Primates

Abstract

Homo sapiens is just one of some 400 extant species allocated to the mammalian order Primates, originally proposed by Linnaeus in the mid-18th Century. As George Gaylord Simpson tartly noted in his seminal 1945 classification of the class Mammalia: “The primates are inevitably the most interesting of mammals to an egocentric species that belongs to this order.” Intense interest in our own origins is directly reflected by ever-increasing research into primate biology, including morphology, physiology, behaviour and ecology, as well as genetics and genomics. Over the past four decades, the number of recognized primate species has more than doubled, due to expanding field studies and molecular investigations. Across primates, comparisons of both mitochondrial and nuclear DNA have led to the identification of many ‘cryptic’ species that were not immediately evident from general morphology. Homo sapiens is just one of some 400 extant species allocated to the mammalian order Primates, originally proposed by Linnaeus in the mid-18th Century. As George Gaylord Simpson tartly noted in his seminal 1945 classification of the class Mammalia: “The primates are inevitably the most interesting of mammals to an egocentric species that belongs to this order.” Intense interest in our own origins is directly reflected by ever-increasing research into primate biology, including morphology, physiology, behaviour and ecology, as well as genetics and genomics. Over the past four decades, the number of recognized primate species has more than doubled, due to expanding field studies and molecular investigations. Across primates, comparisons of both mitochondrial and nuclear DNA have led to the identification of many ‘cryptic’ species that were not immediately evident from general morphology. Although Simpson rightly lampooned the bias emanating from human arrogance, primates are interesting in their own right. Most notably, all living species live in fairly elaborate social networks with enhanced communication between individuals, foreshadowing the social complexity shown by modern humans. It is notable, however, that many relatively primitive primates are nocturnal and commonly described as ‘solitary’. This label has often been seen as the opposite of ‘social’. But field studies have revealed that nocturnal primates also have well established patterns of social interactions, so all primates are social. The difference is that ‘solitary’ nocturnal primates do not move around in groups, whereas diurnal (day-active) primates are typically gregarious, living in recognizable social groups. Gregarious behaviour is seemingly connected with increased brain size and, presumably, with intelligence. Yet a shift from nocturnal to diurnal habits in primate evolution is also connected with increased importance of vision, itself a cause of brain expansion, so this may be a driving influence. In any event, the pronounced social tendency now documented for all primates is doubtless linked to heavy investment in individual offspring (including intensive parental care) and extended lifespans. From geographical distribution alone, five ‘natural groups’ of extant primates are apparent (Figure 1), which provide the scaffold for all classifications and evolutionary trees. The first group contains the lemurs (Lemuriformes), the only primates present on the island of Madagascar, where they underwent a major adaptive radiation. In addition to the almost eighty species of lemur alive today, that array included around twenty mostly larger-bodied sub-fossil species — some almost as big as a gorilla — that died out during the last two thousand years or so, after the first humans colonized Madagascar. The second natural group contains lorises, pottos and bushbabies (Lorisiformes). They are far more widely spread, occurring in Africa and South and Southeast Asia. But their adaptive radiation was more limited, comprising only some thirty species. The third group, containing a dozen or so generally similar tarsier species (Tarsiiformes), represents an even smaller array in the Southeast Asian archipelago. The monkeys of South and Central America (Platyrrhini) are the fourth natural group. They are the only extant primates found in the New World, where they diversified extensively, yielding some one-hundred-and-thirty known species. Platyrrhine monkeys fall into two fairly distinct groups, the relatively small, claw-bearing marmosets and tamarins and the larger-bodied true monkeys. The fifth group, containing Old World monkeys and apes (infra-order Catarrhini), is the largest of all, with over one hundred-and-fifty species in Africa, South Asia and Southeast Asia. Despite extensive overlap in geographical distribution, monkeys and apes of the Old World belong to two distinct sister groups. Humans also count among the ape subgroup of catarrhine primates, but expanded far beyond the original geographical range during the later stages of their evolution. Because they have generally retained a greater proportion of primitive characters, the first three natural groups of primates (lemurs, loris group, tarsiers) are often collectively called prosimians (literally ‘pre-monkeys') or ‘lower primates’. Prosimians are all relatively small, with a modal body weight around 500 g, and most are active at night. In fact, various lines of evidence indicate that ancestral primates, like the ancestral placental mammals, were nocturnal. As a rule, primates are clearly either nocturnal or diurnal. But certain lemurs, notably bamboo and brown lemurs, show a highly unusual blend of nocturnal and diurnal activity, for which Ian Tattersall coined the term ‘cathemerality’. Contrasting with prosimians, the ‘higher primates’ or simians — monkeys, apes and humans — share a distinctive suite of advanced anatomical features in their teeth, jaws, brain and reproductive system. Except for the owl monkeys of the New World, all simians are diurnal. They are typically large-bodied, with a modal weight of about 5 kg. Across primates in general, body sizes show a three-thousand-fold range from 40 g for the pygmy mouse lemur to 120 kg for an adult male gorilla. Although they have retained many primitive features, tarsiers show several specific similarities to simians in vision, olfaction, brain morphology and reproduction. This has long suggested an ancestral link between tarsiers and simians that has been confirmed by multiple lines of molecular evidence. For this reason, another basic distinction is drawn between lemurs and lorisiforms on one hand and tarsiers and simians on the other. Lemurs and lorisiforms are known as ‘strepsirrhines’ because they have retained a naked, moist area of skin (rhinarium) around the nostrils. Tarsiers and simians are called ‘haplorhines’ because, uniquely among mammals, they have secondarily lost the rhinarium. It is often said that primates lack obvious defining anatomical features of other orders of mammals, such as gnawing teeth of rodents or the wings of bats. Moreover, primates have traditionally been seen as forming a graded series, ranging from primitive lemurs to highly advanced humans. This perceived gradation among primates is allied to the concept of a smooth transition from insectivores — the archetypal primitive mammals — to primates, across an ‘insectivore–primate boundary’. This idea was connected to the inclusion of the tree-shrews of South and Southeast Asia in the order Primates, accepted by Simpson in his classification. Many investigators saw tree-shrews as ideal intermediates between an insectivore, such as a hedgehog, and a relatively primitive primate, such as a lemur. But, this interpretation directly resulted from the ‘frozen ancestor’ approach to evolutionary relationships, in which extant species are taken as models for evolutionary stages. Of course, there is no evolutionary sequence from hedgehogs through tree-shrews to lemurs. These extant species are all end-points on the phylogenetic tree of mammals, which must be painstakingly reconstructed through analysis of individual characters. Such reconstructions indicate that tree-shrews, at best, are only distantly related to primates. With tree-shrews excluded, all extant primates do in fact share a substantial set of characteristics distinguishing them from other placental mammals. Primates are typically tree-living (arboreal) inhabitants of tropical and subtropical forests. Arboreality is relatively rare among extant placental mammals, and primates have special adaptations for that lifestyle: their hands and feet are adapted to grasp twigs and branches, rather than to grapple tree trunks. In all extant primates except humans, the big toe (hallux) diverges widely from the other digits, permitting the foot to grasp powerfully, while the hand usually has at least some grasping capacity. The fingers typically bear blunt, flat nails rather than bilaterally flattened, pointed claws. The ventral surfaces of fingers and toes bear tactile pads with skin ridges (dermatoglyphs) that provide traction on arboreal substrates and, in association with Meissner's corpuscles, enhance the sense of touch. The body's center of gravity is typically located closer to the hindlimbs and locomotion is generally characterized by hindlimb domination. The characteristic walking gait follows a diagonal sequence, with the hand preceding the foot on each side, rather than a lateral sequence, which otherwise predominates among placental mammals. In the foot, the distal segment of the heel-bone is commonly somewhat elongated. As a further adaptation for life in trees, primates have a greatly enhanced visual sense. Their eyes are notably large in relation to body size, and primates with nocturnal habits generally have even bigger eyes, while most other nocturnal mammals have very small eyes and depend on other senses to make their way around at night. The prominent eyes of primates are consistently associated with the presence of a bony bar behind the eye-socket (orbit). Although rare among mammals, the bony bar is not confined to primates. Haplorhine primates, however, are truly unique. In addition to the postorbital bar, tarsiers and simians have an ossified partition behind the eye, more-or-less isolating the eye in a bony cup. But, orientation is what really makes the eyes of all primates special. Forward rotation of the eyes, along with their orbits, ensures extensive overlap between the left and right visual fields, especially in simians. This basic adaptation for binocular viewing of objects provides the basis for well-developed stereoscopic vision, involving enhancement of visual centres in the brain. Inputs from the optic nerves have been fundamentally reorganized. In the primitive vertebrate condition, which is largely preserved in tree-shrews, the optic nerves cross over almost completely, such that inputs from the right eye predominantly pass to the left side of the brain and vice versa. In primates, by contrast, only half of the inputs cross over, while the rest pass to the same side of the brain. This means that inputs from the two eyes can be directly connected and processed on each side of the brain. The ear of primates is also distinctive. In mammals, a ventral floor protects the middle ear chamber that evolved in parallel in most orders of mammals, in some cases inflating to form an auditory bulla. In primates, the bulla is formed predominantly as an outgrowth of the petrosal bone, which houses the inner ear mechanism and the semicircular canals. Formation of an auditory bulla from the petrosal is unique to primates, contrasting, for example, with tree-shrews, whose bulla is formed from a separate entotympanic element. It is commonly stated that the olfactory system has been reduced in primates, but this is most evident in haplorhines. Several nocturnal strepsirrhines show little evidence of reduction, but anatomical elements of the olfactory apparatus have been reduced in a number of diurnal lemurs. Largely because of the increased importance of vision, brain enlargement is also common among primates. However, this feature is often overstated as primates having larger brains than other mammals. This is clearly not true of absolute brain size, which is four times larger in an elephant, for instance, than in humans. But primates are not even clearly distinguished from other mammals when body size is taken into account. Although humans do have the largest relative brain size among mammals, many dolphins have brains that are almost as large compared to body size. Relative brain size varies widely within mammals, and a few primates actually have values lower than the average mammal. Nonetheless, the average relative brain size in primates is greater than the average for any other order of mammals. There are also two unique features of primate brain anatomy. Extant species consistently possesses a true sylvian sulcus, extending obliquely backwards from the rhinal sulcus and reflecting the increased importance of the temporal lobe, and a three-branched calcarine sulcus on the inner face of the occipital lobe. Reconstruction of evolutionary relationships among mammals has relied heavily on jaws and teeth. Primate teeth have remained comparatively primitive — for instance, the cheek teeth (premolars and molars) have remained relatively unspecialized. Molars in the common ancestor of marsupials and placentals most likely had a triangle of cusps in the upper molar and a comparable triangle in the lower molar combined with a low posterior heel bearing additional cusps. Extant primates show a general tendency to possess an additional, fourth cusp on the upper molar, while the lower molar typically retains only two cusps from the original triangle. The cusps of primate molars are generally low and rounded, often attributed to a shift in diet away from arthropods toward fruits. The maximum dental formula of crown placental mammals is 3 incisors, 1 canine, 4 premolars and 3 molars on either side of both upper and lower jaws. This formula (3.1.4.3/3.1.4.3) is commonly taken as the likely ancestral condition. The maximal formula of extant primates (2.1.3.3/2.1.3.3) differs through loss of one incisor and one premolar in each tooth row. Loss of an incisor is connected with a distinctive feature in the upper jaw of primates, namely marked reduction in length of the premaxilla (the anterior bone bearing the incisors) and a shift from longitudinal to transverse arrangement of the upper incisors. Primates are also distinctive with respect to reproduction: females give birth to well-developed (precocial) neonates after comparatively long gestation periods. Most primates have just a single infant at a time. Relative to body size, fetal and postnatal growth are slow, sexual maturity is attained late and life-spans are long. In sum, primates are adapted to breed at a leisurely pace, dubbed ‘life in the slow lane’. Thus, daily investment of resources in primate reproduction is low, but adds up to heavy investment in individual offspring over the long term. There are also notable features of reproductive anatomy. Male primates consistently have permanent descent of the testes into a scrotum behind the base of the penis. Unusually, however, descent typically occurs around the time of birth, despite relatively late sexual maturation. In contrast to many other mammals (including tree-shrews), adult female primates are distinguished by complete separation of the urinary and reproductive tracts. Although all primates share certain advanced features, such as elimination of the yolk-sac at least after mid-gestation, they are decidedly unusual when it comes to placentation. Whereas placentation of strepsirrhines is non-invasive (epitheliochorial), haplorhines have a highly invasive (haemochorial) placenta. A long-cherished view has been that a non-invasive placenta is primitive and inefficient and that increasing invasiveness is an advanced feature associated with more efficient transfer of maternal resources to the fetus. However, recent analyses suggest that ancestral placental mammals had invasive placentation, probably of an intermediate (endotheliochorial) type, from which the non-invasive placentation of strepsirrhines and the highly invasive placentation of haplorhines probably diverged. Clearly recognizable, direct fossil relatives of primates — ‘euprimates’ or ‘primates of modern aspect’ — date back to the earliest Eocene, about 55 million years ago (mya). By the beginning of the Miocene (about 25 mya), identifiable relatives of most modern groups are present. In addition to euprimates, it is common practice to include in the order Primates an array of generally earlier plesiadapiform mammals, collectively known as ‘archaic primates’. However, these fossil forms — which come mainly from the Palaeocene (65–55 mya) — show few of the defining features of extant primates and their affinity with primates is questionable. However, the current consensus is that archaic primates diverged before the adaptive radiation that gave rise to extant primates and their direct fossil relatives (Figure 2). The earliest known euprimates are evidently adapted for arboreal life and possess many of the key features in the skull, teeth and postcranial skeleton that characterize modern primates. In fact, two main families of early euprimates are documented mainly from the Eocene (35–55 mya), although a few species survived until the late Miocene. Representatives of both families were found widely in North America, Europe and Asia. The family Adapidae contains species that are often medium-sized and rather lemur-like, while the Omomyidae includes species that are generally smaller and quite tarsier-like. Many authors have linked adapids to extant strepsirrhines and omomyids to modern haplorhines, although they may be independent radiations from ancestral primates. In addition, middle Eocene fossil deposits in China have yielded early relatives of simians (e.g. Eosimias). For many years, the earliest known fossils reliably identified as simians all came from a single site in Egypt, the Fayum Depression, which also yielded adapids and omomyids. Increasingly, fossils with affinities to simians have also emerged from Asia, notably from late Eocene sites in Myanmar and Thailand. But these Asiatic fossils generally seem to be stem forms rather than members of the crown radiation of simians. The origins of the natural groups of extant primates have been increasingly documented in the fossil record, with one glaring exception: the Malagasy lemurs. Not a single fossil representative from the major adaptive radiation of lemurs is known prior to the recently extinct subfossils. By contrast, a few early fossil members of the sister group, the lorisiforms, have been found. For some considerable time, Miocene forms from Kenya dating back to about 20 mya were the earliest documented lorisiforms. However, new discoveries at the Fayum site extended the known age of this primate group back to the late Eocene, around 40 mya. In fact, the Fayum fossils include an early bushbaby along with a relative of lorises, so those two subgroups of lorisiforms had evidently already diverged. Hence, even without fossils from Madagascar, it can be concluded that lemurs and lorisiforms diverged more than 40 million years ago. On the haplorhine side of the primate tree, Chinese Middle Eocene fossil deposits have yielded a form so similar to modern tarsiers that it has been included as a species in the same genus — Tarsius eocaenus. As for simians, fossil relatives of extant groups are documented from the late Oligocene, about 30 mya. Relatives of New World monkeys have been discovered in South America, beginning in the latest Oligocene and extending through the Miocene. Early Miocene forms, such as Homunculus, seemingly have no direct relationship to extant lineages. In contrast, by the late Miocene it is possible to recognize members of individual families, including a fossil owl monkey. In the Old World, particularly in Africa, early Miocene deposits dating back to about 20 mya have yielded fossil relatives of both monkeys and apes. Direct fossil evidence for early human evolution is confined to Africa and potentially extends back about 7 mya to Sahelanthropus, represented by a single skull from Chad. Uncertainty surrounds the 6-million-year-old Kenyan fossil Orrorin, known only from some fragmentary long bones (suggesting some adaptation for bipedal locomotion) and a few teeth. Convincing evidence for early hominids dates back only about 4 mya to the australopithecines, starting with Australopithecus and later its robust relative Paranthropus. Strikingly, the earliest direct evidence for striding bipedalism is a footprint trail from Tanzania dating back to about 3.4 mya, predating the famous Lucy skeleton of Australopithecus afarensis (about 3.2 mya) from Ethiopia. Fossil evidence of the more advanced genus Homo first appears in Africa about 2.5 mya, which is also the date from which stone tools are documented. By 2 mya, Homo had expanded out of Africa, as is indicated by the 1.7-million-year-old Homo georgicus from Dmanisi in Georgia. One key shift in the early evolution of Homo may have been further refinement of bipedal locomotion to permit endurance running. For primarily land-living organisms such as mammals, geographical isolation can directly influence evolutionary divergence. Thus, the five geographically delimited ‘natural groups’ correspond to basic subdivisions within the primate evolutionary tree (Figure 2). Conclusions based on morphological evidence alone have been reinforced by findings from molecular comparisons, yielding a fairly clear consensus. All five ‘natural groups’ — lemurs, lorisiforms, tarsiers, New World monkeys, Old World monkeys with apes — are clearly monophyletic. That is to say, in every group all members descended from a distinct common ancestor that gave rise to no other extant species. The overall phylogenetic tree (Figure 2) also reveals that strepsirrhines and haplorhines both constitute higher-level monophyletic units. In other words, lemurs and lorisiforms are sister groups, while tarsiers are sister to simians. All lemurs and all lorisiforms belong to separate monophyletic groups. Among lorisiforms, it has also been shown that bushbabies (family Galagidae) and lorises and pottos (family Lorisidae) are also monophyletic. Simians, or higher primates, are similarly monophyletic — all monkeys, apes and humans are derived from a common ancestor. Simians, in turn, include two monophyletic groups: platyrrhines (New World monkeys) and catarrhines (Old World monkeys, apes and humans). And within catarrhines there is a further division between one monophyletic group containing Old World monkeys and another containing apes and humans. Among apes, the gibbons branched away first, while orangutans were the first great apes to diverge. Subsequently, the gorilla split off prior to the common ancestor that gave rise to chimpanzees and humans. It is also important to establish relationships between primates and other mammals, notably in order to identify their sister group. Primates are one of 18 extant orders of placental mammals. Although it is generally accepted that euprimates are monophyletic, persistent uncertainty has surrounded relationships with other mammals, notably tree-shrews. Originally classified as insectivores, tree-shrews were included in Primates by Simpson but are now generally allocated to their own order Scandentia. Yet, regardless of classification, it has been widely accepted that, among extant mammals, tree-shrews are the closest relatives of primates. Many authors have inferred that tree-shrews share several derived features with primates, but those may be interpreted instead either as primitive retentions or as results of convergent evolution for arboreal life. Broadly-based molecular phylogenies have yielded a fairly stable consensus interpretation of higher-level relationships among placental mammals (Figure 3). One notable outcome is recognition of four high-level clusters recognized as superorders. Unexpectedly, a cluster of endemic African mammals (Afrotheria) emerged, including aardvarks, certain insectivores, elephant-shrews, elephants, sirenians and hyraxes, but not primates, which had previously been seen as a group with African origins. The second cluster (Euarchontoglires) contains colugos, primates and tree-shrews along with a sister group containing lagomorphs and rodents (Figure 4). The large third cluster, forming a superorder labelled Laurasiatheria, contains the remaining insectivores, bats, carnivores, pangolins, artiodactyls, cetaceans and perissodactyls. The fourth assemblage is quite small, being restricted to the single order Xenarthra containing armadillos, anteaters and sloths.Figure 4Inferred relationships within the mammalian superorder Euarchontoglires.Show full captionSolid lines indicate branching indicated by a supertree integrating molecular data. Dashed lines with question marks indicate possible alternative links. A basal split between Euarchonta and Glires is often recognized, but some molecular evidence indicates a link between tree-shrews (Scandentia) and lagomorphs. Within Euarchonta, colugos (Dermoptera) have been linked either to tree-shrews or to primates. Molecular evidence has generally provided little support for any specific connection between tree-shrews and primates.View Large Image Figure ViewerDownload Hi-res image Download (PPT) Solid lines indicate branching indicated by a supertree integrating molecular data. Dashed lines with question marks indicate possible alternative links. A basal split between Euarchonta and Glires is often recognized, but some molecular evidence indicates a link between tree-shrews (Scandentia) and lagomorphs. Within Euarchonta, colugos (Dermoptera) have been linked either to tree-shrews or to primates. Molecular evidence has generally provided little support for any specific connection between tree-shrews and primates. Molecular evidence indicates that Euarchontoglires is monophyletic, but the relationships among its five constituent orders — in particular, between colugos, primates and tree-shrews — have not been clearly resolved (Figure 4). A few studies have identified tree-shrews as the sister group of primates, but the majority have indicated that colugos and primates are sister groups. This would be a revolutionary finding as morphologists had never thought that colugos might be more closely related to primates than tree-shrews. Overall, molecular evidence favours a sister-group relationship between colugos and primates, while relationships of tree-shrews remain unclear. Extant primates, excluding tree-shrews, constitute a well-defined order of mammals with a patchy fossil record extending back to the earliest Eocene. Undisputed fossils documenting their earlier evolution have yet to be found. It now seems that, among extant mammals, the little-studied gliding colugos (Dermoptera) may be the sister group of primates. The implications of this relatively new finding, based on molecular evidence, have barely been explored. Within primates, a basal divergence between strepsirrhines (lemurs and lorisiforms) and haplorhines (tarsiers and simians) is now widely recognized. This means that the tarsiers are of special interest for attempts to reconstruct the early stages of primate evolution. Overall, the well-resolved evolutionary trees now available provide us with a more reliable basis for interpreting the special case of human evolution.