Catarrhine Species Research Articles

An Evolutionarily Conserved Sexual Signature in the Primate Brain

The question of a potential biological sexual signature in the human brain is a heavily disputed subject. In order to provide further insight into this issue, we used an evolutionary approach to identify genes with sex differences in brain expression level among primates. We reasoned that expression patterns important to uphold key male and female characteristics may be conserved during evolution. We selected cortex for our studies because this specific brain region is responsible for many higher behavioral functions. We compared gene expression profiles in the occipital cortex of male and female humans (Homo sapiens, a great ape) and cynomolgus macaques (Macaca fascicularis, an old world monkey), two catarrhine species that show abundant morphological sexual dimorphism, as well as in common marmosets (Callithrix Jacchus, a new world monkey) which are relatively sexually monomorphic. We identified hundreds of genes with sex-biased expression patterns in humans and macaques, while fewer than ten were differentially expressed between the sexes in marmosets. In primates, a general rule is that many of the morphological and behavioral sexual dimorphisms seen in polygamous species, such as macaques, are typically less pronounced in monogamous species such as the marmosets. Our observations suggest that this correlation may also be reflected in the extent of sex-biased gene expression in the brain. We identified 85 genes with common sex-biased expression, in both human and macaque and 2 genes, X inactivation-specific transcript (XIST) and Heat shock factor binding protein 1 (HSBP1), that were consistently sex-biased in the female direction in human, macaque, and marmoset. These observations imply a conserved signature of sexual gene expression dimorphism in cortex of primates. Further, we found that the coding region of female-biased genes is more evolutionarily constrained compared to the coding region of both male-biased and non sex-biased brain expressed genes. We found genes with conserved sexual gene expression dimorphism in the occipital cortex of humans, cynomolgus macaques, and common marmosets. Genes within sexual expression profiles may underlie important functional differences between the sexes, with possible importance during primate evolution.

A remarkable female cranium of the early Oligocene anthropoid Aegyptopithecus zeuxis (Catarrhini, Propliopithecidae)

The most complete and best-preserved cranium of a Paleogene anthropoid ever found, that of a small female of the early Oligocene ( approximately 29-30 Ma) stem catarrhine species Aegyptopithecus zeuxis, was recovered from the Jebel Qatrani Formation (Fayum Depression, Egypt) in 2004. The specimen is that of a subadult and, in craniodental dimensions, is the smallest Aegyptopithecus individual known. High-resolution computed tomographic (microCT) scanning of the specimen's well preserved cranial vault confirms that Aegyptopithecus had relatively unexpanded frontal lobes and a brain-to-body mass ratio lower than those of living anthropoids. MicroCT scans of a male cranium recovered in 1966 [Egyptian Geological Museum, Cairo (CGM) 40237] reveal that previous estimates of its endocranial volume were too large. Thus, some amount of encephalization evolved independently in platyrrhine and catarrhine anthropoids, and the relative brain size of the last common ancestor of crown Anthropoidea was probably strepsirrhine-like or smaller. A. zeuxis shows extreme sexual dimorphism in craniodental morphology (apparently to a degree otherwise seen only in some highly dimorphic Miocene catarrhines), and the crania of female Aegyptopithecus lack a number of morphological features seen in larger males that have been accorded phylogenetic significance in catarrhine systematics (e.g., a well developed rostrum, elongate sagittal crest, and frontal trigon). Although a unique pattern of craniofacial sexual dimorphism may have characterized advanced stem and basal crown catarrhines, expression of various allegedly "discrete" craniofacial features may have been intraspecifically variable in early catarrhine species due to high levels of dimorphism and so should be treated with caution in phylogenetic analyses.

Correlation of cranial and mandibular prognathism in extant and fossil hominids

This pilot study investigates the correlation between mandibular symphysial orientation and both craniofacial and subnasal prognathism in modern humans, chimpanzees, gorillas, and a range of other catarrhine species. The purpose was to assess the potential value of using the degree of prognathism as a parameter that might relate isolated crania and mandibles in the Plio-Pleistocene hominin fossil record of Africa. It is found that angles expressing cranial and mandibular prognathism are intraspecifically correlated in modern humans from pre-industralised populations, but not in the African apes, or interspecifically among catarrhine species. Hominin fossils investigated in this comparative context broadly follow the pattern of correlation shown by modern humans, with some potentially interesting differences that warrant further investigation. In all, the results suggest that the degree of prognathism has little practical value in determining associations between isolated hominin mandibles and crania.

Olfactory fossa of Tremacebus harringtoni (platyrrhini, early Miocene, Sacanana, Argentina): implications for activity pattern.

CT imaging was undertaken on the skull of approximately 20-Myr-old Miocene Tremacebus harringtoni. Here we report our observations on the relative size of the olfactory fossa and its implications for the behavior of Tremacebus. The endocranial surface of Tremacebus is incomplete, making precise estimate of brain size and olfactory fossa size imprecise. However, olfactory fossa breadth and maximum endocranial breadth measured from CT images of one catarrhine species and eight platyrrhine species for which volumes of the olfactory bulb and brain are known show that the osteological proxies give a reasonably accurate indication of relative olfactory bulb size. Nocturnal Aotus has the largest relative olfactory fossa breadth and the largest olfactory bulb volume compared to brain volume among extant anthropoids. Tremacebus had a much smaller olfactory fossa breadth and, by inference, bulb volume--within the range of our sample of diurnal anthropoids. Variations in the relative size of the olfactory bulbs in platyrrhines appear to relate to the importance of olfaction in daily behaviors. Aotus has the largest olfactory bulbs among platyrrhines and relies more on olfactory cues when foraging than Cebus, Callicebus, or Saguinus. As in other examples of nocturnal versus diurnal primates, nocturnality may have been the environmental factor that selected for this difference in Aotus, although communication and other behaviors are also likely to select for olfactory variation in diurnal anthropoids. Considering the olfactory fossa size of Tremacebus, olfactory ability of this Miocene monkey was probably not as sensitive as in Aotus and counts against the hypothesis that Tremacebus was nocturnal. This finding accords well with previous observations that the orbits of Tremacebus are not as large as nocturnal Aotus.

Cortical Orofacial Motor Representation in Old World Monkeys, Great Apes, and Humans

This study presents a comparative stereologic investigation of neurofilament protein- and calcium-binding protein-immunoreactive neurons within the region of orofacial representation of primary motor cortex (Brodmann’s area 4) in several catarrhine primate species (Macaca fascicularis, Papio anubis, Pongo pygmaeus, Gorilla gorilla, Pan troglodytes, and Homo sapiens). Results showed that the density of interneurons involved in vertical interlaminar processing (i.e., calbindin- and calretinin-immunoreactive neurons) as well pyramidal neurons that supply heavily-myelinated projections (i.e., neurofilament protein-immunoreactive neurons) are correlated with overall neuronal density, whereas interneurons making transcolumnar connections (i.e., parvalbumin-immunoreactive neurons) do not exhibit such a relationship. These results suggest that differential scaling rules apply to different neuronal subtypes depending on their functional role in cortical circuitry. For example, cortical columns across catarrhine species appear to involve a similar conserved network of intracolumnar inhibitory interconnections, as represented by the distribution of calbindin- and calretinin-immunoreactive neurons. The subpopulation of horizontally-oriented wide-arbor interneurons, on the other hand, increases in density relative to other interneuron subpopulations in large brains. Due to these scaling trends, the region of orofacial representation of primary motor cortex in great apes and humans is characterized by a greater proportion of neurons enriched in neurofilament protein and parvalbumin compared to the Old World monkeys examined. These modifications might contribute to the voluntary dexterous control of orofacial muscles in great ape and human communication.

New Catarrhine fossils from Moroto II, Early Middle Miocene (ca 17.5 Ma) Uganda

During the 1998–2003 field seasons of the Uganda Palaeontology Expedition, dental remains of three catarrhine species were recovered from Moroto II, Uganda. Micromammals from the locality indicate a late Early Miocene to basal Middle Miocene (ca 17.5–17 Ma) age, younger than Rusinga (17.8 Ma), but similar in age to Buluk (17.2 Ma) and Kalodirr (17.2 Ma). This paper describes and interprets new catarrhines from the site, one of which is a victoriapithecid monkey, the second a new genus and species of small-bodied ape, and the third a large hominoid. A fourth species collected in the 1960's is attibuted to Afropithecus turkanensis. To cite this article: M. Pickford et al., C. R. Palevol 2 (2003).

Species richness, species range size and ecological specialisation among African primates: geographical patterns and conservation implications

The geographical distribution of species richness and species range size of African anthropoid primates (catarrhines) is investigated and related to patterns of habitat and dietary niche breadth. Catarrhine species richness is concentrated in the equatorial regions of central and west Africa; areas that are also characterised by low average species range sizes and increased ecological specificity. Species richness declines with increasing latitude north and south of the equator, while average species range size, habitat and dietary breadth increase. Relationships between species richness, species range size and niche breadth remain once latitudinal and longitudinal effects have been removed. Among areas of lowest species richness, however, there is increased variation in terms of average species range size and niche breadth, and two trends are identified. While most such areas are occupied by a few wide-ranging generalists, others are occupied by range-restricted specialist species. That conservation efforts increasingly focus on regions of high species richness may be appropriate if these regions are also characterised by species that are more restricted in both their range size and their ecological versatility, although special consideration may be required for some areas of low species richness.

Nails and claws in primate evolution

The issue of whether nails or claws were present on the digits of the last common ancestor of living primates is central to the understanding of the ecological context in which the order originated. Two lines of evidence are available, the shape (claw, nail, toilet-claw) and the histological structure (one or two horny strata). Here we review the existing data regarding the shape and histological structure of cheirideal appendages in primates and present new information from a wide range of living primates. We demonstrate the presence of a typical toilet-claw inDaubentonia madagascariensisand discuss its consequences, since the alleged lack of such structures in this species has long obscured the issue. The general view that primate nails, with the exception of those in New World primates, consist of only one layer is disproved by the presence of two distinct strata in the nails of the feet of three out of seven catarrhine species examined, as well as inLemur catta. The combined new and old data indicate that the last common ancestor of the extant primates had lost the typical mammalian claws of its ancestors and developed nails on all pedal digits except digit II, which bore a toilet-claw. All nails as well as the toilet-claw originally consisted of two layers. We present a new hypothesis regarding the adaptational significance of these changes.

Competition, coalitions and canine size in primates

Explanations of the evolution of canine tooth size sexual dimorphism in primates implicitly assume that male canine size is the primary target of natural or sexual selection, even though there is substantial unexplained variation in female canine size. Here we demonstrate that the canines of both males and females are relatively larger in species where agonistic interactions are more likely to escalate. Hence, the canine teeth of both sexes are influenced by selection for the development of weaponry, though the nature of the selection (natural or sexual) favoring development of the canines as weapons depends on the objects of competition (mates vs. food, for example). However, we also suggest that where the outcome of fights is typically determined between coalitions of individuals, selection for weaponry is reduced, even though agonistic competition can be very intense. Coalitionary aggression between males occurs in only a handful of anthropoid primates, but it is common among female anthropoids, and helps explain, in part, the extreme sexual dimorphism in the canine teeth of a number of catarrhine species. This is the first demonstration that cooperation among animals may affect their morphology. The lack of sexual dimorphism in canine size among prosimian primates is also consistent with the model. This analysis demonstrates that a better understanding of the interspecific variation in sexual dimorphism among primates is gained by considering behavioral variation in both sexes.

On the sense of taste in two Malagasy Primates (Microcebus murinus and Eulemur mongoz)

The relationship between phylogeny and taste is of growing interest. In this study we present recordings from the chorda tympani proper (CT) nerve of two lemuriforme primates, the lesser mouse lemur (Microcebus murinus) and the mongoose lemur (Eulemur mongoz), to an array of taste stimuli which included the sweeteners acesulfame-K, alitame, aspartame, D-glucose, dulcin, monellin, neohesperidin dihydrochalcone (NHDHC), saccharin, sodium superaspartame, stevioside, sucralose (TGS), sucrose, suosan, thaumatin and xylitol, as well as the non–sweet stimuli NaC1, citric acid, tannin and quinine hydrochloride. In M.murinus the effects of the taste modifiers gymnemic acid and miraculin on the CT response were recorded. Conditioned taste aversion (CTA) experiments in M.murinus and two-bottle preference (TBP) tests in E.mongoz were also conducted. We found that all of the above tastants except thaumatin elicited a CT response in both species. The CTA technique showed that M.murinus generalized from sucrose to monellin but not to thaumatin. The intake of aspartame, ranging in concentration from 0.1 to 30 mM was measured in E.mongoz with TBP tests. At no concentration did we see a preference, but there was a significant rejection of 10 and 30 mM aspartame (P←0.025). Miraculin had no effects on the CT response to acids, and gymnemic acid did not selectively suppress the CT response to sucrose or that of any other sweeteners. The absence of ability to taste thaumatin in these species supports the dichotomy between catarrhine and non-catarrhine species. The difference in results with thaumatin and monellin indicate that their sweet moieties are not identical. It also points to a phylogenetic difference in taste within the prosimian group. Further, the results with aspartame indicate that the perception of sweetness from aspartame is limited to catarrhine species. Finally, neither miraculin nor gymnemic acid exhibit the same taste modifying effects in lemuriformes as they do in hominoidea. Thus the results with gymnemic acid and miraculin corroborate those obtained earlier in other prosimians.

Tandemly duplicated alpha globin genes of gibbon.

The alpha globin gene locus of the common gibbon (Hylobates lar) was isolated, and it contains two closely linked alpha globin genes that share the same arrangement as that found for the homologous genes of other catarrhine primates. The nucleotide sequences of the gibbon alpha globin genes were determined and compared with the alpha globin gene sequences from other primate species (human, chimpanzee, orangutan, baboon, and rhesus); the prosimian primate, galago, alpha A and alpha B globin genes provided the out-group for this analysis. The degree of divergence for both synonymous and nonsynonymous substitutions among the alpha globin genes are generally smaller for intraspecies than interspecies comparisons, which is indicative of concerted evolution between the paired alpha globin genes of each catarrhine species. The pattern of differences is suggestive of gene conversions. This possibility is supported by both site-by-site and branch-swapping parsimony analyses. The site-by-site parsimony analysis was also used to determine the 3' boundary of each catarrhine species-specific conversion. These alpha globin gene conversion events encompass most of the transcriptional region, including the promoter, exons, introns, and about one-half of the 3'-untranslated region. However, the paired gibbon alpha globin genes show the highest degree of divergence, differing by five nucleotides in their coding regions, three of which encode amino acid replacement substitutions. It appears that the last convergence event between the paired gibbon alpha globin genes is relatively ancient, having occurred approximately 11 million years ago. The remaining 3'-untranslated region and flanking DNAs show no evidence of involvement in any recent conversion event as the parsimony analysis of these sequences group all the alpha 1 globin genes of the different catarrhine species into one clade and all the alpha 2 globin gene of these species into a separate clade. The sequence comparison among the alpha globin genes of different primate species also provides interesting implications regarding the evolution and functional domains of the 3'-untranslated regions.

Phylogenetic relationships and rates of evolution in primates: Allozymic data from catarrhine and platyrrhine species

The genetic electrophoretic variation at up to 43 protein loci was studied in four hominoid, three cercopithecoid, and three ceboid species. Phylogenetic reconstructions based on genetic distances show that the two chimpanzee species are closest to humans, while the gorilla diverged earlier than the split between humans and the chimpanzee. Within the cercopithecoids the green monkey apparently diverged earlier than the macaques, and within the ceboids, the owl monkey is only distantly related to the capuchin and squirrel monkeys. The hypothesis that rates of evolution at the level of protein electrophoretic variation are equal both among the groups, as well as within each group, could not be rejected.

The ontogeny of sexual dimorphism in the cranium of Bornean orang-utans (Pongo pygmaeus pygmaeus): 1. Univariate analysis

Based on a homogeneous sample of 212 individuals spanning all postnatal age periods, we examine the ontogeny of cranial sexual dimorphism in Bornean orang-utans (Pongo pygmaeus pygmaeus) by means of univariate statistics. A distinct pattern emerges at the early juvenile stage and continues at all subsequent stages with males tending to exceed females in all cranial dimensions. In conjunction, starting at mid-juvenile stage, there is a strong tendency for an increase in number and strength of significant cranial sex differences, all of them in favor of males. Significant sex differences in the viscerocranium, reflecting stronger prognathism in males, emerge prior to those in the neurocranium. The total ontogenetic pattern of cranial sexual dimorphism in orang-utans is remarkably similar to that of gorillas, except that there is no evidence of a sex difference in timing of the adolescent growth spurt in the orang-utan. As for other catarrhine species (Wood 1976), male variance of cranial dimensions tends to be greater than that of females, thus lending support to Leutenegger & Cheverud's (1982, 1985) model on the evolution of character dimorphism by means of variance dimorphism.

New primate fossils from the Middle Miocene of Maboko Island, Kenya

Understanding the biogeography and evolution of Miocene catarrhines relies on accurate specimen provenience. It has long been speculated that some catarrhine specimens among the early collections from Miocene sites in Kenya have incorrect provenience data. The provenience of one of these, the holotype of Equatorius africanus (NHM M16649), was previously revised based on x-ray fluorescence spectroscopy. Here we use nondestructive portable x-ray fluorescence spectroscopy to test the provenience of additional catarrhine specimens that, based on morphology and/or incomplete provenience information, were identified as possibly having been collected at a different site from that recorded at museum accession. We test the hypotheses that two specimens purportedly from the Early Miocene site of Rusinga (KNM-RU 1681 and KNM-RU 1999) are instead from Maboko, three specimens purportedly from the Middle Miocene site of Fort Ternan (KNM-FT 8, KNM-FT 41, and KNM-FT 3318) are instead from Songhor, and one specimen accessioned as being from Songhor (KNM-SO 5352) is from that site. Elemental data reveal that two of the specimens (KNM-FT 3318 and KNM-RU 1681) are likely to have been collected at sites other than their museum-accessioned provenience, while two others (KNM-RU 1999, and KNM-FT 41) were confirmed to have correct provenience. Results for both KNM-FT 8 and KNM-SO 5352, while somewhat equivocal, are best interpreted as supporting their accessioned provenience. Our results have implications for the distribution of certain catarrhine species during the Miocene in Kenya. Confirmation of the provenience of the specimens also facilitates taxonomic attribution, and resulted in additions to the morphological characterizations of some species. The protocol presented here has potential for wider application to assessing questions of provenience for fossils from other locations and periods.

Variation in rates of activity and inhibition of serum cholinesterase among anthropoid primates

Cholinesterase activity in the plasma of five hominoid and five cercopithecoid species was measured and characterized by profiles of inhibition by dibucaine and sodium fluoride. Chimpanzees and gorillas strongly resemble humans, and differ from other hominoids and cercopithecoids, in patterns of dibucaine and fluoride resistance and relative activity toward various thio esters. “Silent” cholinesterase phenotypes of probable veterinary significance, and analogous to a rare human variant, are apparently normal in some catarrhine species and are present as a polymorphism among orangutans and lion-tailed macaques.