The influence of bipedal postural behaviour on the human skeleton

Bipedalism is a locomotory mode whereby an organism moves within an environment on two legs. Humans are unique amongst the extant primates in being obligate bipeds [Harcourt-Smith & Aiello 2004] but are postulated to have evolved from an arboreal, quadrupedal, knuckle-walking ancestor [Richmond et al. 2001; Schmitt 2003; Sockol et al. 2007; Thorpe et al. 2007]. The transition within the human lineage towards bipedality has been accompanied by the accumulation of a multitude of adaptive musculoskeletal traits. The majority of these traits are post-cranial in that they manifest inferior to the head in a fully erect posture. This suite of adaptations includes direct evolutionary modifications to the weight-bearing structures: the vertebral column, the pelvis, the lower limb and the foot. Other indirect modifications for example in the upper limb, present as a result of our abandoning of arboreal climbing, will also be discussed. An examination of these characters exhibited in modern humans will be compared and contrasted with corresponding character states in extant and fossil apes. Evidence will come from morphological and developmental studies of modern humans, Great Apes, fossil hominins such as Ardipithecus and Australopithecus & the remarkably informative fossil apes Dryopithecus and Oreopithecus.

Vertebral column

Given the effects of gravity, the maintenance of bipedal posture requires an effective transmission of the upper body weight from the trunk, through the pelvic girdle to the lower limbs. In humans the centre of mass (COM) lies centrally and directly vertical above the hips, thus the upper body weight is absorbed at the foot of the vertebral column. Therefore we expect to see weight-bearing adaptations in this region of the back. One such adaptation is known as a lumbar lordosis, a posterior concavity of the vertebral column in the lumbar region. Dorsal wedging of the L1-L5 vertebrae creates a curvature in the lower spine that, much like a spring, helps absorb body weight and allows flexion & extension of the trunk. The angle created is typically 30° but can reach 50° in a pregnant female [Whitcome et al. 2007]. Lovejoy [2005] describes this feature as ‘uniquely human’ however analyses of the Upper Miocene hominoid Oreopithecus bambolii and Australopithecus afarensis suggest that they too possessed lordoses indicative of bipedal posture [Köhler & Moyà-Solà 1997; Sanders, 1998]. Extant Great Ape vertebral columns lack lumbar lordoses and are therefore restricted in their lower back mobility (Figure 1). Further, the lumbosacral angle in humans averages 60°, almost double that seen in the Great Apes [Aiello & Dean, 1990]. Again this illustrates how lower back flexibility is essential for cushioning the impacts of walking or running.

Lordosis

Figure 1. Blue highlighted lumbar regions of a modern human (left) and chimpanzee (right). The lordotic human curvature allows lower back flexibility in contrast with the ape’s rigid condition. Arrows indicate centre of mass/gravitational direction. Source: Adapted from Whitcome et al, 2007.

Other weight-loading adaptations in the lower spine include the lengthening and thickening of the lumbar region. Humans usually possess 5 lumbar vertebrae with progressively widening zygapophyses [Lovejoy 2005]. This contrasts with chimpanzees who have between 3 and 4 lumbar segments with narrowing facets. In addition, continuing caudally along the column, human vertebral bodies become larger in overall size [Hauesler et al. 2002].

Pelvis

The human pelvis has undergone significant remodelling in order to maximise the efficiency of bipedal locomotion. Compared to the chimpanzee pelvis, the human version is considerably shorter and broader (Figure 2). This has had the effect of distancing the thorax from the ilium and freeing the lumbar region from within the pelvis [Lovejoy 2005]. Consequently the human lower back is capable of a greater range of movement than a Great Ape’s. This alteration has also brought into close proximity the sacroiliac and hip joints, reducing force transmission stress on the ilium [Aiello & Dean 1990].

Joint surface sizes are skeletal indicators of bipedalism because they are proportional to the quantity of force passing through them [Aiello & Dean, 1990]. It follows that the lower limb joints of a human are larger relative to body size than other apes because of the body weight they perpetually support in bipedal stance [Jungers, 1988]. The auricular surface of a human hip for example is comparable to a gorilla’s of twice the body weight [Schultz, 1961].

Pelvis

Figure 2. Anterior pelvic view of a) chimpanzee, b) Australopithecus afarensis Al-288-1, c) Homo sapiens female and d) Homo sapiens male. Note the tall and narrow chimpanzee ilium in contrast to the short and broad human condition. The Australopithecine pelvis showcases a transitional morphology with extreme lateral iliac flare. The broadened human sacrum frees the lumbar region which is sunken rigid within the chimpanzee hip.   Source: Lovejoy, 2005.

Other modifications to the human pelvis have repositioned muscle attachment sites relative to those seen in the apes. Humans have an expanded, anteriorly-projecting iliac blade with respect to the ischium unlike the chimpanzee’s whose is more aligned. The resulting hip structure facilitates a reorganisation of gluteal musculature without compromising the hamstring lever arm [Sockol et al 2007]. Whereas in apes the gluteals function as extensors of the thigh at the hip joint, in humans they primarily assist in abduction thanks to their more anterior origins [Aiello & Dean 1990].

A broader human sacrum and an expanded posterior superior iliac spine greatly improve the surface attachment and lever advantages of the posture-maintaining erector spinae muscle group. Significantly, the prominent human anterior inferior iliac spine (which provides attachment for the knee-extending rectus femoris muscle and the trunk-balancing iliofemoral ligament) is absent or reduced in apes [Aiello & Dean 1990].

A shift towards the human pelvic condition is documented in fossils of A. afarensis such as Al 288-1, better known as ‘Lucy’. Superiorly Lucy’s hip showcases adaptations to a bipedal gait including a broad sacrum, a widened interacetabular distance and pronounced lateral iliac flare [Berge 1994]. Unlike in humans though, Lucy’s hip was subject to large rotatory movements as her gluteals did not function as stabilisers of the joint [Ward, 2002]. The human-like pattern of iliac cancellous bone in O. bambolii indicates that it too was probably a biped [Rook et al, 1999].

Femur

The femoral bicondylar angle is a classic feature that distinguishes bipedal humans from quadrupedal apes. In humans this angle averages 8-11° compared to 1-2° in the African apes. A larger bicondylar angle aligns the distal end of the femur, knee and lower leg with the body’s midline thus minimising the distance the body’s COM must be displaced in walking to lie directly over the stance leg [Aiello & Dean, 1990]. Interestingly, the biped A. afarensis exhibits a larger 12-15° angle perhaps as a consequence of its exceptionally broad pelvis (Figure 3).

Bicondylar angles

Figure 3. Femoral bicondylar angles in a) modern humans b) Australopithecus and c) chimpanzees. Source: Shefelbine et al, 2002.

Another noticeable difference between humans and great apes is found in limb proportions. Humans compared to apes have significantly longer lower limbs relative to upper limbs (Figure 4). Ruff [2003] finds that although human infants exhibit a characteristically adult femoral: humeral length ratio, their femoral: humeral shaft strength only increases following the adoption of bipedalism at the age of 1, hinting at a developmental response to stress. Tardieu [2010] illustrates how the tibio-femoral angle reverses in a juvenile from markedly abducted in a newborn to 6° adducted in a 6-7 year old.

Femoral - Humeral

Figure 4. Femoral to humeral length in 100 modern humans (open circles) and 100 non-human Catarrhines (filled squares). Humans consistently show greater femoral lengths and overlap only with leaping colobine monkeys. Source: Ruff, 2003.

Other osteological aspects of the femur betray bipedal locomotion. Some help to diagnose bipedalism in fossil hominins, for example the 6 million year-old proximal femur of Orrorin tugenensis [Richmond et al 2008]. Human features include a marked obturator externus groove indicating full hip extension of a habitual biped. An enlarged femoral head, a broader neck, a marked intertrochanteric line, a prominent gluteal tuberosity and a raised linea aspera are all evidence of greater weight-bearing abilities and enhanced lever arm attachments for muscles & ligaments in humans that help maintain upright posture. Such features are lacking or reduced in apes.

Knee

The enlarged, elliptical profile of a human’s distal femoral condyles (when viewed inferiorly) compared to the chimpanzee’s maximises tibial contact in extension of the knee joint, effectively distributing the weight load. Due to the differential length of the articular femoral condylar surfaces, human knees are capable of assuming a close-packed position in full extension whereby the femur rotates medially on the tibia. The structure of the cruciate ligaments and menisci within the chimpanzee knee do not permit this [Aiello & Dean, 1990]. Hence a human can stand stationary upright for long periods whereas a chimpanzee or bonobo must exhibit an unspecialised, bent hip-bent knee (BHBK) gait when walking bipedally [D’Août et al 2004]. Horizontally-angled tibial plateaus (when viewed medially) are characteristic of fully-extended modern human knees whereas continually flexed Great Ape knees tend to produce reclined angles in excess of 110° to the vertical.

Ankle & Foot

The plane of the tibiotalar (ankle) joint in humans is near perpendicular to the long axis of the tibia. This helps position the leg vertically to the foot which is advantageous to a biped as it provides stability in walking. An ape’s ankle joint is considerably more flexible and is characterised by a 20-35° tibiotalar angle [Aiello & Dean 1990].

A human foot exhibits multiple osteological features which are beneficial to bipedalism compared to the ape’s which is adapted for grasping (Table 1). The nature of the human calcaneus reflects its function in absorbing the force of heel strike in walking. The human metatarsal (MTS) robusticity pattern provides evidence of lateral to medial weight transfer across the foot. Strikingly the human hallux has been laterally rotated and adducted in humans to realign it with the other digits. This, combined with a greater robusticity, provides a sturdier platform and increases the power of toe push-off achieved by the strong flexor hallucis longus muscle. In apes the hallux is widely abducted and mobile due to a convex, medially facing MTS1 facet on the medial cuneiform. In addition, curved phalanges equipped with broad bases and flexor sheath ridges reflect the function of the ape’s foot in grasping.

Table 1

Human feet exhibit a unique longitudinal arch structure supported by (plantar and spring) ligaments & a well developed plantar aponeurosis. The thick aponeurosis absorbs 60% of the stress on the foot, cushioning it on ground contact. Enhanced plantar ligament attachments sites in humans provide greater stability to the foot which acts as a lever. The shared presence of an os peroneum facet (sesamoid bone of the peroneus longus muscle) on the cuboid of humans and Ardipithecus ramidus suggests that the p. longus tendon supports the longitudinal arch [Lovejoy et al, 2009]. Its general absence in apes is a pointer to greater foot flexibility. Wedged cuneiforms contribute to the transverse arch in humans and apes however only in the former do the metatarsal heads contact the substrate.

The functional interpretations of the famous Stw573 “Little Foot” Australopithecus africanus and OH8 Homo habilis feet are strongly debated due to their mosaic of human-ape features [Clarke & Tobias 1995; Kidd & Oxnard, 2005]. In contrast to humans, the fossil ape O. bambolii exhibits a more medial lever axis and abducted lateral metatarsals. However a near vertical calcaneal tuberosity and tall medial trochlea, unlike in Dryopithecus and extant apes, suggest a parallel tibial axis and COM as in humans [Köhler & Moyà-Solà 1997].

Foramen magnum

One cranial trait used to diagnose bipedality in fossil hominids is the position of the foramen magnum at the base of the skull. Humans possess an anterior location of the foramen magnum in contrast to a chimpanzee’s more posterior position relative to the bitympanic line. The human condition when viewed in norma basilaris helps position the vertebral column and body weight directly under the cranium. Brunet et al [2002] used this indicator to assign bipedality to the 6-7 million year old Sahelanthropus tchadensis type specimen, though their conclusions are hotly debated [Wolpoff et al. 2002].

Thorax and upper limb

Humans in contrast to the African apes have a barrel-shaped thorax containing 12 pairs of medio-laterally flattened ribs. This serves to centralise the axis of the body’s COM whilst the lack of a 13th rib pair increases lower trunk mobility. Arboreality in apes is associated with a more superiorly-oriented glenoid fossa. This permits a range of upper limb movements above the head for example suspension in the fossil ape Dryopithecus [Köhler & Moyà-Solà 1996]. In contrast, humans exhibit a more laterally-facing glenoid fossa; a derived trait assuming they had an arboreal last common ancestor (LCA). The human condition reflects how bipedalism has freed our upper limbs for use in an anterior position to manipulate objects.

Conclusions

In summary the evolution of habitual bipedalism in humans has been accompanied by numerous musculoskeletal modifications. Structures such as the pelvis, lower limb and foot have been remodelled to improve their weight-bearing abilities. Such remodelling has facilitated subtle alterations in the attachment sites and functioning of key postural muscles like the erector spinae group and important walking muscles like the gluteals. The hip, knee and ankle joints also document osteological and anatomical changes which betray a human’s obligatory locomotor mode. In contrast, extant apes such as the chimpanzee, with which we share a LCA, exhibit tell-tale adaptations to an arboreal lifestyle in their corresponding character states. Some traits shared between humans and fossil hominids like O. tugenensis & A. afarensis could reflect shared ancestry. Other traits present in humans and fossil apes such as O. bambolii probably reflect homoplasy or convergent evolution.

Biogeography and the origin and evolution of specific primate lineages

Primates are an order of mammals that have distinctive features such as a clavicle, grasping hands, nails and stereoscopic vision. Today primates number ~400 species and have a predominantly tropical distribution [Nystrom & Ashmore, 2008]. Primates group consistently alongside the tree shrews (Scandentia) and colugos (Dermoptera) within the mammalian superorder Archonta [Adkins & Honeycutt, 1991; Murphy et al, 2001; Bloch et al, 2007; Janecka et al, 2007]. The balance of evidence suggests primates are a monophyletic clade [Schmitz et al, 2002; Poux & Douzery, 2004] though some studies suggest paraphyly [Arnason et al, 2002].

Undisputed early primates, termed ‘euprimates’, first appear in the fossil record around 55-60 million years ago (Ma) in the Palaeocene epoch of the Tertiary. However, molecular studies estimate a Cretaceous origin for the primates of at minimum 80Ma and possibly as early as 110Ma [Kumar & Hedges, 1998; Tavaré et al, 2002; Arnason et al, 2002; Murphy et al, 2007]. This discordance has been well documented [Steiper & Young, 2008]. The relationship of euprimates with the extant strepsirrhine and haplorhine lineages has been extensively debated. Plesiadapiformes, an order of extinct insectivorous Palaeocene mammals, are thought to be closely related to the euprimates, possibly containing the last common ancestor (LCA) of all primates [Silcox, 2001; Bloch & Boyer, 02; Silcox et al, 2007]. Later adaptive radiations of primates created modern day groups such as the platyrrhines & catarrhines which contain the anthropoids and cercopithecoids. At the time of the earliest accepted fossil primates the configuration of the earth’s continents was different to today [Scotese, 2000]. This has promoted considerable deliberation over the lemur colonisation of Madagascar and how and when the platyrrhines reached the new world.

This essay will examine the origins and evolution of specific lineages including the problematic tarsiers and the nature of the plesiadapids. Phylogenetic relationships between the major clades of extant and extinct primates will be explored in an attempt to determine ancestry. The issue of how or whether primates can cross large water bodies will also be addressed. First and foremost, the biogeographical context of primate evolution will be investigated.

Biogeography

During the late Cretaceous ~94Ma, when primates are hypothesised to have split from other placental mammals, the continental make-up of the earth was different to today. Laurasia and Gondwana, the two constituents of the supercontinent Pangaea, had split to conceive most recognisable land masses (Figure 1). South America was separate from North America and had a continuous connection with Australia in the southern hemisphere via Antarctica. Africa had fragmented from South America and was migrating towards its present day position. India and Madagascar were a conjoined island, east of Africa. Eurasia was detached from Africa and contacted North America at the Asian-Alaskan land bridge [Scotese, 2000].

 Cretaceous

Figure 1. A palaeomap containing projections of the earth’s continents during the late Cretaceous, 94 million years ago. Source: Scotese, 2000.

Soon after 90Ma India broke free from Madagascar [Briggs, 2003]. Progressing into the Eocene ~50Ma and the Indian subcontinent collided with Asia causing Himalayan uplift. Australia had begun detaching from Antarctica and was headed northwards. Africa had attained its current position accompanied by the widening of the Atlantic Ocean. Approximately 27Ma South America and Antarctica split opening the Drake Passage [Barker, 1991]. By the middle Miocene ~14Ma the continental positions resembled modern day earth though much of Eurasia remained flooded due to high sea levels.

In climatic terms the Eocene was characterised by tropical conditions and an average temperature of 30°C. During this epoch ‘alligators swam in swamps near the North Pole’ according to Scotese [2000]. Moving into the Oligocene and temperatures dropped sharply to a cool ≤10°C resulting in an increased seasonality and the formation of a southern polar ice cap. The Miocene witnessed a slight recovery in overall warmth before temperatures dropped to today’s average of 10°C.

Plesiadapids

The plesiadapids were a successful order of insectivorous mammals that lived in the Palaeocene [Nystrom & Ashmore, 2008]. Research over the last 15 years has solidified their close relationship with the euprimates. An analysis of dental characters confirms the sister clade relationship of the two groups [Silcox, 2001]. Another shared trait called a petrosal bulla closely unites the two orders [Nystrom & Ashmore, 2008]. In their description of the plesiadapid Carpolestes simpsonii, Bloch and Boyer [2002] frank the above conclusions. C. Simpsonii dates to 55Ma hence was a contemporary of the earliest euprimates. In common with the euprimates C. Simpsonii possessed an abducted hallux complete with a nail and long proximal hand phalanges. These features convey efficiency of arboreal grasping, an integral primate trait. However C. simpsonii lacked other intrinsic primate features such as orbital convergence and leaping adaptations. Cladistical analysis supports the position of plesiadapids as sister group to the euprimates (Figure 2). Further, Bloch et al [2007] nest both groups within the primates in a large clade called the euprimateformes.

Euprimate phylogeny

Figure 2. Phylogenetic tree displaying the relationships amongst the Archonta. Note how euprimates and plesiadapiformes are sister clades. The position of Carpolestes simpsonii suggests a closer affinity than previously assumed. Source: Bloch and Boyer, 2002.

Whether the early plesiadapids contained the LCA of the euprimates is a matter of debate. Regardless, their close affinity to basal primates and their importance in their evolution are indisputable. According to Bloch and Boyer [2002] they are best considered as ‘primates not closely related to the flying lemurs (Dermopterans)’. Whether the traits shared by the plesiadapids and the euprimates are parallelisms or plesiomorphs has no bearing on the origin of the primates which was almost certainly prior to the pre K-T boundary.

Euprimates

The euprimates are the first accepted fossils of ‘true’ primates that appear in the fossil record in the late Palaeocene some 55Ma with the discovery of Altiatlatius [Godinot, 1994; Tabuce et al, 2004]. Euprimates are typically divided into two groups called the adapids and omomyids. Combined, the adapids and omomyids comprise five speciose families that were geographically distributed across North America, Eurasia and Africa during the aforementioned warm Eocene. Their demise coincides with the cooling phase that characterised the late Eocene-Oligocene transition. Despite this, particular groups such as the Sivaladapid family resided in a so-called Asian refugium until as late as the Miocene [Ciochon & Gunnell, 2002].

The euprimates are a case study in mosaic evolution for they share some characters but differ in others. For example both adapids and omomyids exhibit postorbital bars, a petrosal bulla in their ears, opposable digits equipped with nails and relatively large skulls with unfused metopic sutures. In contrast the two groups differ in their dental traits and the bony structure of their inner ear. Overall adapids tend to exceed 1kg whereas omomyids are usually less than 400g [Franzen et al, 2009; Williams et al, 2010]. Early forms of both groups bear such resemblance that it is implausible to reject theories of shared ancestry [Gingerich, 1986; Rose, 1995]. Over evolutionary time both groups become more derived particularly in their dentition [Nystrom & Ashmore, 2008].

 Primate phylogeny

Figure 3. Phylogenetic tree displaying potential relationships of the euprimates to extant primate lineages. The extant strepsirrhine crown clade is borne out of the adapids whereas the omomyids and extant strepsirrhines share a common ancestor. Source: Williams et al, 2010.

The origins of the euprimates have already been discussed above with respect to the plesiadapids. Their relationship with extant primate taxa is equally sketchy. To summarise the positions of the adapids and omomyids within the primates Williams et al [2010] present the phylogenetic tree seen in Figure 3. Classically the adapids are hypothesised to be more closely related to the living strepsirrhine clade because of a few shared features like an ectotympanic ring. However, their lack of a toothcomb suggests no special relationship between the two groups [Miller et al, 2005]. As will be seen later, the current consensus is that omomyids are a sister group to the anthropoids within the haplorrhine lineage [Bajpai et al, 2008].

Conversely, when describing the middle Eocene adapid Darwinius masillae, Franzen et al [2008] infer a haplorrhine-like status on the basis of primitive and derived character states. The absence of a toothcomb and grooming claw are cited as reasons for rejecting D. masillae simply as a fossil lemur. The near-complete specimen, better-known as ‘Ida, was found in the Messel Pit in Germany and dates to 55Ma when Eurasia experienced a paratropical climate.

Quite as to where the euprimates originated is another topic open for discussion due to the paucity of the fossil record. Given the majority distribution of euprimate fossil sites across North America and Eurasia one might be tempted to predict a northern hemispherical origin [Martin et al, 2007]. However, the occurrence of African euprimates such as Altiatlatius and Algeripithecus [Godinot & Mahboubi, 1992] negate this theory as Africa was an isolated continent during the Eocene. Hence unless the euprimates had an unforeseen deep origin when all the landmasses were last connected, ocean crossings must be envisaged.

Strepsirrhines

Strepsirrhines are the ‘wet-nosed’ primates comprising the lemurs, lorises and bushbabies. The strepsirrhines are one of two extant suborders of primates along with the ‘dry-nosed’ haplorrhines. Tavaré et al, [2002] estimated the LCA of extant primates, or the divergence date between the strepsirrhines and haplorrhines, as 81·5Ma. Therefore, in accord with the molecular data, the strepsirrhine-haplorrhine split must have occurred early in the evolutionary history of primates.

Studies support an early dichotomy within the strepsirrhines ~46-62Ma of the lorisiformes and lemuriformes [Yoder et al, 1996; Poux & Douzery, 2004]. The discovery in 2001 of two fossils from the Fayum Depression in Egypt confirms the antiquity of the crown strepsirrhine split [Seiffert et al, 2003]. The fossils, one loris and one galago, date to the middle Eocene 37-41Ma. In common with all extant strepsirrhines except the enigmatic aye aye Daubentonia the loris Karanisia possessed a toothcomb. In the knowledge that Daubentonia diverged from crown strepsirrhines prior to the loris-galago split, the evidence points towards a middle Eocene lemur colonisation of Madagascar at latest. Despite this, only recent subfossils of lemurs have ever been identified, disregarding the contentious Bugtilemur from the Oligocene of Pakistan [Martin, 1990; Marivaux et al, 2001]. Thus a mysteriously long ghost lineage for lemurs must exist. Biogeographically speaking, the Fayum fossils boost support for an Afro-Arabian origin of the crown strepsirrhines which is consistent with today’s distribution of extant forms across Africa and Asia.

Haplorhines

Poux and Douzery [2004] estimate the haplorrhine crown group divergence at 57Ma. Haplorrhines are characterised by their bilophodont tooth pattern, enclosed orbits and fused frontal bones. Their fused mandibular symphses, a feature shared with later adapids, could be a potential homoplasy or a potential link to ancestry. Given that basal haplorrhines coexisted with euprimates in the Eocene, ancestral ties seem unlikely [Nystrom & Ashmore, 2008]. Early haplorrhines belonging to the Fayum of Africa constitute 15 genera of parapithecids, proteopithecids, oligopithecids and proplipithecids [Williams et al, 2010]. Certain cranial features of parapithecids implicate an affinity with the New World Monkeys (platyrrhines) which will be examined later. Oligopithecids are candidates for stem catarrhines because of their dental formula 2.1.2.3.

Traditionally Africa was considered the cradle of the anthropoids (haplorrhines excluding tarsiers) with a rich fossil fauna dating to ~37Ma. Seiffert et al, [2005] describe Biretia and make connections with the more ancient 45Ma Algeripithecus. In recent years though an Asian origin has gained popularity due to multiple discoveries of earlier anthropoids across the continent. Beard et al, [2004] cued a change in thinking when presenting Eosimias to the world. Eosimias dates to ~45Ma. Most authors now accept that Eosimias is not a direct relative of the African anthropoids and is instead closer related to other Asian types [Gunnell and Miller, 2001]. Bajpai et al [2008] further extended the history of Asian anthropoids when reporting the discovery of Anthrasimias, an early Eocene anthropoid that lived ~55Ma in India. The coexistence of Anthrasimias with adapids and omomyids in India effectively rules out an anthropoid origin from within these groups. Moreover, a phylogenetic analysis implicates the omomyids as a sister group to the Eosimiidae which contain Anthrasimias (Figure 4). Interestingly the authors’ results have Altiatlatius as an eosimid anthropoid rather than a euprimate as previously considered.

Myanmar has also proved keystone locality for Eocene anthropoid finds over the years including Amphipithecus [Ciochon and Gunnell, 2001]. The discovery of the 37 million year-old Afrasia specimen has shed light on the dispersal of Asian anthropoids into Africa [Chaimanee et al, 2012]. Morphological similarities in the molar dentition of Afrasia and the contemporaneous African haplorrhine Afrotarsius suggest a sister taxon relationship. Hence the tarsiers may represent an early offshoot of basal haplorrhines that have a shared, deep ancestry with the anthropoids. The close affinity of Asian and African anthropoids is also noted by Ducrocq et al, [1995] who liken the Upper Eocene Wailekia found in Thailand to Oligopithecus from the Fayum.

Primate phylogeny 2

Figure 4. Phylogram displaying the sister relationship between the omomyid ‘euprimates’ and the extant haplorrhines containing the ancient tarsier lineage. The placement Anthrasimias extends the anthropoid lineage by some 10 million years. Source: Bajpai et al, 2008.

Thus the evidence weighs heavily in the favour of an Asian origin for the anthropoids with subsequent migrations into Africa (Figure 5). The Indo-Madagascan [Krausse & Maas, 1990] and Paratethyan [Rasmussen, 1994] theories have also been proposed. Although both theories are compatible with molecular data, they are circumstantial and lack substantiation from the fossil record [Miller et al, 2005; Nystrom & Ashmore, 2008].

Anthropoid migration

Figure 5. Global map illustrating two potential migratory routes for the Asian anthropoids into Africa during the Palaeocene. Land shaded grey was hypothetically exposed at the time, land coloured white was submerged, thus an ocean crossing may have been necessary. The phylogenetic tree on left demonstrates relationships between strepsirrhines and the basal haplorrhines. Source: Miller et al, 2005.

Platyrrhines

Comparing mitochondrial genomes of extant primates, Schrago and Russo [2003] time a late Eocene split between platyrrhines and catarrhines at 35Ma. Estimations vary wildly though. Arnason et al, [1998] for example predicted a divergence closer to 70Ma. Africa remains the widely accepted yet unproven hypothesis for the origin of the platyrrhines. How they came to be distributed across the new world is discussed later.

Schrago and Russo’s minimum divergence date of 27Ma closely corresponds to the age of Branisella boliviana, the oldest New World Monkey fossil described by Hofftstetter [1969]. Branisella retained many primitive traits and does not closely resemble modern platyrrhines though it does exhibit the necessary platyrrhine dental formula [Takai et al, 2000; Nystrom & Ashmore, 2008]. In support of the African origin hypothesis is one important trait displayed in both the parapithecids and platyrrhines: cranial articulation between the sphenoid and parietal. Conversely, the temporal and frontal bones contact in catarrhines. Resemblances between Branisella and the African anthropoids from late Eocene Fayum deposits cannot be confirmed phylogenetically [Kay et al, 2008]. Morphologically modern monkeys similar to the extant genera Saimiri and Aotus appear only 12-14Ma in Columbia [Fragaszy et al, 2004; Rosenberger et al, 2008].

Catarrhines

The early Oligocene saw the evolution of the basal catarrhines from within the anthropoids in Afro-Arabia [Nystrom & Ashmore, 2008]. As already noted, the dental formula of oligopithecids highlights them as potential forebears of the catarrhines. Propliopithecids, perhaps descendants of oligopithecids, are documented in fossils of the famed Aegyptopithecus. By the late Oligocene we begin to see basal apes in the fossil record, in accordance with molecular evidence which predicts a hominoid-cercopithecoid split around 25-30Ma [Kumar & Hedges, 1998; Schrago & Russo, 2003]. Defining ape characteristics such as the classic Y-5 molar cusp pattern are first seen in the quadrupedal Proconsul. Another evolutionary feature is their increased brain size.

The onset of the Miocene signalled the heyday of the ‘true’ apes whence they diversified and distributed widely across Africa and Eurasia. Their adaptive radiation may in part have been coincident with or consequent of a warm recovery in global temperature. Their dispersal into Eurasia was facilitated by a landbridge between the continents [Scotese, 2000]. In Africa resided Afropithecus and Kenyapithecus. The suspensor Dryopithecus and peculiar biped Oreopithecus could be found in Europe [Moyà-Solà & Köhler, 1996; Köhler & Moyà-Solà, 1997; Rook et al, 1999; Kordos & Begun, 2001] whilst in Asia lived the massive Gigantopithecus and the Sivapithecus lineage of which orangutans may represent relicts [Cameron, 1997]. The late Miocene witnessed an extinction of apes in Europe leaving today’s solely tropical distribution.

Cercopithecoids, which contain the African and Asian monkeys, have a patchy fossil record. Their first appearance in the in the early Miocene is marked by basal forms like Victoriapithecus, currently believed to be a sister taxon to extant forms [Benefit, 1999]. Their evolution is punctuated by a long gap that fails to document the split between ‘cheek-pouched’ cercopithecines and ‘leaf-eating’ colobines around 12Ma. Following this division, and on the reappearance of fossils in the late Miocene, the cercopithecoids have spread across Eurasia much like the apes. Macaques remained in Europe until only a few hundred thousand years before present. Global cooling, as it did for the apes in the late Miocene, probably accounted for the final extirpation of monkeys from Eurasia [Nystrom & Ashmore, 2008].

Palaeogeography

Figure 6. Conformation of the earth’s southern continents 40 million years ago. The potential landbridge between Antarctica and South America may have facilitated faunal exchange, though the lack of fossil primates on Antarctica rules out this potential route for platyrrhine into the new world. Sites of mammal fossils including the early Asian anthropoids are annotated on. Source: Houle, 1999.

Ocean crossings

The occurrence of platyrrhines in South America and lemurs in Madagascar poses problems to the accepted origins theories: how did they get there? To explain the plight of the platyrrhines Houle [2009] examined one hypothesis whereby protoplatyrrhines, conceived in Asia or Africa, could have utilised a land corridor connecting Antarctica to Patagonia that existed until the late Eocene (Figure 6). The theory is rejected on the basis of a damning lack of primate fossils in Antarctica.

The authors also investigated the African origins hypothesis with regards to palaeowinds, sea currents and the floating island model. They postulate that a trans-Atlantic ocean crossing could have been achieved in 7-10 days in the Eocene ~40Ma, or 11-15 days in the Oligocene ~30Ma. Platyrrhines, Houle argues, were physiologically preadapted to cope with water deprivation. The fact that a contemporaneous rodent similarly of African ancestry undertook such a route is supportive [Wyss et al, 1993; Mouchaty et al, 2001; Schrago and Russo, 2003].

More clear is how lemurs reached Madagascar. Phylogenetically lemurs and lorises share a common African ancestor hence it’s parsimonious that the former colonised Madagascar via an African route [Yoder et al, 1996]. Molecular data suggests that lemurs colonised on Madagascar 50-60 Ma (Figure 7); compliant with the earliest dates for their intra-strepsirrhine divergence with lorisiformes. This postdates the Indo-Madagascan split ~60-88Ma [Crottini et al, 2012].

Two age-old hypotheses compete to account for the lemurs spread to Madagascar: the ‘rafting’ hypothesis and the ‘stepping-stone’ hypothesis. The rafting hypothesis stipulates that a group of lemurs were inadvertently swept across the Mozambique Channel on some form of vegetation raft. Favourable Palaeogene ocean currents directed from Tanzania to Madagascar could have facilitated such a migration [Ali and Huber, 2010; Samonds et al, 2012]. The region is also a known epicentre for cyclonic activity – a prerequisite for the creation of floating vegetation. Field observations of metabolically-inactive dwarf lemurs provide analogues for the survival of rafting organisms [Kappeler, 2001]. The stepping-stone hypothesis counters the rafting hypothesis, instead implicating a sub-aerially exposed landmass such as the Davie Ridge as an ancient corridor for animal dispersal from mainland Africa [McCall, 1997]. The theory has received some support [Tattersall, 2006] although the observed low mammalian diversity on Madagascar is the downfall (Simpson, 1940; Krause, 2010).

Lemur Madagascar

Figure 7. Molecular timings of the route into Madagascar of the four represented mammalian clades. Accordingly, lemurs arrived first in the Palaeocene probably via a raft of vegetation and fortuitous currents in the Mozambique Channel which have since reversed. Source: Krause, 2010. 

In contrast, Heads [2010] is in direct opposition to both the platyrrhine and lemur colonisations of South America and Madagascar. Instead he proposes a vicariant scenario for the attainment of their current distributions. On the basis of tectonic data, he calculates an ancient strepsirrhine divergence of ~160Ma and a platyrrhine-catarrhine split between ~120-130Ma. These estimates eliminate the need for ocean crossings due to the conformation of Gondwana during the Jurassic period [Scotese, 2000]. Although a neat explanation, such dates would imply extensive (~100 million year) ghost lineages exist for all primate groups which seems highly implausible [Krause, 2010]. What’s more it disagrees with all available molecular data.

Conclusion

In summary, our knowledge of primate evolution remains murky. Discordance exists between molecular evidence which strongly suggests a Cretaceous origin of primates, and palaeontological evidence which only extends to the Palaeocene. What we do know is thus. Early euprimates shared traits with plesiadapid mammals though this may be due to convergence. Two groups of euprimates, adapids and omomyids, coexisted with anthropoids in the Eocene of Asia. Adapids probably gave rise to the strepsirrhine crown group whereas omomyids are a probable sister taxon to the anthropoids. The platyrrhine-catarrhine split likely followed the migration of anthropoids into Africa. Hominoids and cercopithecoids, who diverge around 25Ma, have a patchy fossil record. A trans-Atlantic voyage is the most parsimonious explanation for the occurrence of platyrrhines in South America. Similarly, the colonisation of Madagascar by the lemurs was probably achieved via a raft of vegetation fortuitously swept across the Mozambique Channel.

Paranthropus in pictures

I can’t quite tell you exactly how much time I put into the following sketches of Paranthropus casts. All I can say is that when I snapped out of the trance and took a step back – I was pleasantly surprised!

Pictorial 1. Sketch of KNM-ER 406, Paranthropus boisei in norma frontalis with annotated osteological landmarks. Note the broad facial region, prominent sagittal crest and wide zygomatic arches.

Pictorial 1. Sketch of KNM-ER 406, Paranthropus boisei in norma frontalis (frontal view) with annotated osteological landmarks. Note the broad facial region, prominent sagittal crest and wide zygomatic arches.

Pictorial S1. Norma lateralis (right side) of KNM-ER 406 cranium, Paranthropus boisei. Relevant anatomical landmarks are annotated. Note the temporal overlapping on the parietal bone at the squamosal suture.

Picture 2. Norma lateralis (right side) of the KNM-ER 406 cranium, Paranthropus boisei. Relevant anatomical landmarks are annotated. Note the temporal overlapping on the parietal bone at the squamosal suture.

The above helped to illustrate my otherwise text-heavy Hominid Palaeontology lab book during my MSc in Palaeoanthropology. The opportunity to handle the casts and to combine artistry with science was just one of the many reasons why I thoroughly enjoyed the course.

Essay Season is here!

Having recently published one piece of my Masters’ coursework on this blog, the time feels right to share the other fruits of my intensive one-year taught programme! What use, after all, is my work when it simply resides on the hard-drive of my laptop? Better surely to bring it to light like a long-buried hominin fossil?!

As such, the coming days on The Human Story will be characterised by a number of 3000-word postings that constitute the essays, reports and critiques that I completed during my MSc in Palaeoanthropology at the University of Sheffield. Each is the product of two or more week’s hard graft spent toiling through pulse-racing primary literature!

The first article in the series was produced for a module entitled Evolutionary Primatology. This review paper examines the evolution of the primates (including specific lineages) amidst the ever-changing structure of the earth’s land masses and continents aka biogeography.

Bipedalism (the ability to walk on two feet) is the focus of the second installment which acted as a critical component to another module, Human Osteology. This essay looks in closer detail at the human skeleton to identify the evolutionary signatures of our upright stance and posture. Using the Great Apes and extinct hominins as comparative specimens, the nature of the musculoskeletal (muscular and skeletal) changes that occurred during human evolution is revealed.

Beware readers and prospective Palaeo’ students – correctly cite the above content and for personal use only! I have posted these articles as a good gesture. They should be used as reference material for obtaining background information. As a guide, citing any works published on a blog looks decidedly dodgy on any piece of post A-level, university work. Even a mildly competent plagiarising screen will discover your copy and pasting naughtiness.

My first publication: Getting out of “Out of Africa”

It gives me great pleasure to announce, to any straying soul or regular visitor of my blog, that my first ever paper has been published (!) in the Sheffield Graduate Journal of Archaeology: assemblage.

My review article constitutes a re-examination of the Out of Africa theory in light of the growing body of genetics papers that contest the model’s key assumptions.

To shed a little light on the rigours of peer-reviewing, assemblage operate a “double-blind” process whereby the reviewer and author are unknown to one another. Peer-reviewing is a notoriously lengthy process and admittedly there were frustrating times, during the wait, when new publications outdated some of my assertions and references. My advice to budding researchers is simple: keep the faith. If your article is good enough, only minor revisions will be necessary and publication will swiftly follow.

My gratitude goes whole-heartedly to the outgoing assemblage editorial team, who without their sterling work this publication would never have happened. Thank you!

The contents of Issue 13 containing my paper’s abstract and author biography can be accessed here: http://www.assemblage.group.shef.ac.uk/journal/issue-13

My paper itself is freely downloadable, courtesy of assemblage‘s admirable open-access policy at the following link: http://www.assemblage.group.shef.ac.uk/pdfs/issue13/KENDRICK%20Final.pdf

Please cite as follows: Kendrick, J.A. 2014. Rethinking Modern Human Origins: Getting out of Out of Africa. assemblage 13: 1-13

Double act at Dmanisi: evidence for two lineages?

Despite being a subscriber to the likes of Science Direct and Wiley Online Library for my Palaeo-related new release alerts, sometimes one still has to rely on more informal contacts for the necessary heads-up. And on this occasion I have my newly forged Google+ contacts Palaeontology Rocks and the wider Human Evolution community to thank for this latest blog posting.

Not a year has passed since the revelatory unearthing of Skull 5 at the famous Georgian fossil site of Dmanisi. The discovery received much coverage in the blogosphere, therefore please refer to the following sources (1, 2 and 3) for your better informed background information.

Jaw-droppingly different? Two of the mandibles recovered from the Dmanisi assemblage.

Prior to the finding, interpretations of the Dmanisi collection were at best as flaky as a Stone Age tool. Dated close to 1.8 million years ago (Ma), the original remains sported an odd “mosaic” of features. But were they suggestive of Homo erectus (“standing man”, the first to cook meat), Homo habilis (“handy man”, the first to make tools), or an altogether new species dubbed Homo georgicus (“Georgian man”, western Asia not southeast USA)? 

The discovery of Skull 5 (catalogued as D4500) was major in that it apparently unified the Dmanisi fossils with those of Homo habilis in Africa and Homo erectus in Asia. Rather than being separate species, all the fossils were most likely representative of a single evolving lineage. Our family tree it seemed was in need of a pruning…

Now to the new development. Published in PLoS One last week, a study of the Dmanisi jawbones (see photo) contests the above interpretations of Skull 5. Marked shape differences in the jaws, unrelated to the size or sex of the individual who chompsed with it, are present early in growth. This, according to the authors, is evidence of difference not similarity.

What’s more, the argument is supposedly strengthened by the uncertain dating of the earth at Dmanisi. Therefore, on the grounds of the uncertain ground and the developmental differences in mandibular (jawbone) morphology (shape), more than one lineage could well be represented at Dmanisi.

Source: Bermudez de Castro, JM. et al. 2014. On the variability of Dmanisi mandibles. PLoS One 9(2): e88212

Species special over at Evolutionary Anthropology

Despite my ill feelings recently directed towards the journal Evolutionary Anthropology, the quality of its content can never be called into question. Featuring esteemed Associate Editors such as Bernard Wood, Richard Klein and Curtis Marean under the stewardship of journal editor John Fleagle, rarely does an issue pass without an article of outstanding interest emerging.

The latest installment of Evo Anth, covering January and February 2014, is dedicated to the “species concept” theme. Fleagle hastily dispels my prematurely inferred notion that this is to mark the 155th anniversary of Charles Darwin’s On the Origin of Species in the opening editorial passage. Instead, it is explained that the special issue has been compiled to “generate a better understanding” of the observed increase in the number of primate species over the last few decades.

In 2012 a new species of slow loris was discovered in Borneo. Unique to the primates in that it possessed a venomous bite, the toxic topic of primate species numbers dominates the latest issue Evolutionary Anthropology.

The topic is a controversial one with speculation rife over the causes and implications of the “phenomenon” as Fleagle puts it. Multiple competing factors are likely to be at play including:

- the increased study of tropical environments

- a “need to increase species numbers to enhance conservation efforts”

- changing uses of species definitions

Equally, recent genetic studies have shed light on the fuzzy matter at hand. It transpires that species of primates (assumed to be distinct entities) are actually exchanging genes. In other words, they are getting up to monkey business! Strictly speaking this should not be happening. As a result, the number of primate species may actually be lower than current estimations.

As for the body of the issue, in a survey like manner, researchers in various fields were “asked” to offer their “personal and professional views on current issues in primate species identification”. As such, articles are abound with notably entries from the notorious species splitter Ian Tattersall and the more conservative Tim White. Volume 23, Issue 1 looks to be a classic which I look forward to examining in greater depth over the coming days.

Source: Fleagle, J.G. 2014. Identifying Primate Species. Evolutionary Anthropology 23: 1.