the primate fossil record. Such classification elides the variability in light, or the ways that primates internalize light in their environments. Here, we explore the liminality of light by focusing on what it is, its many sources, and its flux under natural conditions. We conclude by focusing on the intensity and spectral properties of twilight, and we review the mounting evidence of its importance as a cue that determines the onset or offset of primate activities as well as the entrainment of circadian rhythms.

First record of a fossil monkey (Primates, Cercopithecidae) from the Late Pliocene of Serbia

The cercopithecid fossil record of the Balkan Peninsula extends from the Late Miocene to the Early Pleistocene, but to date no fossils of non-human primates have been identified in Serbia. Here we report the identification of two primate teeth from Ridjake, a rich paleontological site in western Serbia. NHMBEO 042501 is an upper third molar with heavy occlusal wear and taphonomic weathering. NHMBEO 042502 is a well-preserved lower third molar with only minor damage to the cusps and root apices. We performed an analysis of non-metric traits and made bivariate comparisons of crown linear measurements in order to assess the taxonomic affinity of the molars. Both show typical papionin occlusal patterns and relatively large overall sizes. In combination with the early Villafranchian (MN16) age of the site, we attribute both Ridjake primate fossils to cf. Paradolichopithecus sp. This represents the first identification of a non-human primate in Serbia, and the first identification of any primate in the Neogene period of Serbia. Along with recent hominin discoveries, the Ridjake fossils contribute to the growing primate fossil record in Serbia, and indicate the need for increased research into fossil primates in the country.

Functional morphology of the douc langur (Pygathrix spp.) scapula.

Most colobine monkeys primarily move through their arboreal environment quadrupedally. Douc langurs (Pygathrix spp.), however, are regularly observed to use suspensory behaviors at the Endangered Primate Rescue Center (EPRC) in Northern Vietnam. Previous work has linked variation in scapular morphology to different modes of primate arboreal locomotion. Here we investigate whether the shape of the Pygathrix scapula resembles obligate brachiators (gibbons) or obligate arboreal quadrupeds (other cercopithecoids). Using a MicroScribe G2X 3D digitizer, the positions of 17 landmarks were recorded on 15 different species of nonhuman primates (n = 100) from three categories of locomotor behavior: brachiator, arboreal quadruped, and unknown (Pygathrix). All analyses were conducted in the R package geomorph. A Procrustes analysis uniformly scaled the shape data and placed specimens into the same morphospace. A Principal Component Analysis was used to examine scapular shape and a Procrustes ANOVA was conducted to test for shape difference in the scapulae. A pairwise analysis was used to compare the means of the locomotor categories and identify any statistically significant differences. A phylogenetically controlled Procrustes ANOVA was also conducted using a phylogeny from 10kTrees. Results show Pygathrix scapular morphology is significantly different from both arboreal colobine quadrupeds (p < 0.01) and hylobatid brachiators (p < 0.01). It does, however, share some features with each including a long vertebral border, like other cercopithecoids, and a more laterally projecting acromion process, like the hylobatids. The principal difference segregating Pygathrix from both the arboreal quadrupeds and the brachiators is the more medially placed superior angle. These nuanced morphological characteristics associated with suspensory behaviors may be useful for inferring suspensory locomotion in the primate fossil record.

Scapular Morphology and Forelimb Use during Foraging in Four Sympatric Cercopithecids

Most investigations of primate scapular morphology use differences in locomotion to explain variation; less is known about how scapular geometry covaries with nonlocomotor behavior. We examined forelimb use during foraging in 4 cercopithecids ranging throughout the Ivory Coast's Tai Forest. During 5-min feeding bouts, we recorded the frequency individuals of Piliocolobus badius, Colobus polykomos, Cercocebus atys and Cercopithecus diana performed 5 forelimb behaviors involved in the acquisition and introduction of food to the oral cavity. Scapulae from these populations were examined to determine whether differences in forelimb use were reflected in features known to correspond with varying degrees of arm flexion, abduction and elevation. Our results reveal that the species differ markedly in forelimb use and that these differences are interpretable via their scapular morphology. For example, P. badius engages in more frequent flexion, abduction and elevation of the arm above the head relative to C. polykomos, and red colobus scapulae are longer craniocaudally and have larger, more cranially directed supraspinous fossae than those of closely related black-and-white colobus. Our attempt to explore how nonlocomotor behavior covaries with skeletal morphology should provide for more informed interpretations of the primate fossil record.

The relative correspondence of cranial and genetic distances in papionin taxa and the impact of allometric adjustments

The reconstruction of phylogenetic relationships in the primate fossil record is dependent upon a thorough understanding of the phylogenetic utility of craniodental characters. Here, we test three previously proposed hypotheses for the propensity of primate craniomandibular data to exhibit homoplasy, using a study design based on the relative congruence between cranial distance matrices and a consensus genetic distance matrix (“genetic congruence”) for papionin taxa: 1) matrices based on cranial regions subjected to less masticatory strain are more genetically congruent than high-strain cranial matrices; 2) matrices based on cranial regions developing earlier in ontogeny are more genetically congruent than matrices based on regions that develop later; and 3) matrices based on cranial regions with greater anatomical/functional complexity are more genetically congruent than matrices based on anatomically simpler regions.Morphological distance matrices based on the shape of 15 different cranial regions, delineated on the basis of previous catarrhine studies, were statistically compared to a matrix of known genetic distances in papionins. Since sexual dimorphism and allometry are known to characterize this clade, several analytical iterations were conducted: 1) mixed-sex, male-only, and female-only analyses and 2) with and without an allometric scaling adjustment. Across all datasets, the chondrocranium matrix was the most consistently correlated with genetic distances, which is also consistent with previous studies of cercopithecoid taxa; however, there was no support for the internal predictions of the three hypotheses tested. Allometric scaling corrections had the largest impact on the genetic congruence of facial shape matrices, a result consistent with previous studies that have described facial homoplasy in papionin taxa. These findings differ from patterns described for hominoid taxa, suggesting that no single predictive criterion can explain phylogenetic utility of cranial datasets across catarrhine primate taxa. Many of the differences in morphological-genetic matrix correlations could result from different levels of phenotypic integration and evolvability in cercopithecoids and hominoids, suggesting that further study of these phenomena in extant primates is warranted.

Eocene primates of South America and the African origins of New World monkeys.

The platyrrhine primates, or New World monkeys, are immigrant mammals whose fossil record comes from Tertiary and Quaternary sediments of South America and the Caribbean Greater Antilles. The time and place of platyrrhine origins are some of the most controversial issues in primate palaeontology, although an African Palaeogene ancestry has been presumed by most primatologists. Until now, the oldest fossil records of New World monkeys have come from Salla, Bolivia, and date to approximately 26million years ago, or the Late Oligocene epoch. Here we report the discovery of new primates from the ?Late Eocene epoch of Amazonian Peru, which extends the fossil record of primates in South America back approximately 10million years. The new specimens are important for understanding the origin and early evolution of modern platyrrhine primates because they bear little resemblance to any extinct or living South American primate, but they do bear striking resemblances to Eocene African anthropoids, and our phylogenetic analysis suggests a relationship with African taxa. The discovery of these new primates brings the first appearance datum of caviomorph rodents and primates in South America back into close correspondence, but raises new questions about the timing and means of arrival of these two mammalian groups.

The primate fossil record in the Iberian Peninsula

During the last decade, new discoveries in several Iberian basins, together with the description of previously unpublished finds, have significantly increased the recorded paleodiversity of fossil Primates (Mammalia: Euarchonta) in the Iberian Peninsula. Here we provide an updated compendium of the primate fossil record in Iberia during the Cenozoic and further summarize the changes in primate paleo­diversity through time, which are then analyzed in the light of changing climatic conditions. Thanks to favorable climatic conditions, the highest diversity of Iberian primates was reached during the Eocene, thus reflecting the radiation of both adapoids and omomyoids; only a single plesiadapiform genus is in contrast recorded in the Iberian Peninsula. Near the Eocene-Oligocene boundary, paleoclimatic changes led to a primate diversity crisis and other faunal changes, although two Iberian omomyoids survived the Grande Coupure. From the Middle Miocene onwards, catarrhine primates are recorded in the Iberian Peninsula. During the Middle and Late Miocene, they are represented by pliopithecoids and hominoids, restricted to NE Iberia. The Miocene hominoids from Iberia are of utmost significance for understanding the Eurasian hominoid radiation and its role in the origins of the great-ape-and-human clade. Following the local extinction of these taxa during the early Late Miocene, due to progressively increased seasonality and concomitant changes in plant communities, cercopithecoids are also recorded in the Iberian Peninsula from the latest Miocene through the Plio-Pleistocene, although they finally became locally extinct, whereas hominoids are again represented by fossil humans during the Pleistocene.

Primate phylogenetic relationships and divergence dates inferred from complete mitochondrial genomes

The origins and the divergence times of the most basal lineages within primates have been difficult to resolve mainly due to the incomplete sampling of early fossil taxa. The main source of contention is related to the discordance between molecular and fossil estimates: while there are no crown primate fossils older than 56Ma, most molecule-based estimates extend the origins of crown primates into the Cretaceous. Here we present a comprehensive mitogenomic study of primates. We assembled 87 mammalian mitochondrial genomes, including 62 primate species representing all the families of the order. We newly sequenced eleven mitochondrial genomes, including eight Old World monkeys and three strepsirrhines. Phylogenetic analyses support a strong topology, confirming the monophyly for all the major primate clades. In contrast to previous mitogenomic studies, the positions of tarsiers and colugos relative to strepsirrhines and anthropoids are well resolved. In order to improve our understanding of how fossil calibrations affect age estimates within primates, we explore the effect of seventeen fossil calibrations across primates and other mammalian groups and we select a subset of calibrations to date our mitogenomic tree. The divergence date estimates of the Strepsirrhine/Haplorhine split support an origin of crown primates in the Late Cretaceous, at around 74Ma. This result supports a short-fuse model of primate origins, whereby relatively little time passed between the origin of the order and the diversification of its major clades. It also suggests that the early primate fossil record is likely poorly sampled.

Species in the primate fossil record

Species in the fossil record are population pools of genetic and phenetic variation at a place and time, morphologically recognizable and distinguishable from others by empirical standards. Change through time can be substantial, requiring subdivision of lineages that becomes more arbitrary as they become more complete. Evolution is about form, space, and time; it is about variation and change. Interpretation of species in the fossil record touches all of these.

Morphological variation of genetically confirmedAlouatta Pigra×A. palliatahybrids from a natural hybrid zone in Tabasco, Mexico

While hybridization has been reported for a large number of primate taxa, there is a general lack of data on hybrid morphology for wild individuals with known genetic ancestry. A confirmed hybrid zone for the closely related Neotropical primates Alouatta palliata and A. pigra has provided a unique opportunity to study primate hybrid morphological variation. Here we used molecular evidence based on mitochondrial, Y-chromosome, and autosomal data to assess hybrid ancestry. We conducted univariate and multivariate statistical comparisons of morphometric data collected from individuals both outside and within the hybrid zone in Tabasco, Mexico. Our results show that of all the hybrids detected (N = 128), only 12% of them were approximately genetically intermediate, and none of them were first generation hybrids. Univariate pairwise comparisons among parental individuals, multigenerational backcrossed hybrids, and intermediate hybrids showed that overall, multigenerational backcrossed hybrids resemble the parental species with which they share most of their alleles. Conversely, intermediates were highly variable. Similarly, principal component analysis depicts an overlap between the parental species and their backcrosses when considering overall morphological differences. Finally, discriminant function analysis of the morphological variables was overall unreliable for classifying individuals into their assigned genotypic classes. Taken together, our results suggest that primate natural hybridization studies should incorporate molecular methods for determining ancestry, because morphology may not always be a reliable indicator of hybrid status. Hybrid zones could comprise a large number of multigenerational backcrossed hybrids that are indistinguishable from the parental species. The implications for studying hybridization in the primate fossil record are discussed.

The Developmental Origins of Mosaic Evolution in the Primate Limb Skeleton

The central hypothesis of this paper is that basic properties of vertebrate limb development bias the generation of phenotypic variation in certain directions, and that these biases establish focal units, or regions, of evolutionary change within the primate hand and foot. These focal units include (1) a preaxial domain (digit I, hallux or pollex, metapodial and proximal phalanx), (2) a postaxial domain (metapodials and phalanges of digits II–V), and (3) a digit tip domain (terminal phalanges and nails/claws of rays I–V). The existence of these focal units therefore provides a mechanistic basis for mosaic evolution within the hand and foot, and can be applied to make specific predictions about which features of the limb skeleton are most likely to be altered in primate adaptive radiations over time. Examination of the early primate fossil record provides support for this model, and suggests that the existence of variational tendencies in limb development has played a major role in guiding the origin and evolution of primate skeletal form.

Functional morphology of cercopithecoid primate metacarpals

The primate fossil record suggests that terrestriality was more common in the past than it is today, particularly among cercopithecoid primates. Whether or not a fossil primate habitually preferred terrestrial substrates has typically been inferred from its forelimb anatomy. Because extant large-bodied terrestrial cercopithecine monkeys utilize digitigrade hand postures during locomotion, being able to identify if a fossil primate habitually adopted digitigrade postures would be particularly revealing of terrestriality in this group. This paper examines the functional morphology of metacarpals in order to identify osteological correlates of digitigrade versus palmigrade hand postures. Linear measurements were obtained from 324 individuals belonging to digitigrade and palmigrade cercopithecoid species and comparisons were made between hand posture groups. Digitigrade taxa have shorter metacarpals, relative to both body mass and humerus length, than palmigrade taxa. Also, digitigrade taxa tend to have metacarpals with smaller dorsoventral diameters, relative to the product of body mass and metacarpal length, compared to palmigrade taxa. The size and shape of the metacarpal heads do not significantly differ between hand posture groups. Multivariate analyses suggest that metacarpal shape can only weakly discriminate between hand posture groups. In general, while there are some morphological differences in the metacarpals between hand posture groups, similarities also exist that are likely related to the fact that even digitigrade cercopithecoids can adopt palmigrade hand postures in different situations (e.g., terrestrial running, arboreal locomotion), and/or that the functional demands of different hand postures are not reflected in all aspects of metacarpal morphology. Therefore, the lack of identifiable adaptations for specific hand postures in extant cercopithecoids makes it difficult to determine a preference for specific habitats from fossil primate hand bones.

On the genetic architecture of cortical folding and brain volume in primates

Understanding the evolutionary forces that produced the human brain is a central problem in neuroscience and human biology. Comparisons across primate species show that both brain volume and gyrification (the degree of folding in the cerebral cortex) have progressively increased during primate evolution and there is a strong positive correlation between these two traits across primate species. The human brain is exceptional among primates in both total volume and gyrification, and therefore understanding the genetic mechanisms influencing variation in these traits will improve our understanding of a landmark feature of our species. Here we show that individual variation in gyrification is significantly heritable in both humans and an Old World monkey (baboons, Papio hamadryas). Furthermore, contrary to expectations based on the positive phenotypic correlation across species, the genetic correlation between cerebral volume and gyrification within both humans and baboons is estimated as negative. These results suggest that the positive relationship between cerebral volume and cortical folding across species cannot be explained by one set of selective pressures or genetic changes. Our data suggest that one set of selective pressures favored the progressive increase in brain volume documented in the primate fossil record, and that a second independent selective process, possibly related to parturition and neonatal brain size, may have favored brains with progressively greater cortical folding. Without a second separate selective pressure, natural selection favoring increased brain volume would be expected to produce less folded, more lissencephalic brains. These results provide initial evidence for the heritability of gyrification, and possibly a new perspective on the evolutionary mechanisms underlying long-term changes in the nonhuman primate and human brain.

Ecological correlates of infraorbital foramen area in primates

The infraorbital foramen (IOF) transmits the infraorbital nerve (ION) to specialized sensory cells (mechanoreceptors) in the maxillary region. The size of the IOF has been used in numerous paleoecological interpretations of the fossil record. However, these interpretations have been applied without an explicit analysis of the relationship between ecological variables and the IOF. ION and IOF cross-sectional area show a strong positive correlation. As a result, IOF area can be a proxy for ION area, and it is hypothesized that IOF area may be a good measure for maxillary somatosensory acuity. Differences in diet, substrate preference, and/or activity pattern have been shown to correlate with differences in maxillary somatosensory acuity among mammals. This study examines how IOF area covaries with different ecological variables. IOF area was measured for 89 primate species. Ecological profiles were also created for each species and used to evaluate interspecific variation in relative IOF area within each ecological category. The results show a significant relationship between relative IOF area and diet, but not substrate preference or activity pattern. Frugivores have significantly larger relative IOFs than either folivores or insectivores, but the relative IOFs of folivores and insectivores do not differ significantly from one another. These results partially support the hypothesis that maxillary mechanoreception is a critical sensory cue for primates within a feeding context. Results for this study suggest the IOF can be used as an informative character in some paleoecological interpretations of the primate fossil record.

Estimating primate divergence times by using conditioned birth-and-death processes

The fossil record provides a lower bound on the primate divergence time of 54.8 million years ago, but does not provide an explicit estimate for the divergence time itself. We show how the pattern of diversification through the Cenozoic can be combined with a model for speciation to give a distribution for the age of the primates. The primate fossil record, the number of extant primate species, and information about the structure of the primate phylogenetic tree are combined to provide an estimate for the joint distribution of the primate and anthropoid divergence times. To take this information into account, we derive the structure of the birth-and-death process conditioned to have a subtree originate at a particular point in time. This process has a size-biased law and has an immortal line running from the root of the tree to the root of the subtree, with species on the spine having modified offspring and length distributions. We conclude that it is not possible, with this model, to rule out a Cretaceous origin for the primates.

Identification of a single birth cohort in Kenyapithecus kizili and the nature of sympatry between K. kizili and Griphopithecus alpani at Paşalar

The sample of the less common hominoid species at Paşalar, Kenyapithecus kizili, is characterized by a number of unusual attributes. All ten of the upper central incisors attributed to this species show a distinct, identical pattern of two linear enamel hypoplasias. The two hypoplasias occur on the same portion of the labial crown face, revealing that the two hypoplasia-causing events occurred at the same stage of development in all individuals. The morphology of the two hypoplasias and the amount of time between them, as determined by both their separation and counts of perikymata, are also the same on all teeth. In addition, all of the approximately 70 teeth assigned to K. kizili appear to come from young adults based on degrees of wear; there are no younger or older individuals (diagnostic morphology at most tooth positions would be evident even with heavy wear). Thus, all of the K. kizili individuals (minimum number of individuals is nine: seven males, two females) appear to have died at essentially the same age. It is concluded that the most plausible interpretation of all these features is that the incisor hypoplasias were caused by the same two events in all the K. kizili individuals and that these individuals therefore represent a single birth cohort. As such, and because they died at essentially the same age, they would also have died at the same time, which is consistent with the catastrophic nature of the Paşalar deposits. The number of coincidences needed to explain all of the attributes of the K. kizili sample if these animals were born in, and died in, different years seems highly improbable. Moreover, the lack of a typical age-class structure for the K. kizili sample, or any age-class structure at all beyond the one age class of young adult, strongly suggests that the species was not resident in the area that contributed to the Paşalar accumulation, and that K. kizili was not permanently sympatric with the other Paşalar hominoid, Griphopithecus alpani. Rather, the nine K. kizili individuals must have been transients in, or recent immigrants to, the area at the time of the events that led to the formation of the site. Recent observations on social associations in male chimpanzees offer at least a possible interpretive framework to explain this unprecedented occurrence in the primate fossil record.

Using extant patterns of dental variation to identify species in the primate fossil record: a case study of middle Eocene Omomys from the Bridger Basin, southwestern Wyoming

Patterns of extant primate dental variation provide important data for interpreting taxonomic boundaries in fossil forms. Here I use dental data from several well-known living primates (as well as data from selected Eocene forms) to evaluate dental variation in Middle Eocene Omomys, the first North American fossil primate identified by paleontologists. Measurements were collected from a sample of 148 omomyid dental specimens recovered from Bridger B localities in the Bridger Basin, Wyoming. Most of these specimens have not previously been described. Nonmetric traits were also scored for this sample. Lower molar coefficients of variation range from 4.01 for M2 length (n = 80) to 6.73 for M3 talonid width (n = 57). All of the nonmetric traits scored exhibit less than 100% presence in the overall sample, including traits previously described as representative of Omomys (e.g., P4 metaconids present in 91%, n = 55; M2 pericones present in 80%, n = 15). Dental traits also vary in a set of spatially restricted localities from the same fossil horizon and in a separate, single fossil locality (DMNH 868, P4 metaconids present in 67%, n = 6). An increasing frequency in several premolar traits across time in these more restricted samples suggests an anagenetic change in Bridger B Omomys. However, this degree of morphological variability is consistent with that seen in extant primate species from single locations. Metric variation in this sample is comparable to that seen in other Eocene primates, such as new data presented here for the omomyid Arapahovius gazini from the Washakie Basin, southern Wyoming. Omomys metric variation is also comparable to that found in several samples of well-known extant primates from single localities (e.g., ring-tailed lemurs and gray-brown mouse lemurs). These metric data also correspond to the patterns of variability described in previously published studies of Omomyscarteri. In sum, a single species interpretation (O. carteri) for this new Bridger B Omomys sample from southern Wyoming is affirmed, and this study illustrates the usefulness of dental data from extant primates for evaluating primate fossil samples.

Fossils, Hunters, and Controversies: Exploring Primate Evolution

The study of primate evolution opens a fascinating window onto the varied adaptations, behaviors, and origins of our closest relatives and therefore ourselves. Four books reviewed give different perspectives on the primate fossil record and cover diverse time periods, from the Eocene to the Pleistocene. Four major themes are explored in this article: defining “primatehood” and classifying primates, comparative approaches, reconstructing behavior and ecology, and the importance of non-fossil data. Together, the books show that the study of ancient and modern primates is rooted firmly in anthropology, sharing with other sub-disciplines fundamental aims like classification and relying on a comparative approach.

Christopher Beard: The Hunt for the Dawn Monkey. Unearthing the Origins of Monkeys, Apes and Humans

It is definitely time for a popular book on primate evolution that does not view everything through the myopic lens of human origins. Anthropoid origins is the ideal focus for such a book, necessitating as it does a discussion of everything from the omomyiforms of Asia to the anthropoids of North Africa. Beard does a nice job of reviewing the Eocene primate fossil record, and the book is a very readable but fairly detailed treatment of the issues surrounding the origins and relationships of primate higher taxa. The chapters begin with entertaining fieldwork vignettes or introductions of important historical figures in primate paleontology, before diving into readable, but in depth accounts of the fossil record of primate evolution. Accounts of adapiforms, omomyiforms, and the Fayum anthropoids precede Beard’s presentation of his case for tarsier affinities for Shoshonius and anthropoid affinities for Eosimias. His review of the competing hypotheses regarding anthropoid relationships is a tidy summary that will be useful for those wanting to familiarize themselves with the history of the literature. In contrast, Beard’s treatment of explanations for anthropoid origins is scant, limited to Cachel’s theory, which is supported by no one whom I can recall. More detailed explanations, such as Cartmill’s, or mine, are not presented, either because Beard does not agree with them, or he is less interested in explanations than with patterns. The book also includes entertaining and accurate descriptions of some of the major players and events in the anthropoid origins debate. Beard’s account of his first presentation of Eosimias at the Anthropoid Origins Conference and Duke University in 1992 replays my memory of events nicely, and description of Elwyn Simons is right on the button. These accounts add color to the story. Int J Primatol (2007) 28:1195–1196 DOI 10.1007/s10764-007-9212-y