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Origin of anthropoidea: dental evidence and recognition of early anthropoids in the fossil record, with comments on the Asian anthropoid radiation.

Among the earliest fossil anthropoid primates known are Catopithecus browni, Serapia eocaena, Arsinoea kallimos, and Proteopithecus sylviae, from the late Eocene quarry L-41, Fayum Depression, Egypt. Two of these taxa, C. browni and S. eocaena, may be the oldest known members of the Propliopithecidae and Parapithecidae, respectively, while A. kallimos and P. sylviae are archaic anthropoids of less certain familial affiliation. Dental features of C. browni, S. eocaena, A. kallimos, and P. sylviae are compared with those of younger propliopithecids and parapithecids from the Fayum in order to determine the morphocline polarities of dental features among these early anthropoids. From this, a basal African anthropoid dental morphotype is constructed. Among the features of this morphotype are: dental formula of 2.1.3.3; incisors subvertically implanted and somewhat spatulate; p2 as large as p3, both lacking paraconids; p4 weakly obliquely oriented but not exodaenodont; all lower molars with small paraconids present; upper anterior premolars lacking protocone; upper molars with small, cingular hypocones, all cheek teeth nonbunodont; and canines projecting but not necessarily sexually dimorphic. Comparisons are made between this African anthropoid morphotype and two of the best-represented proposed basal anthropoids, Eosimias and Djebelemur, with the result that neither appears to be a good candidate to have been ancestral to the African anthropoids. Other possible basal simians such as Algeripithecus, Tabelia, and Biretia also are evaluated but are too poorly known for adequate analysis. The larger-bodied Asian primates Pondaungia, Amphipithecus, and Siamopithecus also are not likely ancestors for African anthropoids, but like Eosimias they may share a common ancestry. Despite many recent claims of an Asian origin for anthropoids, the evidence remains far from compelling. The true origins of Anthropoidea remain obscure.

Africa↗

Siamopithecus eocaenus, a late Eocene anthropoid primate from Thailand: its contribution to the evolution of anthropoids in Southeast Asia.

Dental remains of a late Eocene anthropoid primate from Thailand, Siamopithecus eocaenus, have been recently reported; complete description and comparisons of this material are given here. Siamopithecus displays several derived dental features that suggest close phylogenetic affinities among the Thai species, the Burmese Pondaungia, and the North African and Omani propliopithecines Aegyptopithecus and Moeripithecus. The geographic origin of anthropoid primates cannot be securely determined at present, but the available fossil record indicates that faunal exchanges between Africa and Southeast Asia were very probable during the Eocene, and that direct relationships between Asian and African anthropoid primates can be inferred.

Animals↗

Anthropoid primates from the Oligocene of Pakistan (Bugti Hills): data on early anthropoid evolution and biogeography.

Asian tarsiid and sivaladapid primates maintained relictual distributions in southern Asia long after the extirpation of their close Holarctic relatives near the Eocene-Oligocene boundary. We report here the discovery of amphipithecid and eosimiid primates from Oligocene coastal deposits in Pakistan that demonstrate that stem anthropoids also survived in southern Asia beyond the climatic deterioration that characterized the Eocene-Oligocene transition. These fossils provide data on temporal and paleobiogeographic aspects of early anthropoid evolution and significantly expand the record of stem anthropoid evolution in the Paleogene of South Asia.

Animals↗

Evolution of anthropoid jaw loading and kinematic patterns.

Major transformations in the skull and masticatory system characterized the evolution of crown anthropoids. To offer further insight into the phylogenetic and arguably adaptive significance of specific primate mandibular loading and kinematic patterns, allometric analyses of metric parameters linked to masticatory function are performed within and between 47 strepsirhine and 45 recent anthropoid species. When possible, basal anthropoids are considered. These results are subsequently integrated with prior experimental and morphological work on primate skull form. As compared to strepsirhines, crown anthropoids have a vertically longer ascending ramus linked to a glenoid and condyle positioned relatively higher above the occlusal plane. Interestingly, anthropoids and strepsirhines do not exhibit different mean ratios of condylar to glenoid height, which suggests that both clades are similar in their ability to evenly distribute occlusal contacts and perhaps forces along the postcanine teeth. Thus, given the considerable suborder differences in the scaling of both glenoid and condylar height, we argue that much of this variation in jaw-joint height is linked to suborder differences in relative facial height due in turn to increased encephalization, basicranial flexion, and facial kyphosis in anthropoids. Due to a more elongate ascending ramus, anthropoids evince more vertically oriented masseters than like-sized strepsirhines. Having a relatively longer ramus and a more medially displaced lateral pterygoid plate, crown anthropoids exhibit medial pterygoids oriented similar to those of strepsirhines, but with a variably longer lever arm. As anthropoid masseters are less advantageously placed to effect transverse movements/forces, we argue that balancing-side deep-masseter activity underlying a wishboning loading regime serves to increase, or at least maintain, transverse levels of jaw movement and occlusal force at the end of the masticatory power stroke. Crown anthropoids are also more isognathic and isodontic than strepsirhines. A consideration of early anthropoids suggests that the crown anthropoid masticatory pattern, i.e., more vertical masseters due to a high condyle as well as greater isognathy and isodonty, occurred stepwise during stem anthropoid evolution. This appears to correspond to a more transverse, and perhaps progressively larger, power stroke across oligopithecids, parapithecids, and propliopithecids.

Adaptation, Physiological↗

Phylogenetic analysis of anthropoid relationships.

The relationships of anthropoids to other primates are currently debated, as are the relationships among early fossil anthropoids and crown anthropoids. To resolve these issues, data on 291 morphological characters were collected for 57 taxa of living and fossil primates and analyzed using PAUP and MacClade. The dental evidence provides weak support for the notion of an adapid origin for anthropoids, the cranial evidence supports the tarsier-anthropoid hypothesis, and the postcranial evidence supports a monophyletic Prosimii and a monophyletic Anthropoidea. Combining these data into a single data set produces almost universal support for a tarsier-anthropoid clade nested within omomyids. Eosimias and Afrotarsius are certainly members of this clade, and probably basal anthropoids, although the Shanghuang petrosal may not belong to Eosimias. The tree derived from the combined data set resembles the tree derived from the cranial data set rather than the larger dental data set. This may be attributable to relatively slower evolution in the cranial characters. The combined data set shows Anthropoidea to be monophyletic but the features traditionally held to be anthropoid synapomorphies are found to have evolved mosaically. Parapithecines are the sister taxon to crown anthropoids; qatraniines and oligopithecids are more distantly related sister taxa. There is support for a relationship of a Tarsius + Anthropoidea clade with either washakiines on Uintanius. These elements of tree topology remain fairly stable under different assumptions sets, but overall, tree topology is not robust. Previously divergent hypotheses regarding anthropoid relationships are attributable to the use of restricted data sets. This large data set enables the adapid-anthropoid hypothesis to be rejected, and unites Tarsius, Anthropoidea and Omomyiformes within a clade, Haplorhini. However, relationships among these three taxa cannot be convincingly resolved at present.

Animals↗

Anthropoid cranial base architecture and scaling relationships.

This paper examines how various measures of basicranial length and cranial base angulation affect the relationship between basicranial flexion and relative brain size in anthropoids, including Homo sapiens. Most recent studies support the "spatial packing" hypothesis, that basicranial flexion in haplorhines maximizes braincase volume relative to basicranial length. However, a few studies find the basicranium is less flexed in H. sapiens than expected for other anthropoids, suggesting that other factors contribute to variation in hominin basicranial flexion. The measure of relative brain size used to test the spatial packing hypothesis, the Index of Relative Encephalization (IRE), is calculated with basicranial length (BL) in its denominator, so that shorter BL and larger brain size potentially inflate H. sapiens IREs. To investigate this problem, the lengths of midline cranial floor sections were scaled relative to the cube root of endocranial volume in 157 specimens from 18 anthropoid species. Results indicate that the posterior cranial base and planum sphenoideum are significantly shorter in H. sapiens than in other anthropoids, accounting for higher IREs. Including the cribriform plate in BL, advisable in studies using anthropoids, affects whether H. sapiens differs from other anthropoids for basicranial flexion vs. IRE. However, despite a shorter BL and elevated IRE, H. sapiens does not deviate significantly from the anthropoid relationship between basicranial flexion and relative brain size for two cranial base angles. Because different measures of cranial base angulation change how H. sapiens falls along the anthropoid regression line, it remains equivocal whether the basicranium is less flexed in H. sapiens than in other anthropoids when compared to relative brain size.

Animals↗

Anthropoid origins and the modern symphysis.

To highlight adaptive transformations in craniomandibular form during anthropoid origins, symphyseal character states and underlying masticatory loading regimes were investigated vis-à-vis shifts in diet and body size. A study of fossil anthropoids is possible because variation in symphyseal fusion is continuous and directly proportional to the amount of symphyseal stress and because such variation can be considered a series of discrete character states each with unique functional underpinnings. Using recent systematic renderings of Eocene and Oligocene taxa as a template with which to assess character evolution, this analysis indicates when, and in which clade(s), specific masticatory features became fixed and thus diagnostic. A general trend throughout early anthropoid evolution is for descendent taxa to be progressively larger than ancestral forms. Coupled with this pattern is the tendency for larger-bodied fossil anthropoids to have ingested tougher diets variably consisting of thick-coated, unripe fruits and/or leaves. Mastication of mechanically tougher foods entails greater repetitive loading of the mandible and requires relatively larger amounts of balancing-side muscle force, thus resulting in correspondingly greater symphyseal fusion due to elevated dorsoventral shear. With a single exception, these adaptive transformations characterize the evolutionary pathway leading both to parapithecines and a catarrhine:platyrrhine clade (crown anthropoids). While the ancestor of crown anthropoids would have possessed a body size, diet and masticatory adaptations similar to parapithecines, such a common suite of features evolved independently. Moreover, the evolution of an early-fusing symphysis and associated wishboning loading regime of catarrhines and platyrrhines is unique among all anthropoids. Lastly, the apparent lack of reversals in symphyseal fusion indicates the improbability of phylogenetic hypotheses in which a relationship is proposed between 'ancestral' taxa with a greater degree of symphyseal fusion and 'descendent' anthropoids with a lesser degree of ossification.

Animals↗

Temporalis function in anthropoids and strepsirrhines: an EMG study.

The major purpose of this study is to analyze anterior and posterior temporalis muscle force recruitment and firing patterns in various anthropoid and strepsirrhine primates. There are two specific goals for this project. First, we test the hypothesis that in addition to transversely directed muscle force, the evolution of symphyseal fusion in primates may also be linked to vertically directed balancing-side muscle force during chewing (Hylander et al. [2000] Am. J. Phys. Anthropol. 112:469-492). Second, we test the hypothesis of whether strepsirrhines retain the hypothesized primitive mammalian condition for the firing of the anterior temporalis, whereas anthropoids have the derived condition (Weijs [1994] Biomechanics of Feeding in Vertebrates; Berlin: Springer-Verlag, p. 282-320). Electromyographic (EMG) activities of the left and right anterior and posterior temporalis muscles were recorded and analyzed in baboons, macaques, owl monkeys, thick-tailed galagos, and ring-tailed lemurs. In addition, as we used the working-side superficial masseter as a reference muscle, we also recorded and analyzed EMG activity of the left and right superficial masseter in these primates. The data for the anterior temporalis provided no support for the hypothesis that symphyseal fusion in primates is linked to vertically directed jaw muscle forces during mastication. Thus, symphyseal fusion in primates is most likely mainly linked to the timing and recruitment of transversely directed forces from the balancing-side deep masseter (Hylander et al. [2000] Am. J. Phys. Anthropol. 112:469-492). In addition, our data demonstrate that the firing patterns for the working- and balancing-side anterior temporalis muscles are near identical in both strepsirrhines and anthropoids. Their working- and balancing-side anterior temporalis muscles fire asynchronously and reach peak activity during the power stroke. Similarly, their working- and balancing-side posterior temporalis muscles also fire asynchronously and reach peak activity during the power stroke. Compared to these strepsirrhines, however, the balancing-side posterior temporalis of anthropoids appears to have a relatively delayed firing pattern. Moreover, based on their smaller W/B ratios, anthropoids demonstrate a relative increase in muscle-force recruitment of the balancing-side posterior temporalis. This in turn suggests that anthropoids may emphasize the duration and magnitude of the power stroke during mastication. This hypothesis, however, requires additional testing. Furthermore, during the latter portion of the power stroke, the late activity of the balancing-side posterior temporalis of anthropoids apparently assists the balancing-side deep masseter in driving the working-side molars through the terminal portion of occlusion.

Animals↗

Chronology of primate discoveries in Myanmar: influences on the anthropoid origins debate.

The history of primate paleontology in Asia is long and complex, beginning with the first discoveries of fossil primates on the Indian subcontinent in the early 1830's. The first Eocene mammals from Asia were collected in Myanmar and described in 1916, while the first primates, Pondaungia and Amphipithecus, were described in 1927 and 1937, respectively, both from the Pondaung Formation in Myanmar. For the next 60 years, these two Pondaung taxa remained as the only known Eocene primates from Myanmar and one of the few records of Eocene primates from all of Asia. Taxonomically, Pondaungia and Amphipithecus were linked with a number of different groups, including archaic, hoofed ungulates (condylarths), adapiform primates, omomyid primates, and anthropoids. While no consensus existed, Pondaungia and Amphipithecus were most commonly compared with anthropoids. Beginning in the late 1990s, new primates were discovered in Myanmar, including smaller-bodied forms such as Bahinia and Myanmarpithecus. Also, new and better specimens of the larger-bodied Pondaungia and Amphipithecus began to appear, including the first cranial and postcranial fragments. Evaluations based on these new specimens, especially the postcrania, indicate that the two larger-bodied Myanmar taxa are adapiform primates that show their closest affinities to North American notharctines. The smaller-bodied taxa remain enigmatic, but may share their closest affinities with North American and Asian omomyid primates and Asian Tarsius. None of the known Asian primate taxa appear closely related to African anthropoids, which suggests that true anthropoids did not reach Asia until the latest Oligocene or earliest Miocene. These facts make an Asian origin for Anthropoidea unlikely. Additional and earlier evidence from both Asia and Africa is required before the ultimate origin of anthropoids can be determined. It appears possible that true anthropoids were an ancient radiation that may have been part of a Gondwanan (southern hemisphere) community that is, at present, poorly sampled and little understood.

Animals↗

Astragalar morphology of late Eocene anthropoids from the Fayum Depression (Egypt) and the origin of catarrhine primates.

The phylogenetic relationships of the late Eocene anthropoids Catopithecus browni and Proteopithecus sylviae are currently a matter of debate, with opinion divided as to whether these taxa are stem or crown anthropoids. The phylogenetic position of Catopithecus is of particular interest, for, unlike the highly generalized genus Proteopithecus, this taxon shares apomorphic dental and postcranial features with more derived undoubted catarrhines that appear in the same region 1-2 Ma later. If these apomorphies are homologous and Catopithecus is a stem catarrhine, the unique combination of plesiomorphic and apomorphic features preserved in this anthropoid would have important implications for our understanding of the crown anthropoid morphotype and the pattern of morphological character transformations that occurred during the early phases of stem catarrhine evolution.Well-preserved astragali referrable to Proteopithecus, Catopithecus, and the undoubted early Oligocene stem catarrhine Aegyptopithecus have provided additional morphological evidence that allows us to further evaluate competing hypotheses of interrelationships among Eocene-Oligocene Afro-Arabian anthropoids. Qualitative observations and multivariate morphometric analyses reveal that the astragalar morphology of Proteopithecus is very similar to that of early Oligocene parapithecids and living and extinct small-bodied platyrrhines, and strengthens the hypothesis that the morphological pattern shared by these taxa is primitive within crown Anthropoidea. In contrast, Catopithecus departs markedly from the predicted crown anthropoid astragalar morphotype and shares a number of apomorphic features (e.g., deep cotylar fossa, laterally projecting fibular facet, trochlear asymmetry, mediolaterally wide astragalar head) with Aegyptopithecus and Miocene-Recent catarrhines. The evidence from the astragalus complements other independent data from the dentition, humerus and femur of Catopithecus that support this taxon's stem catarrhine status, and we continue to maintain that oligopithecines are stem catarrhines that constitute the sister group of a clade containing propliopithecines and Miocene-Recent catarrhines.

Animals↗

First skulls of the early Eocene primate Shoshonius cooperi and the anthropoid-tarsier dichotomy.

The phylogenetic relationships of living tarsiers and extinct omomyid primates are critical for deciphering the origin and relationships of primate higher taxa, particularly anthropoids. Three competing phylogenetic hypotheses are: (1) tarsiers are most closely related to early Cenozoic Omomyidae, particularly genera such as Necrolemur from the late Eocene of Europe; (2) tarsiers share a more recent common ancestry with anthropoids than they do with any known omomyid; (3) tarsiers and/or omomyids are most closely related to strepsirhines. The anatomy of four skulls of the early Eocene omomyid Shoshonius cooperi--the first cranial material recovered for this genus--strongly suggests that Shoshonius shares a more recent common ancestry with Tarsius than do either anthropoids or other Eocene omomyids for which cranial anatomy is known. If the primate suborder Haplorhini (anthropoids, omomyids, tarsiids) is monophyletic, the phylogenetic position of Shoshonius requires that anthropoids and Tarsius diverged by at least the early Eocene, some 15 million years before the first appearance of anthropoids in the fossil record.

Animals↗

The oldest known anthropoid postcranial fossils and the early evolution of higher primates.

The middle Eocene primate family Eosimiidae, which is known from sites in central and eastern China and Myanmar, is central to efforts to reconstruct the origin and early evolution of anthropoid or 'higher' primates (monkeys, apes and humans). Previous knowledge of eosimiid anatomy has been restricted to the dentition and an isolated petrosal bone, and this limited anatomical information has led to conflicting interpretations of early anthropoid phylogeny. Here we describe foot bones of Eosimias from the same middle Eocene sites in China that yield abundant dental remains of this primate. Tarsals of Eosimias show derived anatomical traits that are otherwise restricted to living and fossil anthropoids. These new fossils substantiate the anthropoid status of Eosimias and clarify the phylogenetic position of anthropoids with respect to other major primate clades. Early anthropoids possessed a mosaic of primitive and derived traits in their postcranial skeletons, reflecting their derivation from haplorhine ancestors that retained many prosimian-like features.

Animals↗

A new Late Eocene anthropoid primate from Thailand.

The fossil record of anthropoid primates from the Middle Eocene of South Asia is so far restricted to two genera (Pondaungia cotteri Pilgrim, 1937 and Amphipithecus mogaungensis Colbert, 1937 from the Eocene Pondaung deposits of Burma) whose anthropoid status and phylogenetic position have long been under debate because they represent the oldest highly derived fossil primates of anthropoid grade. Moreover, several new African taxa, some of which are even older, have been recently included in the suborder Anthropoidea, suggesting an African origin for this group. Conversely, new fossil primates recently discovered in China (Eosimias) have been related to the most primitive representatives of Anthropoidea, alternatively suggesting an Asian origin and a probable Asian radiation centre. We report here the discovery of a new anthropoid from the Thai Late Eocene locality of Krabi, which displays several additional anthropoid characters with regard to those of the Eocene Burmese genera. This species, which is about the size of the Fayum Aegyptopithecus, can be related to the Burmese forms, and it further provides strong additional evidence for a southeast Asian evolutionary centre for anthropoids.

Animals↗

Intrasexual competition and body weight dimorphism in anthropoid primates.

Body weight dimorphism in anthropoid primates has been thought to be a consequence of sexual selection resulting from male-male competition for access to mates. However, while monogamous anthropoids show low degrees of weight dimorphism, as predicted by the sexual selection hypothesis, polygynous anthropoids show high variation in weight dimorphism that is not associated with measures of mating system or sex ratio. This observation has led many to debate the role of other factors such as dietary constraints, predation pressure, substrate constraints, allometric effects, and phylogeny in the evolution of anthropoid weight dimorphism. Here, we re-evaluate variation in adult body weight dimorphism in anthropoids, testing the sexual selection hypothesis using categorical estimates of the degree of male-male intrasexual competition ("competition levels"). We also test the hypotheses that interspecific variation in body weight dimorphism is associated with female body weight and categorical estimates of diet, substrate use, and phylogeny. Weight dimorphism is strongly associated with competition levels, corroborating the sexual selection hypothesis. Weight dimorphism is positively correlated with increasing female body weight, but evidence suggests that the correlation reflects an interaction between overall size and behavior. Arboreal species are, on average, less dimorphic than terrestrial species, while more frugivorous species tend to be more dimorphic than folivorous or insectivorous species. Several alternative hypotheses can explain these latter results. Weight dimorphism is correlated with taxonomy, but so too are competition levels. We suggest that most taxonomic correlations of weight dimorphism represent "phylogenetic niche conservatism"; however, colobines show consistently low degrees of weight dimorphism for reasons that are not clear.

Animals↗

Deep time and the search for anthropoid origins.

Recent fossil discoveries, phylogenetic analyses, revised reconstructions of continental drift, and accumulating molecular evidence have all yielded new information relating to anthropoid origins within the broader context of primate evolution. There is an emerging consensus among molecular studies that four superorders of eutherian mammals can be recognized: Afrotheria, Euarchontoglires (to which primates belong), Laurasiatheria, and Xenarthra. Overall, molecular phylogenies for mammals agree with some statistical analyses of the primate fossil record in indicating an early origin for primates around 85 Ma ago, and the divergence of haplorhines and strepsirrhines at ca. 77 Ma. Such an ancient date for the origin of haplorhines is some 17 Ma prior to the first known possible primate, and some 22 Ma before the earliest fossil evidence of undoubted euprimates. Because anthropoid fossils date back at least to the late Eocene and perhaps to the middle Eocene, and given indications of an early origin for primates, it is unlikely that ancestral anthropoids arose within any other currently known clade of fossil primates (adapiforms, omomyiforms, strepsirrhines, or tarsiiforms). Implications of new molecular, morphological, and biogeographic lines of evidence are explored with respect to the likely time and place of the origin of anthropoids. Four competing, testable hypotheses are reviewed in detail: 1) the Paratethyan hypothesis, 2) the continental Asian hypothesis, 3) the Indo-Madagascar hypothesis, and 4) the African hypothesis. A case is made that current evidence best supports a relatively ancient Gondwanan origin for primates, as well as a Gondwanan (African or Indo-Madagascan) origin for anthropoids at least as old as that of any other currently documented major primate clade. Available fossil evidence at present seems to be most compatible with the African hypothesis, but it is noteworthy that primates are included not in Afrotheria but in Euarchontoglires.

Animals↗

Architectonics of the parietal and temporal association cortex in the strepsirhine primate Galago compared to the anthropoid primate Macaca.

A number of higher order association areas have been described in the parietal and temporal cortex of large-brained anthropoid primates such as Macaca. However, little is known about the evolution of these areas, and the existence of homologous areas has not yet been clearly demonstrated in other mammalian groups. We addressed this issue by comparing the myelo- and cytoarchitecture of posterior association cortex in the anthropoid Macaca to that of the small-brained, strepsirhine ("prosimian") primate Galago. Our results suggest that Galago possesses many, if not most, of the areas present in Macaca. We were able to identify regions in Galago which resemble Macaca posterior parietal area 7, superior temporal polysensory cortex (ST), inferotemporal visual cortex (IT), the temporoparietal auditory area (Tpt), and posterior parahippocampal cortex (areas TH and TF). Area 7, ST, and IT can each be subdivided further in Macaca, and for most of these subdivisions we were able to identify counterparts in Galago. However, we could not distinguish as many divisions of ST cortex in Galago as in Macaca, and it is possible that new areas arose in this region during anthropoid evolution. There also appear to be general differences in architectonic organization between these animals, with Macaca exhibiting greater development of pyramidal layer IIIc and of the internal granular layer (IV) across much of the parieto-temporal cortex. These findings suggest that many, although possibly not all, of the parietal and temporal association areas present in the modern anthropoid Macaca evolved early in primate history, prior to the divergence of the lineages leading to strepsirhines and anthropoids.

Animals↗

Rapid electrostatic evolution at the binding site for cytochrome c on cytochrome c oxidase in anthropoid primates.

Cytochrome c (CYC) oxidase (COX), a multisubunit enzyme that functions in mitochondrial aerobic energy production, catalyzes the transfer of electrons from CYC to oxygen and participates in creating the electrochemical gradient used for ATP synthesis. Modeling three-dimensional structural data on COX and CYC reveals that 57 of the >1,500 COX residues can be implicated in binding CYC. Because of the functional importance of the transfer of electrons to oxygen, it might be expected that natural selection would drastically constrain amino acid replacement rates of CYC and COX. Instead, in anthropoid primates, although not in other mammals, CYC and COX show markedly accelerated amino acid replacement rates, with the COX acceleration being much greater at the positions that bind CYC than at those that do not. Specifically, in the anthropoid lineage descending from the last common ancestor of haplorhines (tarsiers and anthropoids) to that of anthropoids (New World monkeys and catarrhines) and that of catarrhines (Old World monkeys and apes, including humans), a minimum of 27 of the 57 COX amino acid residues that bind CYC were replaced, most frequently from electrostatically charged to noncharged residues. Of the COX charge-bearing residues involved in binding CYC, half (11 of 22) have been replaced with uncharged residues. CYC residues that interact with COX residues also frequently changed, but only two of the CYC changes altered charge. We suggest that reducing the electrostatic interaction between COX and CYC was part of the adaptive evolution underlying the emergence of anthropoid primates.

Adaptation, Physiological↗