Verhaegen Human Evolution

It is traditionally believed that human ancestors evolved in a warm and dry environment. The available evidence, however, favours the vision that it happened in a warm and wet environment.

The paleo-environmental data suggest that the early australopithecines Australopithecus anamensis, afarensis and africanus lived in warm, moist, and wooded landscapes such as gallery forests. In the Pleistocene, the robust australopithecines A. robustus and boisei seem to have dwelt in more open, possibly cooler and generally dryer places, in the vicinity of shallow and relatively stagnant waters of lakesides, lagoons, marshes and riverbanks. Dental and microwear studies suggest that the australopithecines, more than Western lowland gorillas, regularly fed on aquatic herbaceous vegetation (AHV).

Homo fossils, on the other hand, as suggested by the paleo-environmental data, are more frequently discovered near lakes, seas and rivers where molluscs were abundant. Shellfish could provide a dietary supplement for their frugivorous diet. This is how early hominines might have learned to use stones to crack bivalves. This subsequently could have led to stone tool use for other purposes.

Key words

Hominids, australopithecines, enamel thickness, microwear, bipedalism, tool use, palaeo-environment, savanna theory

Introduction

The savanna hypothesis of human evolution was strongly promoted by Professor Dart in 1924 after the discovery of the skull of Taung in South Africa’s treeless grasslands. He wrote (1925):

‘South Africa, by providing a vast open country with occasional wooded belts and a relatively scarcity of water, together with a fierce and bitter mammalian competition, furnished a laboratory such as was essential to this penultimate phase of human evolution.’

And:

‘It will appear to many a remarkable fact that an ultra-simian and pre-human stock should be discovered, in the first place, at this extreme southern point in Africa, and, secondly, in Bechuanaland, for one does not associate with the present fringe of the Kalahari desert an environment favourable to higher primate life. It is generally believed by geologists (vide A. W. Rogers, "Post-Cretaceous Climates of South Africa," African Journal of Science, vol. xix., 1922) that the climate has fluctuated within exceedingly narrow limits in this country since Cretaceous times.’

While we now know that the South African climate did change since the time of Taung (Partridge, 1985), Dart was thus convinced that the present and the ancient environment did not differ significantly and that the Taung child had lived in such open grasslands. Dart only got recognition a few decades later. Piltdown Man (rather big brain and big teeth) was unmasked as a fraud and anthropologists accepted the Taung fossil (small brain, small teeth) as a more likely link between apes (small brain, big teeth) and humans (big brain, small teeth). However, they not only accepted Dart’s view on Taung’s affinity, but also his view on Taung’s lifestyle in a dry and open country. While many anthropologists today no longer automatically follow the savanna hypothesis (e.g. Tobias, 1995; Wood, 1996), the idea remains unquestioned in most popular books.

However, a savanna past of humans is comparatively and physiologically improbable, since humans in most respects differ from savanna-dwellers (e.g. Schmidt-Nielsen, 1979; Morgan, 1982, 1990; Verhaegen, 1991, 1997). In a comparison of humans with apes, arboreal, semi-aquatic, fully aquatic and savanna mammals (Verhaegen, 1993), not one feature distinguishing the savanna mammals was found in humans. Mammals of dry, warm and open landscapes are relatively independent of drinking-water and water-containing nourishment, have a high tolerance of dehydration and radiation heat, have high diurnal body temperatures and high daily temperature fluctuations, and high renal concentration power. They usually have very large external ears, a slender build, and running velocities of 30 miles per hour and more. They are unguli- or digitigrade, not plantigrade like opossums, bears, racoons, eared seals or African hominoids. Most of them do not have dextrous hands like racoons, many otters and primates. They never have abundant fat tissues under the skin like humans, but protect themselves from the sun with fur (or with dust coverings in elephants or rhinoceroses). Their vocalisations are less varied than those of dolphins, otters or primates are. They never copulate face to face as some slow branch-hangers (sloths, pottos, orang-utans), marine mammals (cetaceans, sirenians) and humans do. All have an excellent sense of smell, as opposed to many marine mammals and humans. Most of them grow up fast and reach adulthood in less than three years. They often sustain body temperatures of more than 40°C (Grant’s gazelle can maintain 46°C for many hours) and show temperature fluctuations of more than 6° between day and night. Their urine concentration can be twice that of humans and more. They can bear a dehydration of 20 per cent, whereas in humans a dehydration of more than 10 per cent is fatal without medical intervention. They are very conservative with salt and water (many savanna mammals, even carnivores like the fennec fox, do not need drinking-water), and they never sweat ten to fifteen litres a day as humans can do in hot environments (hunting-dogs and many other savanna-dwellers do not sweat at all).

Recently, anthropologists are appreciating these data: ‘physiologically, biochemically and histologically, we should be hopeless as savanna-dwellers. All of the former savanna supporters must swallow our earlier words’ (Tobias, 1995). Since humans differ strongly from such animals, a thorough reconsideration of the available fossil data is necessary. Our discussion will be mainly based on the paleo-environmental evidence and on the dental and microwear evidence of hominids.

Paleo-milieu

Not only the Taung cranium, but most hominid fossils - from a time span covering at least the last six million years - have been found in varied, but consistently wet environments: in humid forested areas or in the immediate proximity of abundant water collections at the time. However, there are the well-known difficulties of paleo-ecological reconstructions (Shipman & Harris, 1988): ‘taphonomic events […] may selectively destroy or distort the fossil record and the association among species’; animals ‘may stray out of their preferred habitats into other areas’; ‘habitats are often complex and mosaic’; ‘ecological zones or habitats [migrate] across basins in response to climatic and other fluctuations’; and, most importantly, ‘depositional variables […] bias the fossil record by sampling a disproportionate number of habitats related to water (e.g. lake margins, streams, channels, deltas) and by failing to sample many open-country habitats farther away from water sources’. Indeed, that many hominid fossils have been discovered in such places by no means proves that they actually lived there. However, it certainly does not exclude it.

The following list confirms the comparative evidence that it is rather improbable that the hominids ever lived in a savanna milieu, and provides a more shaded picture.

Lukeino KNM-LU 335 "pre-australopithecine": ‘The red beds seems to contain marginal lacustrine deposits as indicated by the presence of algal mats and lacustrine bivalves (including complete specimens with valves in the closed position)’ (Pickford, 1975).
Tabarin KNM-TH 13150 "pre-australopithecine": ‘The fauna includes aquatic animals such as molluscs, fish, turtles, crocodiles, and hippotami, along with others that might be found in the vicinity of a lake of river’ (Ward & Hill, 1987).
Ardipithecus ramidus: ‘Sedimentological, botanical and faunal evidence suggests a wooded habitat for the Aramis hominids […] Aquatic elements (turtle, fish, crocodile) are rare. Large mammals (hippopotamus, proboscideans, rhinos, equids, giraffids, bovines) are rare. Primates are very abundant’ (WoldeGabriel et al., 1994); ‘[…] interpreted to have been a closed woodland. At Aramis, aquatic species and large mammals are rare, and colobines make up over 30% of all vertebrate specimens collected’ (Leakey et al., 1995).
Kanapoi KNM-KP 29281 Australopithecus anamensis: Fish, aquatic reptiles, kudus and monkeys are prevalent. ‘A wide gallery forest would have almost certainly been present on the large river that brought in the sediments’ (Leakey et al., 1995).
Chad KT 12 A. cf. afarensis: ‘The non-hominid fauna contains aquatic taxa (such as Siluridae, Trionyx, cf. Tomistoma), taxa adapted to wooded habitats (such as Loxodonta, Kobus, Kolpochoerus) and to more open areas (such as Ceratotherium, Hipparion) […] compatible with a lakeside environment’ (Brunet et al., 1995).
Garusi-Laetoli L.H. A. anamensis or afarensis: Teeth and mandible fragments, the hardest skeletal parts which are frequently left over by carnivores (Morden, 1988), come from wind-blown and air-fall tuffs (Leakey et al., 1976). Cercopithecine and colobine monkeys are present (Protsch, 1981; Leakey et al., 1976).
Hadar, Afar Locality: ‘Generally, the sediments represent lacustrine, lake margin, and associated fluvial deposits related to an extensive lake that periodically filled the entire basin’ (Johanson et al., 1982)
Hadar AL.333 A. afarensis: ‘The bones were found in swale-like features […] it is very likely that they died and partially rotted at or very near this site […] this group of hominids was buried in streamside gallery woodland’ (Radosevich et al., 1992).
Hadar AL.288 gracile A. afarensis: Lucy lay in a small, slow moving stream. ‘Fossil preservation at this locality is excellent, remains of delicate items such as crocodile and turtle eggs and crab claws being found’ (Johanson & Taieb, 1976).
Makapan A. africanus: ‘[…] very different conditions from those prevailing today. Higher rainfall, fertile, alkaline soils and moderate relief supported significant patches of sub-tropical forest and thick bush, rather than savannah. Taphonomic considerations […] suggest that sub-tropical forest was the hominins’ preferred habitat rather than grassland or bushveld, and the adaptations of these animals was therefore fitted to a forest habitat’ (Rayner et al., 1993; see also Reed, 1993; and Wood, 1993).
Taung australopithecine: ‘the clayey matrix from which the Taung cranium was extracted, and the frequent occurrence of calcite veins and void fillings within it (Butzer, 1974, 1980) do suggest a more humid environment during its accumulation’ (Partridge, 1985).
Sterkfontein A. africanus and Swartkrans A. robustus: Many South African australopithecines are discovered in riverside caves, presumably often filled with the remainders of the consumption process of large felids (Brain, 1981).
Kromdraai: A. robustus was found near grassveld and streamside or marsh vegetation, in the vicinity of quail, pipits, starlings, swallows, and parrots, lovebirds and similar psittacine birds (T. N. Pocock in Brain, 1981).
Turkana KNM-ER 17000 and 16005: A. aethiopicus was discovered near the boundary between overbank deposits of large perennial river and alluvial fan deposits, amid water- and reedbucks (Walker et al., 1986).
Lake Turkana: ‘The lake margins were generally swampy, with extensive areas of mudflats […] Australopithecus boisei was more abundant in fluvial environments, whereas Homo habilis was rare in such environments […] Australopithecus fossils are more common than Homo both in channel and floodplain deposits. The gracile hominids […] seem to be more restricted ecologically to the lake margin than are the robust forms’ (Conroy, 1990).
Ileret A. boisei: ‘the fossil sample reflects climatic and ecological environmental conditions differing significantly from those of the present day. At Ilerat, 1.5 Myr ago, climatic conditions must have been cooler and more humid than today, and more favourable to extensive forests […] The prominence of montane forest is particularly striking […] dominated by Gramineae and Chenopodiaceae appropriate to the margins of a slightly saline or alkaline lake’ (Bonnefille, 1976).
Konso A. boisei: ‘The highly fossiliferous sands at the mid-section of KGA10 are interpreted to be the middle to distal portions of an alluvial fan, deposited adjacent to, and extending into, a lake. Fossils and artefacts deriving from horizons of sands and silts are not abraded and show evidence of minimal transport. A large mammalian assemblage has been collected from the deposits, showing a striking dominance of Alcelaphini […] to indicate the presence of extensive dry grasslands at KGA10’ (Suwa et al., 1997).
Chesowanja A. boisei: ‘The fossiliferous sediments were deposited in a lagoon […] Abundant root casts […] suggest that the embayment was flanked by reeds and the presence of calcareous algae indicates that the lagoon was warm and shallow. Bellamya and catfish are animals tolerant of relatively stagnant water, and such situation would also be suitable for turtles and crocodiles’ (Carney et al., 1971).
Olduvai middle Bed I: A. boisei O.H.5 as well as habilis O.H.7 and O.H.62 were found in the most densely vegetated, wettest condition, with the highest lake levels (Walter et al., 1991), near ostracods, freshwater snails, fish, and aquatic birds (Conroy, 1990); ‘[…] the middle Bed-I faunas indicate a very rich closed woodland environment, richer than any part of the present-day savanna biome in Africa […]’ (Fernández-Jalvo et al., 1998). ‘Fossilized leaves and pollen are rare in the sediments of Beds I and II, but swamp vegetation is indicated by abundant vertical roots channels and casts possibly made by some kind of reed. Fossil rhizomes of papyrus also suggest the presence of marshland and/or shallow water’ (Conroy, 1990). ‘[…] Cyperaceae fruits were common in H. habilis habitat (Bonnefille, 1984). Ancient Egyptians ate Cyperus papyrus root which was also present at Olduvai in swamp-margins and river banks’ (Puech, 1992).
Olduvai O.H.24 habilis: ‘Crocodile remains predominate among the faunal material from this site and more than 2,000 teeth were found. Tortoise plates, shells of Urocyclid slugs, fish vertebrae and scales, bird bones and pieces of ostrich eggshell were also relatively common (Leakey et al., 1971).
Malawi UR 501 early Homo: ‘The Plio-Pleistocene Chiwondo Beds of Northern Malawi have yielded molluscs and fragmented remains of fish, turtles, crocodiles and large mammals […] Microvertebrates and carnivores are virtually unrepresented in the assemblage […] The general ecological setting of the Malawi Rift during the Late Pliocene was a mosaic environment including open and closed, dry and wet habitats, and which harbored a small and ecologically unstable paleolake Malawi’ (Schrenk et al., 1995).
Chemeron KNM-BC1 early Homo: ‘The Fish Beds […] seem to be almost entirely lacustrine and fluviatile; fish remains are abundant […] Molluscs also lived in the lake, and locally their remains accumulate to form shelly limestones’ (Martyn & Tobias, 1967).
Turkana Boy KNM-WT 15000 H. erectus: ‘Mammalian fossils are rare at this locality, the most abundant vertebrate fossils being parts of small and large fish. The depositional environment was evidently an alluvial plain of low relief […] Typical lacustrine forms (for example, ostracods, molluscs) could invade the area […] The only other fauna found so far in the fossiliferous bed are many opercula of the swamp snail Pila, a few bones of the catfish Synodontis and two fragments of indeterminate large mammal bone […]’ (Brown et al., 1985).
Mojokerto H. erectus: ‘The basal part of the Putjangan Beds is composed of volcanic breccias containing marine and freshwater molluscs. The rest of the Putjangan Beds is composed of black clays of lacustrine origin’ (Ninkovich & Burckle, 1987).
Peking H. erectus: ‘A big river and possibly a lake were located to the east and contained various water species; along the shorelines grew reeds and plants, which were home for buffalo, deer, otters, beavers and other animals’ (Poirier, 1978); ‘[…] accumulation in quiet water. The cave at this time was probably the locus of ponded water and was probably more open to the atmosphere’ (Weiner et al., 1998).
Hopefield, Rabat & Terra Amata: H. erectus fossils came from sandstone made up from dune sand resting upon a former sea beach (De Lumley, 1990). In Terra Amata, ‘there are also indications that the inhabitants ate oysters, mussels and limpets – shells of which are present. The presence of fish bones and fish vertebrae indicate that the population also fished’ (Poirier, 1987).

Australopithecine lifestyle

The list shows that some very early hominids, more than later australopithecines, have been found near lacustrine molluscs (Lukeino and Tabarin ca. 6.5 and 5 Myr BP). Ardipithecus ramidus, supposedly another early hominid, must have lived in a wooded habitat, amid predominantly colobine monkeys (Aramis ca. 4.5 Myr BP). Pliocene australopithecines ca. 4-3 Myr BP apparently frequently dwelt in warm and humid, more or less closed environments (gallery forest or wooded habitat in Kanapoi, Chad, Hadar, Makapansgat, but inconclusive for Garusi-Laetoli). Pleistocene robust australopithecines since 2.5 Myr BP probably lived in generally dryer and more open landscapes (grassland in Kromdraai and Konso), but their remains lay in riverbanks, lagoons, marshes, lake-margins, near papyrus (Olduvai) and reed (Kromdraai, Olduvai, Chesowanja).

Although ‘all nine Konso A. boisei specimens were recovered among the predominantly dry grassland fauna of KGA 10’ (Suwa et al., 1997), this does not mean that they lived in a savanna milieu, since ‘nearby subsites were also moist and wooded’ (Delson, 1997). Fragmentary fossils like those of Laetoli and Konso are often the remains of carnivore meals (Morden, 1988). Leopards, which preyed upon australopithecines, prefer to feed in dry circumstances and therefore drag away their prey, sometimes several hundred meters (Brain, 1981).

The preponderance of wet environments in our list is striking, but this was not considered to be inconsistent with a savanna view, because it was believed that the fossil record sampled a disproportionate number of habitats related to water (see the above citation from Shipman and Harris, 1988). To be sure, that the hominids have been discovered in humid or wet habitats does not allow firm conclusions about how much time they spent there, but the possibility that wetter rather than drier conditions influenced hominid evolution can not be ignored. Therefore, paleo-ecological data must be verified and supplemented through anatomical and especially dental studies of the fossils.

It is generally agreed that all australopithecines have skeletal features of bipedality. Early graciles also show clear indications of tree climbing such as curved manual and pedal phalanges, though such features are less obvious in the robusts.

Dental studies suggest that whereas gracile australopithecines preferred softer fruits and vegetables, the robusts’ diet included harder food items (e.g. Robinson, 1954; Du Brul, 1977; Walker, 1981; Puech, 1992; Lee-Thorp et al., 1994). Estimates of robust australopithecine bite force suggest ‘low-energy food that had to be processed in great quantities’ and food objects ‘hard and round in shape’ (Demes & Creel, 1988). Du Brul (1977) noticed dental parallelisms between the robust australopithecines and the bamboo-eating giant panda Ailuropoda melanoleuca (broad, high and heavy cheekbones, reduced prognathism and front teeth, broad back teeth, premolar molarisation), as opposed to gracile australopithecines, respectively non-panda bears.

Papyrus and reed were present in the paleo-environment of the later australopithecines (e.g. Olduvai, Chesowanja, Kromdraai), and Cyperaceae and Gramineae are part of the diet of living African hominoids. Gorillas eat sedges and bamboo shoots and stalks, gorillas and chimpanzees eat cane, chimps and humans eat water lilies, and rice and other cereals are staple food for humans. Supplementing their diet with parts of grasslike plants might have been enabled the robusts to bridge the dry season, when fruits and soft vegetables were scarce.

Studies of dental enamel microwear provide other details. In the early australopithecines of Garusi-Laetoli and Hadar (A. afarensis 4-3 Myr BP), the cheekteeth enamel has a polished surface and the microwear looks like that of the capybara Hydrochoerus hydrochaeris and that of the mountain beaver Aplodontia rufa (Puech et al., 1986). These animals are semi-aquatic rodents that feed mainly on sappy marsh and riverside herbs, grasses and bark of young trees. It has recently become clear that Western lowland gorillas G. g. gorilla spend some time eating aquatic herbaceous vegetation (AHV) like Hydrocharitaceae herbs and Cyperaceae sedges (Doran & McNeilage, 1997).

Comparisons of molar enamel in South African fossils show that A. robustus ate substantially more hard food items than A. africanus (Grine & Kay, 1988). Incisal microwear suggests that A. robustus may have ingested foods that required less extensive incisal preparation than the foods consumed by A. africanus, such as fruits (Ungar & Grine, 1991), and ‘incisors need not be employed in the manipulation of hard objects’ (Ungar & Grine, 1989).

The enamel of the East African robusts (Olduvai and Peninj) displays more pits, wide parallel striations and deep recessed dentine, resembling that of the beaver Castor fiber, that eats riverine and riverside herbs, roots of water lilies, bark and woody plants in a temperate climate. ‘Many food plants growing in marsh land and indeed many grasses, have high concentrations of siliceous particles known as opal phytoliths. The consumption of such foods produces a great deal of wear, and the enamel and dentine have a blunted appearance. Ancient Egyptians ate papyrus shoots (Puech et al., 1983b) and we suppose that [O.H.16] did the same with swamp margin plants’ (Puech, 1992). Whereas the East African robusts seem to have had aquatic plants and papyrus shoots in their diet and ate more woody plants than the earlier australopithecines, habilis O.H.16 apparently supplemented the AHV of the earlier australopithecines with acid fruits (Puech, 1984). In the habilis cheekteeth, the margins of the striae have been polished and slightly etched, resembling the microwear of the coypu Myocastor coypus. This rodent feeds on reed, sedges, marsh plants, fruits and molluscs in river and lake margins. It thus seems that an early australopithecine diet of fruits (larger front teeth) and AHV (polishing) was supplemented with unripe fruits (acid etching) in habilis, and with woody plants in the robusts (more wear).

The suggestion of Walker (1981) that A. boisei KNM-ER 406 and 729 were bulk-eaters of whole fruits, ‘small, hard fruits with casings, pulp, seeds and all’, could explain the deep recessed occlusal dentine, but not the glossy appearance of heavily polished enamel, which is more typical for marsh plant feeders. In terrestrial grazers such as sheep, tooth wear is faster, with a different gradient and fabric-like grooves.

These microwear data are consistent with the strontium/calcium ratios in Swartkrans fossils (Sillen, 1992). Apart from partial carnivory (rather unlikely with the robusts’ dentition, see Du Brul, 1977; Walker, 1981), Sillen provides two possible explanations for the low Sr/Ca of A. robustus: eating leaves and shoots of forbs and woody plants (kudu diet), and eating food derived from a wet microhabitat, for instance, from well-drained streamside soils.

In our opinion, the coincidence of several independent lines of evidence (paleo-milieu, dental morphology, enamel microwear, Sr/Ca ratios) leaves little doubt that some or all australopithecines fed regularly on AHV growing in shallow waters, much more than Western gorillas do today (Chadwik, 1995; Doran & McNeilage, 1997). It is conceivable that hominid bipedality first arose in the shallow waters of gallery or mangrove or swamp forests. ‘One of the strong points about the aquatic theory is in explaining the origin of bipedality. If our ancestors did go into the water, that would forced them to walk upright’ (Stringer, 1997). That a gradual evolutionary transition from forest to marshland is possible is illustrated by the Western lowland gorillas that spend some time feeding on AHV, wading bipedally, sitting and playing in marshy forest clearings (Chadwik, 1995; Doran & McNeilage, 1997; NDR TV film, 1997).

Hominine lifestyle

A major distinction between fossil Australopithecus and Homo is the reduction of the last molar (from M1<M2<M3 to M1<M2>M3). This might have been the result of a new, cultural factor: the frequent use of stone tools by the Homo species. 2.5-Myr-old stone tools ‘are found in floodplain environments, close to margins of channels that carried the volcanic cobbles used as raw material for tool manufacture’ (Semaw et al., 1997).

In other mammals, hard objects are used for opening shellfish or nuts. Sea otters Enhydra lutris crush shellfish with stones, chimpanzees Pan troglodytes use stones to crack nuts, mangrove capuchin monkeys Cebus apella apella use oyster shells as hammers to open oysters fixed to the roots and lower branches of mangrove trees (Fernandes, 1991).

Homo species lived in places where freshwater or marine bivalves were more abundant (e.g. Chiwondo, Chemeron, "Turkana Boy", Mojokerto, Terra Amata) than in the australopithecine habitats. Whereas Australopithecus appears to have lived near inland rivers and marshes, early Homo seems to have occupied also bivalve-rich areas such as mangrove forests and other seacoasts. This would explain the "sudden" appearance of Homo erectus-like people along the Indian Ocean and inland along the rivers. They colonised the Indian Ocean shores as far as Java perhaps as early as 2 Myr BP. In contrast with australopithecines, they must have crossed deep-water straits like those of Gibraltar and Flores (Morwood et al., 1998), and their remains have been found all over the Old World, from Indonesia to the Cape and England (e.g. seashore remains in Mojokerto, Hopefield, Rabat, Gesher Benot Ya’aqov, Terra Amata, Boxgrove).

A dietary supplement of shellfish eating, perhaps only seasonal, could also help to explain the dramatic increase in brain size in Homo. It would have abundantly provided the elements essential for brain-growth. It has been claimed that the composition of the long-chain poly-unsaturated fatty acids in tropical fish and shellfish is ‘more similar to that of the human brain than any other food source known’ (Broadhurst et al., 1998).

Natura non facit saltum

This "wet" scenario requires no great evolutionary steps. Forest-dwelling herbivores like capybaras, tapirs or pygmy hippos are partially adapted to the water collections in the tropical or subtropical rain or gallery or mangrove forests, but remain four-legged. In these shallow waters, primates - which, because of their arboreal history, have very mobile joints and a tendency to body erectness - easily adopt a bipedal stance and gait. Lowland gorillas go wading on their hind legs through swamps to get edible sedges and AHV (Chadwik, 1995; Doran & McNeilage, 1997). Proboscis monkeys Nasalis larvatus cross stretches of water on two legs to reach other mangrove trees (Morgan, 1997; Ellis, 1991). Japanese monkeys Macaca fuscata on islands walk bipedally into the sea (e.g. Morgan, 1997).

In mangrove swamps, lower tree parts are occupied with bivalves, which are exposed at low tide (Fernandes, 1991). No doubt, inventive inhabitants of such places began to exploit these rich food sources, just as capuchin monkeys do, who feed on crustaceans and oysters. These relatively large-brained primates even use oyster shells to crack other oysters when no stones are available (Fernandes, 1991). Probably, human ancestors, who already cracked hard-shelled nuts and fruits with stones, used pebbles as tools, at first for opening shellfish and later for processing other food sources like carcasses of hippopotamuses (e.g. Bunn, 1981). Once they mastered how to cut through skins with sharp stones or to use stone tools for processing wood, they would have seen new niches open to them, encouraging them to invade the inland along the rivers.

Physiological data make it very probable that the phase of partial shellfish collection at one time included frequent diving (Schagatay, 1996). Today, human populations all over the world still collect shellfish or seaweed through diving. It could perhaps explain some human parallelisms with sea-mammals, according to the ideas of the so-called aquatic hypothesis of human evolution (Westenhöfer, 1924, 1942; Hardy, 1960; Morgan, 1982, 1990, 1997).

Among these adaptations, those for diving and breath-holding (Schagatay, 1996), in combination with an older sound production as in many arboreal animals like gibbons (Darwin, 1871), could have led the basis for the voluntary and articulate sound production of human speech (Verhaegen, 1997). In this respect, Derek Ellis (personal communication) remarks ‘how well sound travels over water, compared to being muffled in forests, and even compared to grassland. Foraging beach and lagoon apes could separate quite widely and still remain in contact by vocalising’.

Although both Australopithecus and Homo species seem to have dwelt at the edge between land and water, the differences in paleo-milieu, dentition, tool use and brain size suggest that both had different lifestyles. Nevertheless, there is a completely natural sequence of small behavioural innovations that could lead from early australopithecines to modern humans (points 2 to 5 are seen in chimps or gorillas, see Yamakoshi, 1998; Chadwik, 1995; Ellis, 1991; Nishida, 1980; Golding, 1972).

frugi- and herbivory in tropical forests (all hominoids),
using stones to crack hard-shelled fruits and nuts,
frugi- and herbivory also in forest clearings,
plus "short"-legged bipedal wading in shallow waters,
plus more frequent surface-swimming,
wading and swimming also in mangrove forests,
plus feeding on bivalves growing on lower tree parts,
using shells or stones to crush shellfish,
using stone tools for various purposes,
colonising the seashores and rivers as omnivores,
re-invasion of the land along the rivers,
long-legged bipedalism on land.

Conclusion

The combination of comparative, physiological and paleo-environmental data makes a savanna evolution improbable, but does not exclude a temporary evolution of human ancestors and relatives at the edge between land and water. Many human features cannot be explained by a history of tree or forest dwelling alone, but find convergences in primates that live in mangrove areas, such as proboscis monkeys and some tufted capuchins. The paleo-environmental and dental data suggest a gradual evolution, in strongly overlapping phases, from frugi- and herbivores in gallery or tropical or mangrove forests to "short"-legged bipedal waders in forest clearings or mangrove swamps, to omnivores and partial shellfish feeders along seacoasts and rivers, and finally to long-legged bipedalists on land.

Acknowledgements

We wish to thank Elaine Morgan, Roger Crinion, Derek Ellis, Erika Schagatay, Charles Oxnard, Norman McPhail, Stephen Munro, Nicole Oser and Renato Bender for information or corrections.

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Received September 30, 1998 Accepted April 10, 1999

2. Morphological Distance between Australopithecine, Human and Ape Skulls

Human Evolution 11: 35-41, 1996

This paper attempts to quantify the morphological difference between fossil and living species of hominoids. The

comparison is based upon a balanced list of craniodental characters corrected for size (Wood & Chamberlain, 1986). The conclusions are: craniodentally the australopithecine species are a unique and rather uniform group, much nearer to the great apes than to humans; overall, their skull and dentition do not resemble the human more than the chimpanzee’s do.

Key words: human evolution, hominids, apes, skull, Australopithecus, Homo erectus, chimpanzee, gorilla

Introduction

The australopithecine species are commonly considered to be "hominids" beeause they lack some of the features that characterize the living apes, and display certain humanlike characters. Yet it has often been argued that their humanlike characters might be primitive - and indeed many of these characters are found in premature African apes - and that the australopiths should not be included in the evolutionary branch towards humans, but instead are a unique group of apes or might even be closer phylogenetically to the African apes than to humans (e.g., Kleindienst, 1975; Goodman, 1982; Gribbin & Cherfas, 1983; Oxnard, 1984; Hasegawa et al., 1985; Edelstein, 1987; Verhaegen, 1990; 1994).

The aim of this paper is to objectivate morphological resemblances of australopithecine species with living hominoid species. (To establish phylogenetic relationships, biomolecular comparisons of nucleic acids or proteins are preferable to morphological comparisons, but it does not seem very probable that extraction of enough DNA or protein from fossil bone will ever become possible.)

Methods

I have used the comparative data of Wood and Chamberlain (1986) because:

Their data are likely to be comparable since they stem from the same source.
They use a balanced list of 39 characters, i.e., "selected to provide a relatively comprehensive coverage of the head" without much functional or morphological overlapping. The 39 characters stem from: cranial vault and endocranium (11 V), face (7 F), palate and maxilla plus dentition (7 P), cranial base (5 B), and mandible plus dentition (9 M).
Wood and Chamberlain do not use the "raw" metrical data, but ratios, which "help to reduce, if not actually eliminate, differences due to absolute size".

Postcranial data (more scarce and difficult to attribute to a certain species) are not included in their list.

Since the data for the 39 characters were not available for all species, I selected two (overlapping) Character Groups (only characters V9 and B5 were not used at all):

I. one of 32 characters (82 %) that were available for 8 species: Hylobates, Pongo, Pan troglodytes, Gorilla, A. africanus, A. boisei, H. erectus and H. sapiens (characters V1-8,10- 11, F1-7, P1-3,5-6, B1,4, M-6,8-9);

II. one of 27 characters (69 %) that were available for 7 species: Pongo, Gorilla, Pan troglodytes, Homo sapiens, Australopithecus africanus, A. robustus and A. boisei (characters V1,7-8, F1-7, P1-7, B1-3, M1,4-9). This second Group was added since it included data from a third australopithecine species, A. robustus.

The data for Pan paniscus, A. afarensis and H. neanderthalensis could not be used, since they were available for too few characters. The data for "H. habilis" (which included ER-1470, ER-1813, and OH material) were not used since they might belong to more than one species.

A simple method measured the relative overall craniodental distance between the different (fossil as well as living) hominoid species without considering any of these species as an outgroup a priori:

Each character had to have equal weight. For each species and each character, the sum of the differences with the same character in the other species was given an arbitrary weight of 1000, i.e., each of the differences with the other species was divided by the sum of these differences and multiplied by 1000. Tables Ia and IIa show the mean results of all (32 or 27) characters for all (8 or 7) species. These results, of course, are not directly proportional to the morphological distance, but indicate that the difference between species A and B is larger or smaller than that between A and C. As an example, Figure 1 shows the calculation of the results for Character Group II (and more in particular for A. boisei).

These results in Tables Ia and IIa for each species were made more comparable with those for the other species in the same Character Group (e.g., for interpreting the diagrams, see below) by multiplying them by a correction factor consisting of the sum (/1000) of the differences of the other species with that species (see Figure l). This yielded Tables Ib and IIb. (This correction exaggerates the results of the most aberrant species (e.g., H. sapiens in Table II), but does not change the order of differences.)

For illustrating which one of the living species resembled a fossil species most, the diagrams of Figure 2 were constructed. Since all results are relative, the diagrams could be made clearer by equalling one of the species to zero. In this case, Pongo, which was nearest to the mean species, was taken as the reference (this choice, of course, does not influence the conclusions): in Tables Ib and IIb, the results comparing Hylobates, Gorilla, P. troglodytes and H. sapiens with the fossils were subtracted from the results of Pongo, so that a positive result (above the x-axis) means that the fossil resembles the living species more than it resembles Pongo craniodentally; a negative (below the x-axis), less.

(For comparing the diagrams between both Character Groups, the results for Group I could have been multiplied by 5198/3954, which is the quotient of the sums of the differences within Group II and I using only the species common to both Groups (i.e., omitting the results for H. erectus, A. robustus and Hylobates). This second correction factor (even less than the first) would not have influenced the conclusions.)

Discussion

The tables show that morphologically the great hominoids form three clusters: Homo, the australopithecines, and the great apes.

1) The human skull is unique and differs from that of the great apes even more than the gibbon does. Homo is about equidistant from australopithecines and chimpanzees (though evolutionarily he is probably closer to A. africanus than to Pan, only because A. africanus lived almost three million years nearer to the common ancestor). H. erectus in Group I seems to be on the way to H. sapiens. He is about equidistant from H. sapiens, P. troglodytes and A. africanus, but differs from the australopithecines even slightly more than Pongo does.

2) The australopithecine skulls resemble each other more than they resemble the apes (even the African apes) and certainly humans; A. robustus stands somewhere between A. africanus and A. boisei, but nearer to A. boisei. In comparison with the living species (Figure 2):

A. africanus in both Character Groups is closest to the chimp, and closer to chimpanzees, gorillas and orangutans than to humans (and to gibbons in Group I);
A. robustus in Group II also is morphologically closest to the chimpanzee, and much closer to chimp, gorilla and orang than to humans (gibbons were not included in this comparison);
A. boisei in both Groups is closer to G. gorilla than to Pan troglodytes (in contrast with the South African fossils), and very different from Homo, somewhat more different than A. africanus is from Homo.

A. boisei (who lived later) more than A. africanus (who lived earlier) resembles the living African apes compared with humans or orangs or gibbons (Figure 2). In Diagram II of Figure 2, A. robustus also resembles the African apes more than A. africanus does in comparison with humans. This indicates that the australopithecines (from graciles to robusts) were evolving in the African ape direction - whether in parallel with the apes (see Ferguson, 1989) or not (Verhaegen, 1994).

3) The great apes (even including Pongo) resemble each other even more than H. erectus and H. sapiens in Group I resemble each other, in spite of the evolutionary distance between the apes (cf. the African apes and Pongo split perhaps ten times earlier than H. erectus and H. sapiens). They resemble each other more than A. boisei resembles A. africanus. This points to a remarkable degree of conservatism and/or of parallelism in cranial evolution of these three great ape species (and to a remarkably fast evolution of Pleistocene Homo). Yet, chimps, somewhat more than gorillas, resemble Homo more than orangs and certainly gibbons do (in accordance with the biochemical resemblances).

All this implies that the craniodental evidence provides no ground for the anthropological custom of using the living African hominoids as an outgroup when comparing australopithecines with humans or when reconstructing hominoid phylogenetic trees: if the australopithecine species are considered to be hominid, the great apes and certainly the African apes should also be called hominid, since they resemble the australopiths more than humans do, and they do not differ from humans more than the australopiths do (Figure 3).

The australopithecines are often assumed to be hominids on the basis of their postcranial features (not included in Wood and Chamberlain’s list), but many authors argue that locomotorically australopithecines differed more from humans than from the African apes (for discussion and references, see especially Oxnard, 1984; and Verhaegen, 1990, 1993, 1994). In this respect too, the australopithecines could have had unique adaptations (Oxnard, 1984) for an environment or lifestyle that no longer exist. (For instance, there is dental as well as paleo-environmental evidence that the later australopiths fed partly on bamboo or reed or papyrus (Du Brul, 1977; F. E. Grine, pers. comm.; Puech, 1992, and pers. comm.; Verhaegen, 1992), possibly wading bipedally in the shallow waters where most fossils are discovered (discussion in Verhaegen, 1993).)

Although Gorilla and Pan skulls resemble each other morphologically (Tables Ib and IIb), both species differ biochemically (in DNA and proteins) even more than Homo and Pan (e.g., Horai et al., 1995). Since synchronous parallel evolution in related species in response to a climatic change appears to be the rule (e.g., White and Harris, 1977; Seger, 1987, Gibbs and Grant, 1987; Bown et al., 1994; theoretical considerations in Silson, 1988), some African ape features that are usually assumed to be primitive might instead have developed in parallel in gorillas and in chimpanzees. The possibility should even be considered that, if australopiths are more closely related to the African apes than to humans (be it, of course, on morphological grounds, see Figure 3), some australopithecines might evolutionarily be closer to chimpanzees and others to gorillas (discussion in Verhaegen, 1994).

Conclusions

This comparison of 37 craniodental characters of fossil and living apes and humans yields no indication that any of the australopithecine species has evolved in the human direction. South African australopithecine skulls are morphologically closest to the chimpanzee among the living hominoids, and A. boisei is closest to the gorilla among the living hominoids. Human craniodental evolution appears to have been very fast the last one or two million years.

These conclusions could be verified and extended when more (including postcranial) data on living (e.g., P. paniscus) and fossil hominoids (adult and premature) will become available.

Tables

Craniodental differences between hominoid species.

Tables Ia and Ib based on 32 characters (8 species).

Tables IIa and IIb based on 27 characters (7 species).

Tables Ib and IIb corrected (see text and Figure 1).

References

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3. Australopithecines: Ancestors of the African Apes?

Human Evolution 9: 121-139, 1994

Since australopithecines display humanlike traits such as short ilia, relatively small front teeth and thick molar enamel, they are usually assumed to be related to Homo rather than to Pan or Gorilla. However, this assumption is not supported by many other of their features.

This paper briefly surveys the literature concerning craniodental comparisons of australopith species with those of bonobos, common chimps, humans and gorillas, adult and immature. It will be argued, albeit on fragmentary data, that the large australopiths of East Africa were in many instances anatomically and therefore possibly also evolutionarily nearer to Gorilla than to Pan or Homo, and the South African australopiths nearer to Pan and Homo than to Gorilla. An example of a possible evolutionary tree is provided. It is suggested that the evidence concerning the relation of the different australopithecines with humans, chimpanzees and gorillas should be re-evaluated.

Key words: Hominid evolution, Australopithecus, robust polyphyly, gorilla, chimpanzee, bonobo, Lucy, Taung, molecular clock.

Introduction

Biomolecular data place the Homo/Pan splitting time between 8 and 4 Myr BP (e.g. Sarich, 1977; Hasegawa et al., 1987, 1988, 1989; Caccone & Powell, 1989). This means that at the time of the earliest undoubted australopithecines (ca. 4 Myr BP), the differences between human and chimpanzee ancestors were much less than those between present-day Homo and Pan, so that it is difficult to decide whether a particular fossil of that age belonged to the Homo or to the Pan clade. No a priori reason exists therefore to reject the idea that the African apes may have had australopith ancestors. Several people had contemplated this possibility even before Sarich & Wilson (1967) initiated the drastic reduction of the estimated Homo/Pan splitting time (e.g. Woodward, 1925; Smith, 1925; Keith, 1925a, b; 1931, p.115; Schultz, 1941, p.100; A. Hrdlicka in Howells, 1985; W. Abel; W. L. Straus, S. Zuckerman, E. H. Ashton in Reader, 1988, p. 89 and p. 124). Following the introduction of the biomolecular evidence, the idea has revived (e.g. Kleindienst, 1975; Goodman, 1982; Gribbin & Cherfas, 1983; Hasegawa et al., 1985; Edelstein, 1987; Verhaegen, 1990; Trevino, 1991, p. 14-15).

This approach could also explain the discrepancy between the enormous number of fossil finds and the apparent total absence of fossil African ape ancestors from a period covering at least the last four million years (Gribbin & Cherfas, 1983; Verhaegen, 1990). The usual explanations offered are that paleontologists have not worked in the appropriate areas, or that the probability of fossilization in the tropical forests, where the ancestral apes presumably lived, is very low because of the relative acidity or the wetness of the soil (e.g. G. S. Krantz in Kleindienst, 1975). These explanations are hard to reconcile with the numerous discoveries of forest-dwelling bovids, suids, monkeys, dryopithecines and probable early relatives of the orang-utan (Kleindienst, 1975; Kortlandt, 1975; cf. Pilbeam, 1982; Andrews & Cronin, 1982).

When Dart (1925) discovered the skull of Taung, he believed that it was in the human lineage because it showed what he called "humanoid" features such as relatively small canines and forward situation of the foramen magnum. His proposal was promptly rejected by nearly all his colleagues (e.g. Keith, 1925a,b; Smith, 1925; Woodward, 1925; Duckworth, 1925), who saw in Taung nothing more than a sort of young chimp or perhaps gorilla. They were supported in their opinion by the Piltdown skull, which showed a rather ape-like dentition together with a big brain, almost the opposite of the Taung child. But later, when Kenneth Oakley unmasked Piltdown Man as a fraud and Robert Broom concluded from his studies of postcrania that the South African australopithecines were bipedal, opinions about Taung changed and the australopiths became accepted as being closer to man than to apes.

This paper argues that the nearly general acceptance around 1950 of W. E. Le Gros Clark’s ideas, following Dart and Broom, that the South African australopiths were closer to humans than to "pongids" (mostly based on comparisons of their pelvis and dentition, often with male gorillas, e.g. Le Gros Clark, 1978, first edition 1955) might have been an overreaction after the unmasking of Piltdown, and that the anthropologists’ first impressions - that Taung was a fossil species of Pan - should be reconsidered. (That Taung was closer to Homo than to Gorilla and certainly Pongo, is of course not contested in this paper).

Homo-like features in australopiths: primitive?

In imitation of Dart, Broom and Le Gros Clark, the australopithecine species are now usually considered to be closer relatives of humans than of apes. This opinion is based especially on their locomotor and dental features.

Ventral position of foramen magnum

It is generally accepted that the australopiths were more bipedal than present-day gorillas and common chimps, mostly because of the Laetoli footprints almost 4 Myr BP, the short ilia of Lucy and Sts.14, the broader calcaneus and the more human-like orientations (though rather ape-like anatomy) of the ankle and knee articulations of the Hadar specimens (Stern & Susman, 1983; Latimer et al., 1987), and the more ventral position of the foramen magnum in many australopiths. "Early australopithecines are linked with living humans on the basis of shared characters related to bipedalism" (Andrews, 1992), but it is often argued that the African apes’ ancestors also were more bipedal (theory of W. L. Straus; see Coon 1954; Kleindienst, 1975; Goodman, 1982; Gribbin & Cherfas, 1983; Hasegawa et al., 1985; and esp. Edelstein, 1987; cf. Schultz 1949, p. 205). Indeed, that the African apes could evolve from digiti-palmigrades (all other primates, including human infants) to knuckle-walkers implies that they went through a phase where the arms were barely used for pronograde locomotion (cf. Edelstein, 1987); an intermediate phase of orthograde arm-hanging or brachiation insufficiently explains knuckle-walking since neither orangutans nor hylobatids show traces of knuckle-walking. Also, most anthropoids (especially the young) occasionally walk on two legs, and bipedal tendencies are very striking in the African apes (but virtually absent in Pongo). Chimpanzee fetuses shortly before birth show humanlike feet with ventrally oriented and adducted first digital rays (Coon, 1954). Common chimps often walk bipedally on muddy terrain (Nishida, 1980), and bonobos are even more frequently bipedal (Zihlman et al., 1978; De Waal, 1988). "When they are on the ground, anthropoid apes... often walk erect, and the mountain gorilla's foot, indeed, is already similar to man’s" (Rensch, 1972, p. 63; see also p. 130; Schultz, 1950; Edelstein, 1987). In addition, of all primates, only the African hominoids are fully plantigrade (Gebo, 1992):

"Orangutans have further enhanced foot mobility by adapting their feet for suspension and thus similarly utilize foot positions where the heel does not touch the substrate. Chimpanzees and gorillas represent an alternative pattern (plantigrady), in which the heel contacts the surface of the support at the end of the swing phase, especially during terrestrial locomotion. Thus chimpanzees and gorillas possess feet adapted for both arboreal and terrestrial substrates. African apes also share several osteological features related to plantigrady and terrestrial locomotion with early hominids. Humans and African apes are very similar in their use of plantigrady when moving or standing upon a terrestrial substrate and this pattern of foot use is extremely different from what characterizes all other primates".

Also, young gorillas and chimpanzees have foramina magna more ventral than adults and well within the range of A. africanus Sts.5 (e.g. Ashton & Zuckerman, 1952; Schultz, 1955). Even in adults, the foramen has the same position indices in gracile (Sts.5) and robust australopithecines (KNM-ER 406) as in bonobos (Kimbel et al., 1984, table 9). Masters et al. (1991):

"Since Taung was perhaps 3.5 years of age at death (Bromage and Dean, 1985), the position of the foramen magnum may not have achieved its adult status. This contradicts the assessment made by Dart (1925), who interpreted the position of the foramen magnum as indicating bipedal locomotion in Australopithecus africanus".

Thick enamel

Thicker molar enamel was formerly treated as a reliable sign of affinity with the human line, so that species such as "Ramapithecus" (now included in Sivapithecus and usually considered to have Pongo as its closest living relative, see Pilbeam, 1982; Andrews & Cronin, 1982) were designated as possible human ancestors on the strength of this evidence. But this is no argument for a closer affinity of the australopithecines with humans than with African apes, since Martin (1985) argues that the extant great apes have secondarily reduced enamel - slight in the case of Pongo and more marked in Gorilla and Pan (but see also Beynon et al., 1991). It is in no way inconsistent with australopiths being ancestral to African apes (Martin, 1985):

"thick pattern 3 enamel does not identify a hominid. Moreover, the common ancestor of the great apes and man, and of the African apes and man, would have had teeth resembling those of hominids... Of the living members of the great ape and human clade, only Homo sapiens retains the condition of enamel thickness and development from the common ancestor of the clade and can therefore be regarded as the most dentally primitive member of it".

Smaller anterior dentition

The pronounced prognathism and large incisors and very large canines of the adult males of G. gorilla and P. troglodytes are thought to exclude australopith ancestors, since most robust australopiths had "flat" faces and (at least in comparison with their enormous back teeth) small anterior teeth. But this evidence is not conclusive: (1) A. afarensis and A. africanus also possessed moderately projecting canines, and the robust australopiths could have been extinct side-branches specialized for extremely tough food (e.g. Verhaegen, 1992), (2) even in robust australopiths (SK 23, Natron, L.7-125), the indices of the basic rectangle of the mandible are within the range of these of common chimps but outside those of humans (Kinzey, 1970); (3) in many robust specimens, the front teeth are so much worn that it is difficult to estimate how long their unworn canines would have been (but at least the A. boisei from Chesowanja showed unworn canines which were rather short), (4) in Gorilla and Pan "with advancing age, canines tend to wear flat to the level of the incisors" (Ryan & Johanson. 1989); (5) bonobos "have relatively small and only slightly dimorphic canine teeth" (Zihlman et al., 1978); (6) "infant great apes have flat or orthognathic faces like modern humans" (Aiello & Dean, 1990, p, 197); (7) some specimens of H. erectus had maxillary diastemata of 6 mm, as large as an orang’s (Howells, 1959, p. 157; Rensch, 1972, p. 36), and much larger than in the robust australopiths (who lived earlier); (8) selection for larger or smaller teeth can theoretically occur in very short evolutionary periods (cf. Silson, 1988, p. 19), and is claimed to have been demonstrated in only a few thousand years in human populations (Calcagno & Gibson, 1988); (9) the marked difference in prognathism between Negroes and Whites (e.g. Howells, 1959, p.269; Kinzey, 1970, fig. IA-B) developed in a time span of only about 200,000 years (Cann et al., 1987; Vigilant et al., 1991).

Moreover, it is not very likely that the primitive African hominoid condition included ape-like pronounced prognathism and very long canine teeth. See, for instance, Kinzey’s (1970) comparisons of the basic rectangle of the mandible in different Haplorhini (in Kenyapithecus africanus, e.g., it resembles Homo rather than Pan), or the anatomy of the face in infant chimpanzees (orthognathism with relatively short milk canines and vertical mandibular symphysis).

Australopiths resemble young Pan or Gorilla

At first sight, australopith skulls are more reminiscent of African apes, especially juveniles and subadults, than of humans (even Le Gros Clark calls them ape-like creatures): the general morphology of the gracile crania resembles that of bonobos or common chimps, and the larger crania are more gorilla-like (e.g. Lewin, 1987, p. 260; Zihlman et al., 1978; Rensch, 1972, p. 40; Robinson, 1960; Kennedy, 1991, fig.1). This is not contradicted by a more detailed look at their anatomy. Table 1 gives a few striking quotations about ape-like features of australopith skulls in general; Table 2 provides quotations about gorilla-like cranial features in large East African fossils; Table 3, about chimpanzee-like features in africanus and robustus crania.

It is a pity that this paper has to rely so heavily upon the anthropologists’ impressions (quoted in Tables 1, 2 and 3), but extensive comparisons with enough species (including several extinct hominid species, African hominoids and humans) are rather scarce. Even in recent excellent and thorough textbooks (e.g. Conroy, 1990; Aiello & Dean, 1990), australopith fossils are often compared only with man and one of the great apes (usually the common chimp), and detailed comparisons of the australopithecine features with humans and all three African ape species (not to mention orang-utans), preferably of different subspecies (e.g. high- vs lowland gorilla), ages and sexes, are surprisingly rare in the literature (but see e.g. Schultz, 1955; McHenry, 1983; Demes, 1988). Because of these anthropocentric viewpoints, the differences between the African ape species - like those between the different australopith species - are often underestimated. In fact, Pan is more closely related to Homo than to Gorilla biochemically (see below), and Groves & Paterson (1991) in their computer analysis of 89 anatomical features, conclude that Pan is even morphologically slightly nearer to Homo than to Gorilla.

Table 1 - Some quotations on ape-like features in australopith crania

"The evolution of the australopithecine crania was the antithesis of the Homo line. Instead of becoming less ape-like, as in Homo, they become more ‘ape-like’. Cranial proportions and ectocranial features that were thought to be unique among pongids evolved separately [? M. V.] in the australopithecines parallel [? M. V.] with the great apes. The features of KNM-WT 17000, therefore, are not as ‘primitive’ as they look. The robust Australopithecus did not evolve from a big-toothed pongid ancestor with large cranial superstructures, but from a small-toothed hominid with a rounder, smoother ectocranium, like A. africanus". Ferguson, 1989b.
"Plio-Pleistocene hominids had markedly abbreviated [enamel] growth periods relative to modern man, similar to those of the modem great apes". Bromage & Dean, 1985.
"Enamel thickness has been secondarily reduced in the African apes and also, although at a different rare and extent, in the orang-utan. Thick enamel, previously the most important characteristic in arguments about the earliest hominid, does not therefore identify a hominid". Martin, 1985 (but Beynon et al., 1991).
In the South African fossils including Taung, "sulcal patterns of seven australopithecine encocasts appear to be ape-like rather than human-like". Falk, 1987.
"Cranial capacity, the relationship between endocast and skull, sulcal pattern, brain shape and cranial venous sinuses, all of these features appear to be consistent with an ape-like external cortical morphology in Hadar early hominids". Falk, 1985.
In the type specimen of A. afarensis, "the lower third premolar of ‘A. africanus afarensis’ LH-4 is completely apelike". Ferguson, 1987b.
"A. afarensis is much more similar cranially to the modern African apes than to modern humans". Schoenemann, 1989.
"Olson's assertion that the lateral inflation of the A.L. 333-45 mastoids is greater than in any extant ape is incorrect if the fossil is compared to P. troglodytes males or some Gorilla mates and females. Moreover, the pattern of pneumatization in A. afarensis is also found only in the extant apes among other hominoids". Kimbel et al., 1984.
"Prior to the identification of A. afarensis the asterionic notch was thought to characterize only the apes among hominoids. Kimbel and Rak relate this asterionic sutural figuration to the pattern of cranial cresting and temporal bone pneumatization shared by A. afarensis and the extant apes". Kimbel et al., 1984.
"... the fact that two presumed Paranthropus [robustus] skulls were furnished with high sagittal crests implied that they had also possessed powerful occipital crests and ape-like planum nuchale... Nuchal crests which are no more prominent - and indeed some less prominent - will be found in many adult apes". Zuckerman, 1954b.
In Sts.5, MLD-37/38, SK-47, SK-48, SK-83, Taung, KNM-ER 406, O.H.24 and O.H.5, "craniometric analysis showed that they had marked similarities to those of extant pongids. These basicranial similarities between Plio-Pleistocene hominids and extant apes suggest that the upper respiratory systems of these groups were also alike in appearance... Markedly flexed basicrania [are] found only in modern humans after the second year...". Laitman & Heimbuch, 1982.
"The total morphological pattern with regard to the nasal region of Australopithecus can be characterized by a flat, non-protruding nasal skeleton which does not differ qualitatively from the extant nonhuman hominoid pattern, one which is in marked contrast to the protruding nasal skeleton of modern H. sapiens". Franciscus & Trinkaus, 1988.

Table 2 - Quotations on gorilla-like features in large East African australopith crania

"Incisal dental microwear in A. afarensis is most similar to that observed in Gorilla". Ryan & Johanson, 1989.
The composite skull reconstructed mostly from A.L.333 specimens "looked very much like a small female gorilla". Johanson & Edey, 1981, p. 351.
"Other primitive [or advanced gorilla-like? M. V.] features found in KNM-WT 17000, but not know or much discussed for A. afarensis, are: very small cranial capacity; low posterior profile of the calvaria; nasals extended far above the frontomaxillar suture and well onto an uninflated glabella; and extremely convex inferolateral margins of the orbits such as found in some gorillas". Walker et al., 1986.
As for the maximum parietal breadth and the biauriculare in O.H.5 and KNM-ER 406 "the robust australopithecines have values near the Gorilla mean: both the pongids and the robust australopithecines have highly pneumatized bases". Kennedy, 1991 (see also his fig. 1).
In O.H.5, "the curious and characteristic features of the Paranthropus skull... parallel some of those of the gorilla". Robinson, 1960.
The A. boisei "lineage has been characterized by sexual dimorphism of the degree seen in modern Gorilla for the length of its known history". Leakey & Walker, 1988.
A. boisei teeth showed "a relative absence of prism decussation"; among extant hominoids, "Gorilla enamel showed relatively little decussation ...". Beynon & Wood, 1986 (cf. Beynon et al., 1991).

Table 3 - Quotations on chimp-like features in South African australopith crania

"Alan [Walker] has analysed a number of Australopithecus robustus teeth and they fall into the fruit-eating category. More precisely, their teeth patterns look like those of chimpanzees... Then, when be looked at some Homo erectus teeth, be found that the pattern changed". Leakey, 1981, pp. 74-75.
"The ‘keystone’ nasal bone arrangement suggested as a derived diagnostic of Paranthropus [robustus] is found in an appreciable number of pongids, particularly clearly in some chimpanzees". Eckhardt, 1987.
"P. paniscus provides a suitable comparison for Australopithecus [Sts.5]; they are similar in body size, postcranial dimensions and... even in cranial and facial features". Zihlman et al., 1978.
"A. africanus Sts.5, which... falls well within the range of Pan troglodytes, is markedly prognathous or hyperprognathous"". Ferguson, 1989a.
In Taung, "I see nothing in the orbits, nasal bones, and canine teeth definitely nearer to the human condition than the corresponding parts of the skull of a modern young chimpanzee". Woodward, 1925.
"The Taung juvenile seems to resemble a young chimpanzee more closely than it resembles L338y-6", a juvenile A. boisei. Rak & Howell, 1978.
"In addition to similarities in facial remodeling it appears that Taung and Australopithecus in general, had maturation periods similar to those of the extant chimpanzee". Bromage, 1985.
"I estimate an adult capacity for Taung ranging from 404-420 cm², with a mean of 412 cm². Application of Passingham’s curve for brain development in Pan is preferable to that for humans because (a) brain size of early hominids approximates that of chimpanzees, and (b) the curves for brain volume relative to body weight are essentially parallel in pongids and australopithecines, leading Hofman to conclude that ‘as with pongids, the australopithecines probably differed only in size, not in design’". Falk, 1987.
In Taung, "pneumatization has also extended into the zygoma and hard palate. This is intriguing because an intrapalatal extension of the maxillary sinus has only been reported in chimpanzees and robust australopithecines among higher primates". Bromage & Dean, 1985.
"That the fossil ape Australopithecus [Taung] ‘is distinguished from all living apes by the... unfused nasal bones…’ as claimed by Dart (1940), cannot be maintained in view of the very considerable number of cases of separate nasal bones among orang-utans and chimpanzees of ages corresponding to that of Australopithecus". Schultz, 1941.

Only a few possibly relevant data linking an australopith fossil with one of the extant African hominoids could be obtained from the literature (cf. Tables 2 and 3). Uniquely derived cranial features of A. boisei and Gorilla concern: some incisal microwear features (Ryan & Johanson, 1989; though acquired ontogenetically, tooth wear reflects phylogenetic adaptations); enamel prism decussation (Beynon & Wood, 1986; cf. Beynon et al., 1991); orbital morphology (KNM-WT 17000, see Walker et al., 1986); body size (but see also McHenry, 1991). Uniquely derived features of South African australopiths with Pan and Homo concern: mandibular premolar root morphology (Wood et al., 1988; see also below). Uniquely derived features of A. robustus and Pan concern: tooth microwear (e.g. Leakey, 1981, p.74); nasal bone arrangement (Eckhardt, 1987); maxillary sinus topology (Bromage & Dean, 1985; see also Cave & Wheeler Haines, 1940). Not obtained were: uniquely derived features of South African fossils with Gorilla; of A. boisei with Pan; and of any australopith with Homo (i.e. features that are absent from all African ape species, mature and immature). Jenkins (1991):

"Tobias (1988) prepared a comparative list of the cranial, mandibular, dental and endocranial traits for H. habilis, A. africanus, A. robustus, and A. boisei to determine evidence for cladogenetic relationships. His tabular summaries enumerate numerous shared derived characters of all four taxa. However, he did not include any outgroup comparisons. In this poster, data for two outgroups [? M. V.], composed of Gorilla gorilla and Pan troglodytes, were compiled and compared to Tobias’ evaluations of H. habilis, A. africanus and A. boisei. The results show that numerous traits he used are also shared with Gorilla and Pan..."

Thick molar enamel and small anterior dentition are discussed above. Orthognathism, inter- mediate position of foramen magnum, relatively "short" arms, lateral plantar process of calcaneus, longer and adducted first metatarsals, etc. are seen in bonobos or/and immature apes. Lucy’s short ilium is not a good case: overall, her pelvis is as distinct from the human as it is from the chimpanzee’s (e.g. Stern & Susman 1983), and the Sterkfontein Sts.14 pelvis (notably the ischium) is even more chimp-like (Broom & Robinson, 1950; Oxnard, 1984, fig. 10.1); short ilia (in proportion to trunk length) as in monkeys and humans are probably the ancestral condition, so that Coon (1954) could assert that, in pelvic morphology, apes look less like monkeys than humans do (cf. Schultz, 1950, fig. 6). W. L. Straus (in Schultz, 1936, p. 431):

"The human ilium would seem most easily derived from some primitive member of a preanthropoid group, a form which was lacking many of the specializations, such as reduction of the iliac tuberosity and anteacetabular spine and modification of the articular surface, exhibited by the modern apes. I wish to emphasize here that the anthropoid-ape type of ilium is in no sense intermediate between the human and lower mammalian forms. Its peculiar specializations are quite as definite as those exhibited by man, so that it appears very unlikely that a true anthropoid-ape form of ilium could have been ancestral to the human type".

Overall, the more human-like features of the australopith hindlimbs are less abundant than the more ape-like features (summarized in Oxnard, 1984, Nota Bene following p. 334; and in Verhaegen, 1990). Moreover, it has been argued that all these human-like features (e.g. the superhumanly broad sacrum, long femoral neck and valgus knee) could have been correlated with some sort of bipedalism in the ancestral African hominoids (see the discussion above).

With the apparent exception of the front teeth reduction and the relative orthognathism in A. boisei and A. robustus (but juvenile African apes also are orthognathic, see Schmid & Stratil, 1986; Aiello & Dean, 1990, p. 197), later large australopith skulls (KNM-WT 17000) show more gorilla features than earlier ones (from A.L.333), and later smaller ones show more chimpanzee features than earlier ones (Taung more than Sts.5, and much more than Lucy). See, for instance, the first quotation of Table l; for KNM-WT 17000, Table 2; for Taung, Table 3, and Falk et al. (1989); and for Lucy, Ferguson (1987b).

(The same could be true of the postcrania: see Verhaegen (1990) and the discussion of the distal humerus below. Nevertheless, most Kromdraai and Swartkrans remains are usually described as being intermediate between humans and chimps but more human- than ape-like (especially the lower limb features, e.g. the adducted hallux), and more human-like than those of Hadar (Susman, 1989; Gebo, 1992). This does not necessarily contradict the evolutionary trees proposed in this paper: (1) although most Swartkrans fossils certainly belong to A. robustus, a few probably represent Homo (Susman, 1989); (2) the earliest split is not that between humans and (African) apes, but that between Pan-Homo and Gorilla (see below), and A. robustus undoubtedly belonged to Pan-Homo rather than to Gorilla; (3) at the time of A. robustus there already existed much more humanlike fossils (e.g. KNM ER-1470 and -148l), so that A. robustus must have belonged either to Pan or to an extinct side-branch of Pan-Homo; (4) prenatal apes show adducted great toes (see above), and Pan (notably paniscus) is more bipedal than Gorilla).)

In spite of the scarcity of comparative data from single sources, a few figures regarding skulls and dentitions (the postcrania are briefly discussed in Verhaegen, 1990) are brought together in Table 4a (comparative measurements from different sources were not used), and some preliminary conclusions emerge from it (Table 4b):

(1) The figures of the large afarensis skulls from A.L.333 are rather ape-like, with more bonobo-like foramen magnum indices, chimp-like frontal bone, and rather gorilla-like dental features.

(2) Overall, A. africanus from Makapansgat and Sterkfontein resemble Pan rather than Gorilla or Homo, and in bite force and foramen magnum indices, bonobos rather than common chimps.

(3) The figures of A. robustus from Swartkrans, mostly regarding the dentition, are generally intermediate between those of common chimp and gorilla.

(4) A. boisei KNM-ER 406 and O.H.5, in spite of the differences between them, are more gorilla-like (KNM-ER 406 is even super-gorilla in bite force).

Every australopith species in this Table thus appears morphologically nearer to at least one of the African ape species than it is to humans.

Robust polyphyly?

Biomolecular results leave no doubt that Pan is genetically closer to Homo than to Gorilla (e.g. Goodman, 1982; Hasegawa et al., 1985, 1987, 1988; Caccone & Powell, 1989; Sibley et al., 1990; Gonzalez et al., 1990; Ruvolo et al., 1991; Begun, 1992), and contrary to the prevailing opinion this is not contradicted by the anatomical evidence (Groves & Paterson, 1991). This implies that the African hominoids first split into Pan-Homo (smaller, relatively gracile) and Gorilla (larger, super-robust), and that many of the traits that common chimps share with gorillas but not with bonobos or humans could have developed in parallel with gorillas (e.g. very long and sexually dimorphic canines, "very" dorsal foramen magnum, ectocranial crests, arms considerably longer than legs). Convergent and parallel, even reverse or fluctuating evolution of anatomical traits are among the commonest features of biological evolution (e.g. Trinkaus, 1990; Hartman, 1989; Sheldon, 1988; Seger, 1987; Gibbs & Grant, 1987; Cartmill, 1982; White & Harris, 1977; Darwin, 1903, p.171), and the final proof that Darwinism is not a tautology. "Parallel evolution occurs when two species adopt a lifestyle that is more or less similar. If the lifestyle is essentially identical, and the species from a similar genetic background, the end result may be almost indistinguishable to other than detailed examination" (R. G. Silson, pers. comm.).

The very long canines and very dorsal foramen magnum of adult gorilla and common chimp males (but not of subadult African apes nor of adult bonobos) could well be derived and rather recent adaptations to the same environmental (e.g. in response to climatic) changes and cannot be explained by mere allometry. Even knuckle-walking of chimps and gorillas has been argued to have arisen independently (Begun, 1992), possibly in more bipedal ancestors (Kleindienst, 1975; Hasegawa et al., 1985; Edelstein, 1987). Indeed, Gorilla knuckle-walking anatomy and ontogeny are much better developed than in Pan, and are different from Pan (Inouye, 1992). And the LCA (the last common ancestor of Homo and Pan) had not yet acquired knuckle-walking since humans do not at any age show the slightest trace of knuckle-walking behaviour: (1) we lean (e.g. on a table) far more comfortably on our proximal than on our middle hand phalanges; (2) whereas in knuckle-walking apes the middle hand phalanges are naked, in many men they are dorsally haired, and fingers III and IV (that bear most weight in knuckle-walkers) even more frequently than V and II (Harrison, 1958; Singh, 1982; Ikoma, 1986); (3) "human infants walk or run spontaneously on all fours and this invariably with the palms flat on the ground and the fingers completely extended" (Schultz, 1936, p. 264).

Lucy’s arms were much shorter than a bonobo's (humerus 24 cm vs 29 cm; cf. 26 cm in human pygmies) and lacked knuckle-walking adaptations (Jungers, 1982; Stern & Susman, 1982), but later the small hominid O.H.62 had more chimp- and bonobo-like proportions (Korey, 1990; Aiello & Dean, 1990, p. 258; Wood, 1992, box 2), and the larger KNM-ER 1500 (probably a boisei female) showed some gorilla-like proportions, e.g. relatively large forelimbs (McHenry, 1978, 1992). While the early KNM-KP 271 distal humerus was "similar to that of modern man" (Senut, 1980; cf. Oxnard, 1984, fig.10.12; and Aiello & Dean, 1990, p. 365 and p. 368), A. robustus TM 1517 was more chimp-like, and A. boisei KNM-ER 739 more gorilla-like (Senut, 1980; Aiello & Dean, 1990, pp. 365-368). Body weight estimations for robustus and boisei based on formulae for ape postcrania fit much better with the massive jaws than estimations based on human formulae (see McHenry, 1991). The boisei ulnae O.H.36 and L.40-19 and humerus KNM-ER 739 were of gorilla robusticity and length (McHenry, 1991, 1992; Howell & Wood, 1974; Senut, 1980; Leakey, 1971; Aiello & Dean, 1990, p. 367-369), and the curvature and the cross-section of L.40-19 are reminiscent of knuckle-walkers (Howell & Wood, 1974); "the Rudolf australopithecines, in fact, may have been close to the ‘knuckle-walker’ condition, not unlike the extant African apes" (Leakey, 1971). Their arm lengthening and strengthening is paralleled ontogenetically in the African apes; Rensch (1972, p. 45) even states that "it is only after birth that an ape’s arms become disproportionally long", but this can only be true when arm growth relative to the height in African apes is compared with monkeys (Schultz, 1936, fig. 15).

The possibility should be considered that robustus and boisei did not belong to the same (robust) branch, but that their robust traits represented parallel adaptations (cf. Delson, 1987; Grine, 1987; Trinkaus, 1990; Conroy, 1990, fig. 6.40.d). Indeed, super-robust specimens from East Africa (KNM-WT 17000) appeared in the fossil record before the less robust A. robustus from South Africa, and the morphological differences between africanus and robustus are less than those between robustus and boisei (e.g. Leakey, 1959, 1960; Wood, 1978; Wood & Chamberlain, 1987). This is particularly clear in dental morphology (Hunt & Vitzthum, 1986; Wood & Uytterschaut, 1987; Wood & Engleman, 1988; Wood et al., 1988). An analysis of root morphology in mandibular premolars, for instance, revealed moderate root reduction in A. africanus, A. robustus and P. troglodytes, pronounced reduction in Homo but root molarization in A. boisei compared with A. afarensis, G. gorilla and most higher primates (Wood et al., 1988).

Possible evolutionary trees of the australopithecines are obscured by the incompleteness of the fossil material, by parallel (e.g. boisei/robustus) or even reverse evolution of some anatomical characters, by mosaic evolution and retention of ancestral characters in some branches (stagnations, and "sudden" accelerations of certain features). Nevertheless, some relationships seem to emerge (Figure 1):

(1) In East Africa, A. boisei – and perhaps some larger afarensis from A.L.333 or Laetoli as well – is morphologically (Tables 2 and 4), and therefore probably cladistically closer to Gorilla than to Pan or Homo. (This does not imply that some of their anatomical features cannot be closer to humans or to chimpanzees than to gorillas. Nor that (all) gorillas must descend from A. boisei. Biomolecular data suggest that the difference between highland and lowland gorilla - like that between common chimp and bonobo - is less than half that between man and chimp (Gribbin & Cherfas, 1983, p. 137), i.e. highland and lowland gorillas possibly diverged 3-2 Myr BP. In view of the small anterior dentition of A. boisei, the possibilities should be considered that some or all gorillas descend from a form nearer to KNM-WT 17000 than to A. boisei, or - the prevailing opinion - that fossil ancestors of gorillas have not been discovered yet.)

Since Homo and Pan diverged probably one or two million years later than Pan-Homo and Gorilla (e.g. Ruvolo et al., 1991), it is not surprising that Wood (1978), in a classification of East African fossil hominids, states that "by relying solely on morphology, the taxa presented are most obviously subdivided into the ‘robust’ australopithecine taxon Australopithecus boisei, and another group consisting of all the remaining taxa... In contrast to the conformity within the ‘robust’ lineage the ‘non-robust’ hominids display a wide range of variation".

(2) South African australopiths (Tables 3 and 4) - and probably some very small specimens from East Africa such as Lucy or "H. habilis" as well (cf. Zihlman, 1985; Ferguson, 1987a,b, 1992; Wood, 1978, 1992a,b) - show more affinities with Pan-Homo than with Gorilla. A striking example is the incus bone SK 848, which is clearly more like Homo or Pan than like Gorilla (Rak & Clark, 1979, fig. 1). Because A. robustus lived at the time of KNM-ER 1470 (probably an early Homo), and Taung lived even later (Partridge, 1973, 1985), they could have belonged to the Pan clade but not to the Homo clade. Taung’s endocast, dentition, facial growth and possibly foramen magnum position strikingly resemble those of apes and chimpanzees (Falk et al., 1989). Simons (1989):

"Dart’s enthusiasm for A. africanus as a human ancestor was occasioned by his misidentification of the lamboid structure as the lunate sulcus and thus reading a human-like sulcal pattern in the natural endocast of the brain of the Taung child".

Discussion

Why are many paleoanthropologists so reluctant to consider just the possibility that some or all of the australopithecines could have been evolutionarily nearer to one of the African apes than to humans?

(1) When paleoanthropologists discover fossil remains, they often - understandably - tend to stress the human-like features of their finds. Subsequent researchers, however, frequently obtain more detached views.

(2) Man is often considered to possess a great number of features that are uniquely derived from the supposed "primitive hominoid condition": thick enamel, short canines, forward position of the foramen magnum, short ilia, non-grasping feet, low intermembral index, etc. But the primitive hominoid condition is largely hypothetical: as discussed above, man seems to be more primitive in some of these features than the apes (e.g. thick enamel, low pelvis); and in many features the differences between the ape species (e.g. between Pongo and Gorilla) are larger than those between humans and some of the apes (e.g. relative arm length, foot shape). Most probably the ancestral hominoids were neither like humans nor like any of the extant ape species.

(3) In the same way, it is often uncritically accepted that the LCA was much more chimp- than human-like. As Hasegawa et al. (1985) say:

"It is unknown whether the last common ancestor of human and chimpanzee was like the living chimpanzee or like the living human. However it seems to have been widely assumed implicitly that the common ancestor of the two species was more like the chimpanzee than the human. There has been a tendency to view hominid features as specialized and those of apes as unspecialized. Any fossil hominoids that bear some resemblance to humans have been readily considered to be human ancestors".

Such assumptions are reinforced by using terms like "primitive", "plesiomorphic" or "less advanced" (which imply that the ancestral character is known), where the more neutral "apelike" or (if possible, and more precisely) "chimp-like", "bonobo-like" or "gorilla-like" would be preferable. The anthropocentric fallacy enshrined in the usage of "primitive" has more than once been challenged (Gribbin & Cherfas, 1993; Edelstein, 1987; Verhaegen, 1990). Since homoplasy, convergence, and reverse (and even fluctuating) evolution are so common, ontogeny may provide more reliable criteria to decide what is primitive (Trinkaus, 1990; cf. Northcutt, 1990). "Morphological characters can be subjected to parallel or convergent evolution, and cannot be used with confidence for phylogenetic reconstructions unless the probability of parallel evolution is evaluated or rejected in a proper way" (Hasegawa et al., 1987).

As we go further back in time, we may expect that human ancestors become more chimpanzee-like, but also that the chimpanzees’ ancestors become more human-like, i.e. display a few human-like features. Assuming that the LCA looked much more like a chimpanzee than a human and that subsequently humans have evolved much more than common chimps is statistically less likely than assuming that the LCA already possessed a few mosaic human-like features (e.g. facultative bipedalism, orthognathism, thicker enamel) and that both branches (Homo and Pan) underwent evolutionary changes towards their present-day representants (e.g. much longer legs in humans, longer arms in chimps). In fact, it seems most economical to assume that the LCA 8-4 Myr BP looked somewhat like bonobos (or like subadult chimpanzees), which are in several instances - but not, for instance, in body weight - intermediate between humans and common chimps, e.g. in relative canine size, canine dimorphism, orthognathisrn, foramen magnum indices, relative arm and leg lengths, bipedalism and knuckle-walking. Although the LCA lived earlier, the gracile australopiths of 3-2.5 Myr BP (Lucy, Sterkfontein) are the best approximation we presently have: see Aiello & Dean (1990, p. 254), or in Table 3 the quotation of Zihlman et al. (1978).

It seems that, while our ancestors were becoming more and more human-like, the African apes - at first the ancestor of the gorillas and shortly thereafter that of both chimpanzees - for unknown reasons (climatic and habitat changes?) - broke away from our evolutionary direction, partially reversed their evolution, and became again - the three species to different degrees - more like monkeys in thinner enamel, larger front teeth, prognathism, ectocranial crests, relatively smaller endocast, more dorsal foramen magnum, elongated iliac blades, short femoral necks, less valgus knees, more grasping feet, quadrupedalism, etc. (but not, for instance, in body size, relative arm length, knuckle-walking, pelvic height, number of lumbar, sacral and coccygal vertebrae).

There are admittedly several weak spots in this scenario: the many reversals (notably in the lower limb anatomy) and parallelisms (e.g. anterior dentition, iliac anatomy, knuckle-walking adaptations) in the evolution of Gorilla and Pan. (If Pongo is included in the comparison, even more - apparently improbable - parallelisms are needed, although, as discussed above, for most of such features (e.g. sexual dimorphism, foramen magnum position, relative arm length, foot shape), at least one African ape species can be found to be more different from orangs than from humans, and Andrews (1992), in a review of Miocene hominoids, even asserts that "if Sivapithecus belongs in the orangutan clade, as I have argued, the shared [postcranial] morphology of the orang-utan and the African apes must have arisen independently").

However, if these reversals and parallelisms are correlated (re-adaptations to, for instance, an older, less "innovating" or less human-like lifestyle or environment), the counter-argument to my scenario fails. Moreover, the traditional hypothesis - that all australopithecines are more closely related to humans than to African apes - seems to have more serious difficulties, since it does not explain: (1) the apparent complete absence of fossil ancestors or relatives of any African ape; (2) the various australopith-like features that are present in premature though not in adult African apes (e.g. orthognathy, less dorsal foramen magnum, more humanlike feet); (3) the fact that all australopiths lack the uniquely derived bony features which set man (at least since H. erectus) clearly apart from the other catarrhines (e.g. external nose, very large brain, very long legs), and that they resemble the apes in these respects; (4) that every one of the australopith species has more features in common with either gorillas or chimpanzees than with humans (e.g. Tables 2, 3 and 4); (5) and that at the time of the robust australopiths there already lived more humanlike creatures (KNM-ER 1470).

(Oxnard’s (1984, p. 307-332) proposition - that the australopiths were evolutionarily nearly equidistant from African apes and humans and left no descendants today - does not have the fifth difficulty. Also, in my opinion, Oxnard correctly states that many australopith postcrania were biomechanically unique, and could have represented adaptations to a well-defined lifestyle (e.g. Verhaegen, 1992).)

Conclusion

A review of the paleo-anthropological literature reveals no data that exclude the possibility that both gorillas and chimpanzees could have had australopith ancestors. Bipedalism is generally considered to be the shared feature that links australopithecines with humans, and there is no doubt that at least some of the australopith species were partial bipeds. But it has never been proven that the African apes’ unique locomotion (plantigrade knuckle-walking) could not have evolved from some kind of ("short"-legged) bipedalism. In fact, insofar as the fragmentary fossil material and the incomplete comparisons with extant apes allow, ontogenetic and morphological evidence tends to favour the hypothesis that the last common ancestor of Homo and Pan 8-4 Myr BP was a partially bipedal, gracile australopith with chiefly a mosaic of human and chimpanzee (esp. bonobo) features: low sexual dimorphism, minimal prognathism, slightly enlarged canines, non-protruding nasal skeleton, smooth ectocranium without crests, "small" brain with ape-like sulcal pattern, relatively non-flexed basicranium, intermediate position of foramen magnum, "short" forelimbs without knuckle-walking features, low ilia, (very) long femoral necks, "short" legs, (very) valgus knees, full plantigrady, longer and not very abductable halluces.

I expect that when australopith fossil material is re-examined and compared in detail with every one of the large hominoids, in most cases it will resemble either Pan or Gorilla more closely than it resembles Homo and certainly Pongo.

Acknowledgments – I wish to thank A. S. Ryan, M. Goodman, M. Hasegawa, R. G. Silson, M. R. Kleindienst, E. Morgan and especially J. Verhulst for their corrections and comments on various versions of this manuscript.

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Table 4A - Measurements of australopithecine, African ape and human skulls

foramen magnum indices^a 333-45 Sts.5 O.H.5 ER-406 Pt Pp Peking

- basion I (51.4) 43.7 54.9 40.5 33.3 41.6 81.1

- basion II (77.2) 66.2 69.3 (57.1) 52.0 61.3 87.2

- opisthion I (15.9) (14.2) 27.6 15.6 11.2 16.3 31.8

- opistbion II (21.3) (19.4) 33.3 (20.6) 16.2 22.1 33.5

frontal bone indices^b recon. Sts.5 SK-48 O.H.5 ER-406 Gorilla Pt Peking

- B at post-orb.constrict.(mm) 66.0 64.0 (67.0) 69.4 62.0 69.0 70.5 96.0

- minimum frontal B (mm) - 48.0 (27.0) (25.0) 31.0 44.2 54.7 86.0

- fronto-temporal B index - 75.0 40.3 36.0 50.0 64.1 77.4 89.6

- superior facial B (mm) 107.0 93.5 (100.0) 115.5 114.0 125.3 106.2 121.0

- inner biorbital B (mm) 94.0 84.2 (93.0) 97.0 100.0 105.1 90.0 111.0

- fronto-facial B index 62.0 68.4 65.7 60.3 54.4 55.5 66.6 79.3

- fronto-biorbital B index 78.6 76.0 72.0 71.5 62.0 66.0 78.4 86.5

rel.H ant.masseter origin^c recon. Sts.5 SK-48 O.H.5 ER-406 Gorilla Pt Homo

- zygomax.-alveolar margin 24.0 32.0 38.3 36.0 40.0 36.4 24.6 18.1

- orbitoalveolar H (47.5) 51.0 61.0 75.1 62.0 71.3 51.2 41.3

- zm-alv/lorb-alv.index 50. 5 62.7 62.8 47.9 64.5 51.2 48.0 43.8

mandibula^drecon. Sts.7 SK O.H.5 Natron Gorilla Pt Homo

- ramus H (mm) 55.0 61.0 60.7 65.0 47.0 67.0 43.1 35.9

- ramus B (mm) 55.0 46.8 54.5 - 52.8 62.5 46.4 37.4

- H/B % 100.0 130.0 111.4 - 89.0 108.0 92.9 94.7

mandibular fossa ^e MLD A.rob. O.H.5 G male Pt male Homo

- L (mm) 22.7 26.7 27.8 27 25 25.0

- B (mm) 30.4 31.9 34.4 46 29 23.8

- D (mm) 7.8 9.5 8.7 10 7 14.5

- L/B % 74.6 83.5 81.1 58.7 86.3 99.0

- D/L % 34.2 35.8 31.2 37.1 27.9 61.4

- D/B % 25.5 29.8 25.2 22.1 24.1 60.8

bite force^f recon. Sts.5 SK-48 ER-406 Gorilla Pt Pp Homo

- infratemporal fossa (cm²) (16.0) 9.7 (11.0) 18.3 17.5 12.7 7.5 7.2

- molar crown are (cm²) 5.38 5.87 5.73 8.92 6.42 3.53 2.45 2.86

- bite force equivalent M² 13.9 7.8 12.2 18.0 15.6 10.9 6.6 6.7

- bite force equivalent at I 9.2 5.3 9.O 12.0 9.4 6.5 3.9 4.3

incisal microwear^g A.afar. Gorilla Pt Eskimo

- wear striae (/mm²) 4.40 3.02 5.27 6.85

- pits (/mm²) 2.17 1.87 3.87 2.17

- pit diameter (mm) .07 .06 .06 .18

- wear striation orientation 61° 60° 37° 17°

Table 4A-4B - Legend

H human(like); Pt common chimp(like); Pp pygmy chimp(like); G gorilla(like); G>P, P>G apelike; Pp? like Pt, but possibly even more like Pp (no figures available for Pp);

+ very much like ... ; - well outside African hominoid range;

B breadth; D depth; H height; L length;

recon. reconstruction of large A.afarensis; 333-45 large A.afarensis from A.L.333-45;

Sts.5, Sts.7 A.africanus from Sterkfontein; MLD A.africanus MLD-37138 from Makapansgat;

SK mean of A.robustus SK-12, SK-23 and SK-34 from Swartkrans;

O.H.5, ER-406 A.boisoi from Olduvai and Turkana; Natron from Peninj River;

Peking H.erectus; Eskimo H.sapiens.

In extant hominoids, measurements are means of males and females, unless mentioned otherwise.

^aKimbel et al., 1984, table 9 ^e Tobias, 1968, table 1

^b ibid., table 6 ^fDemes & Creel, 1988, table 1 and 2

^c ibid., table 5 ^g Ryan et al., 1989, table 21

^d ibid., table 2

Table 4B - Australopiths compared with African hominoids

foramen magnum indices^a 333-45 Sts.5 O.H.5 ER-406 (Gorilla??)

- basion I Pp Pp+ Pp Pp+

- basion II He Pp Pp Pp>Pt

- opisthion I Pp+ Pp He Pp+

- opistbion II Pp+ Pp>Pt He+ Pp

frontal bone indices^b recon. Sts.5 SK-48 O.H.5 ER-406 (Pp??)

- B at post-orb.constriction G>P G>P G>P+ G>P+ G>P

- minimum frontal B (mm) G>P G- G- G-

- fronto-temporal B index P+ G- G- G-

- superior facial B (mm) P+ Pp? P H>PG H>PG

- inner biorbital B (mm) Pp? Pp? P P>G G>P

- fronto-facial B index P>G P+ P+ G>P G+

- fronto-biorbital B index P+ P+ G>P G>P G+

rel.H ant.masseter origin^c recon. Sts.5 SK-48 0.H.5 ER-406 (Pp?)

- zygomax.-alveolar margin P+ G>P G+ G+ G-

- orbitoalveolar H P P+ P>G G G>P

- zm-alv/lorb-alv.index G+ G>P- G>P- P+ G>P-

mandibula^drecon. Sts.7 SK 0.H.5 Natron (Pp??)

- ramus H (mm) G>P G G G+ P

- ramus B (mm) G>P P+ G>P P>G

- H/B % H>PG G- G+ P>H

mandibular fossa ^e MLD A.rob. O.H.5 (Pp??)

- L (mm) H=P G G

- B (mm) P+ P+ P

- D (mm) P G+ G>P

- L/B % P P+ P

- D/L % G>P+ G+ P

- D/B % P>G+ P>G+ P>G+

bite force^f recon. Sts.5 SK-48 ER-406 (all)

- infratemporal fossa (cm²) G Pp>t Pt G+

- molar crown area (cm²) G G G G-

- bite force equivalent M² G HP Pt>G G

- bite force equivalent at I G+ H>P G+ G-

incisal microwear^g A.afar. (Pp??)

- wear striae (/mm²) P>G

- pits (/mm²) H+

- pit diameter (mm) G>P+

- wear striation orientation G+

Figure 1 - An example of a possible evolutionary tree of fossil hominids

0 Myr BP Gg Pt Pp Hs

: : : : Hn

: : : He

1 ? : : He

Ab ? : He

Ab Ar ? He

Ab Ar O.H.62 .

2 Ab . . . ?ER-1470

. . . .

WT-17000 At ? . ?BC-1

: At ? .

3 : ?Lucy .

?A.L.333

4 ?Laetoli Gorilla gorilla

Pt Pan troglodytes

Pp Pan paniscus

Ab Australopithecus boisei

Ar A. robustus

At A. africanus transvaalensis

He Homo erectus

Hn Homo neanderthalensis

Hs Homo sapiens sapiens

4. Did Robust Australopithecines Partly Feed on Hard Parts of Gramineae?

Human Evolution 7: 63-64, 1992

Estimates of bite force suggest that Paranthropus boisei and P. robustus fed on "low-energy food that had to be processed in great quantities", "a hard object diet", "food objects... hard and round in shape" (Demes & Creel, 1988). According to studies on molar enamel microwear of South African australopithecines, "Paranthropus ate substantially more hard food items than Australopithecus" (Grine & Kay, 1988). Studies on incisal microwear suggest that "P. robustus may have ingested foods that required less extensive incisal preparation than the foods consumed by A. africanus" (Ungar & Grine, 1991), but "incisors need not be employed in the manipulation of hard objects" (Ungar & Grine, 1989). However, the precise nature of the robust australopithecine diet is still unknown.

A solution may be found in the remarkable parallelism between the dentitions of robust australopithecines, especially P. boisei, and the giant panda, Ailuropoda melanoleuca. In comparison with respectively non-robust australopithecines and non-panda bears, both have less prognathic faces, relatively smaller incisors and canine teeth, broader and heavier cheek bones, broader molars and premolars and "molarized" premolars, and thicker molar and premolar enamel (Aiello & Dean, 1990; Du Brul, 1977; Grassé, 1955). The heavy grinding apparatus of P. boisei could have been an adaptation for processing, among other things, tough parts of bamboo plants, on which giant pandas almost exclusively feed. The stalks of bamboo and other Gramineae such as sugar cane fit the description of low-energy food as well as that of hard and round food objects.

P. boisei has been discovered in former lagoons (Carney et al., 1971) and montane forests (Bonnefille, 1976), and P. robustus, near streamside or marsh vegetations (Brain, 1981, p. 189). In such environments the bamboo or reed species on which some primates feed are abundant (e.g. MacKinnon, 1978; Glander et al., 1989).

This diet is not as unlikely for a hominid as it may seem. Humans eat grains of different Gramineae (rice, com, wheat), and our closest relatives are known to feed also on harder parts of Gramineae: common chimpanzees like to chew sugar cane stalks, and young mountain gorillas love the young shoots of bamboo while the adult males crack the stalks of bamboo (MacKinnon, 1978). Other primates that cat different parts of bamboo are Rhinopithecus roxellana, Cercopithecus mitus kanditi, Callicebus moloch and three Hapalemur species (Glander et al., 1989). An electron microscope study of the enamel surface of the teeth of Gigantopithecus blacki indicates that also this fossil ape, which developed thick enamel and strongly molarized premolars in parallel with the robust australopithecines, fed partly on Gramineae, possibly bamboo (Ciochon et al., 1990).

It must be possible to test this hypothesis by comparing molar enamel microwear of Gigantopithecus, Paranthropus and Ailuropoda.

References

Aiello L. & Dean C., 1990. Human Evolutionary Anatomy, Academic Press, London.

Bonnefille R., 1976. Implications of pollen assemblage from Koobi Fora Formation, East Rudolf Kenya. Nature, 264: 403-407.

Brain C. K., 1981. The hunters or the hunted? University of Chicago Press, Chicago.

Carney J., Hill A., Miller J. A. & Walker A., 1971. Late australopithecine from Baringo District, Kenya. Nature 230: 509-514.

Ciochon R. L., Piperno D. & Thompson R. G., 1990. Opal phytoliths on the teeth of the extinct ape Gigantopithecus blacki: implications for paleodietary studies. Proceedings of the National Academy of Sciences USA, 87: 8120-8124.

Demes B. & Creel N., 1988. Bite force, diet, and cranial morphology of fossil hominids. Journal of Human Evolution, 17: 657-670.

Du Brul E. L., 1977. Early hominid feeding mechanisms. American Journal of Physical Anthropology, 47: 305- 320.

Glander K. E., Wright P. C., Seigler D. S., Randrianasolo V. & Randrianasolo B., 1989. Consumption of cyanogenic bamboo by a newly discovered species of bamboo lemur. American Journal of Primatology, 19: 119-124.

Grassé P. P., 1955. Traité de Zoologie, Masson & Cie, Paris, Vol. 1 7.

Grine F. E. & Kay R. F., 1988. Early hominid diets from quantitative image analysis of dental microwear. Nature, 333: 765-768.

MacKinnon J. R., 1978. The ape within us, Collins, London.

Ungar P. S. & Grine F. E., 1989. Maxillary central incisor wear in Australopithecus and Paranthropus. American Journal of Physical Anthropology, 78: 317.

Ungar P. S. & Grine F. E., 1991. Incisor size and wear in Australopithecus africanus and Paranthropus robustus. Journal of Human Evolution, 20: 313-340.

5. African Ape Ancestry

Human Evolution 5: 295-297, 1990

It is commonly believed that the australopithecines are more closely related to humans than to African apes. This view is hardly compatible with the biomolecular data, which place the Homo/Pan split at the beginning of the australopithecine period. Nothing in the fossil hominid morphology precludes the possibility that some australopithecines were ancestral to gorillas or chimpanzees and others to humans.

Key words: Hominid evolution, gorilla, chimpanzee, Australopithecus, Lucy, Taung.

It is commonly thought that from a period covering at least the last four million years, no fossils of ancestors of the African apes have been found so far, although hundreds of hominid fossils have been discovered from that period. The usual explanation for this remarkable absence of fossil apes is low fossilisation probability in tropical forests (where the ancestral apes presumably lived).

A more likely solution is that not only man, but also the African apes have descended from the australopithecines (e.g., Gribbin & Cherfas, 1983; Hasegawa et al., 1985; Edelstein, 1987). The molecular clock leaves little doubt that the man/chimp split occurred between 6 and 4 Myr BP (Hasegawa et al., 1985), which is in the beginning of the australopith period from about 6 (Lukeino, Lothagam) until 1 Myr BP (Taung (PostScript REMARK)).

Australopithecines are generally believed to be closer to man than to apes because of their dental and locomotor features. Like man, they have much thicker molar enamel than apes, but enamel thickness has been secondarily reduced in the African apes (Martin, 1987). The robust forms show much smaller anterior teeth than the adult males of G. gorilla and P. troglodytes (differences with the females are less). But bonobos have rather small and only slightly dimorphic canine teeth (Zihlman et al., 1978). Since the prognathism of Negroes compared with other humans developed in about 200,000 years (Cann et al., 1987), the evolution of the (indeed much more pronounced) ape prognathism in 1 Myr cannot be considered impossible.

The humanlike orientations of afarensis, distal femoral and tibial articulations (Stern & Susman, 1983), the short iliac bones of Lucy and A. africanus (McHenry, 1982), and the more central foramen magnum in the robust australopiths and Taung are thought to be correlated with bipedality. However, Gribbin & Cherfas (1983), Hasegawa et al. (1985) and Edelstein (1987) have argued that the African apes’ ancestors were more bipedal. Also bonobos have a more central foramen (Kimbel et al., 1984) and frequently walk bipedally (Zihlman et al., 1978).

The mistake of many palaeoanthropologists - the anthropocentric fallacy using «primitive» for «gorilla-» or «chimp-like» - is described by Hasegawa et al. (1985): «It seems to have been widely assumed implicitly that the common ancestor (of man and chimp) was more like the chimpanzee».

Cranial resemblances between australopithecines and apes are listed in Table 1. Also «the Homo like features of Australopithecine limb bones tend to have been greatly exaggerated in the literature (O. J. Lewis, pers. comm.). Most afarensis postcranials (AL 288, 129, 333) are different from both humans and apes, but the scapula, humerus, ulna, knee, hand and foot bones are more like apes (McHenry, 1982; Stern & Susman, 1983; Senut, 1981; Feldesman, 1982; Tardieu, 1986; Sarmiento, 1987; Deloison, 1985).

Lucy’s pelvic girdle AL 288 resembles the apes in some respects (lateral enlargement of iliac blades, small auricular and acetabular articulation surfaces, small lumbosacral angle; McHenry, 1982; Stern & Susman, 1983; Abitbol, 1987), and her upper limb looks rather bonobo-like (Stern & Susman, 1983; Feldesman, 1982). Also A. africanus scapula Sts 7 (McHenry, 1982), its hand bones (TM 1526) and those of A. robustus (SKW 14147, SK 84 and 85) are more chimp than humanlike (Lewis, 1977). The enormous L40-19 ulna of A. boisei is of gorilla size, and morphologically intermediate between man and common chimp (Feldesman, 1982).

Although the picture is confused by the retention of ancestral characters in populations that split not very long before (e.g., large and small A. afarensis) and by parallel evolution (both robust forms lived at the same time), it gives me the following impressions. A. boisei and perhaps some of the larger A. afarensis are closer to Gorilla, while Lucy and the South African australopiths show more affinities with Homo-Pan (but A. robustus, living at the time of KNM-ER 1470, could not belong to the Homo lineage). The Taung child, which lived even later (PostScript REMARK) than A. robustus, is perhaps ancestral to Pan paniscus or to Pan troglodytes.

Table l - Cranial resemblances of australopiths with apes

The australopith dentition is more apelike in development pattern (Conroy & Vannier, 1987), enamel growth rate (Bromage & Dean, 1985), dental morphology (Johanson & Edey, 1981), and enamel microwear.
All australopithecine brain endocasts appear to be ape rather than humanlike in size and sulcal pattern (Falk, 1985).
The composite A. afarensis skull (mostly AL 333; Kimbel et al., 1984) «looked very much like a small female gorilla» (Johanson & Edey, 1981).
The extensive pneumatization of the AL 333-45 temporal bone is also seen in chimpanzee males and some gorillas; «the pattern of pneumatization in A. afarensis is also found only in the extant apes among other hominoids» (Kimbel et al., 1984).
KNM-WT 17000 had «extremely convex inferolateral margins of the orbits such as found in some gorillas» (Walker et al., 1986).
«The ‘keystone’ nasal bone arrangement suggested as a derived pattern diagnostic of Paranthropus is found in an appreciable number of pongids, particularly clearly in some chimpanzees» (Eckhardt, 1987).
A. robustus incus SK 848 resembles Pan more than Homo and certainly than Gorilla (Fig. 1 in Rak & Clarke, 1979).
A. africanus Sts 5 resembles a bonobo skull (Zihlman et al., 1978).
The Taung skull has much more chimp than human traits (Bromage, 1985) and is indeed much too recent (Partridge, 1985) to be on the line to Homo.
Its «pneumatization has also extended into the zygoma and hard palate. This is intriguing because an intrapalatal extension of the maxillary sinus has only been reported in chimpanzees and robust australopithecines among higher primates» (Conroy & Vannier, 1987).

References

Abitbol M. M., 1987. Evolution of the lumbosacral angle. American Journal of Physical Anthropology, 72: 361-372.

Bromage T. G., 1985. Taung facial remodeling: a growth and development study. In: P. V. Tobias, ed. Hominid Evolution, pp. 239-245, Liss, New York.

Bromage T. G. & Dean M. C., 1985. Re-evaluation of age at death of immature fossil hominids. Nature, 317: 525-527.

Cann R. L., Stoneking M. & Wilson A. C., 1987. Mitochondrial DNA and human evolution. Nature, 325: 31-36.

Conroy G. C. & Vannier M.W., 1987. Dental development of toe Taung skull from computed tomography. Nature, 329: 625-627.

Deloison Y., 1985. Comparative study of calcanei of primates and Pan-Australopithecus-Homo relationships. In: P. V. Tobias, ed. Hominid Evolution, pp. 143-147, Liss, New York.

Eckhardt R.B. Hominoid nasal region polymorphism and its phylogenetic significance. Nature, 328: 333-335.

Edelstein S. J., 1987. An alternative paradigm for hominoid evolution. Human Evolution, 2: 169-174.

Falk D., 1985. Hadar AL 162-28 endocast as evidence that brain enlargement preceded cortical reorganization in hominid evolution. Nature, 313: 45-47.

Feldesman M. R., 1982. Morphometrics of the ulna of some Cenozoic «hominoids». American Journal of Anthropology, 57: 187.

Gribbin J. & Cherfas J., 1983. The monkey puzzle, Triad, Paladin.

Hasegawa M., Kishino H, & Yano T., 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22: 160-174.

Johanson D. C. & Edey M. A., 1981. Lucy, Granada, London.

Kimbel W. H., White T. D. & Johanson D. C., 1984. Cranial morphology of Australopithecus afarensis: a comparative study based on a composite reconstruction of toe adult skull. American Journal of Physical Anthropology, 64: 337-388.

Lewis O. J., 1977. Joint remodelling and the evolution of the human hand. Journal of Anatomy, 123: 157-201.

Martin L., 1987. Significance of enamel thickness in hominoid evolution. Nature, 314: 260-263.

McHenry H. M., 1982. The first bipeds: a comparison of the A. afarensis and A. africanus postcranium and implications for toe evolution of bipedalism. Journal of Human Evolution, 15: 177-191.

Partridge T. C., 1985. Spring flow and tufa accretion at Taung. In: P. V. Tobias, ed. Hominid Evolution, pp. 171-187, Liss, New York.

Rak Y. & Clarke R. J., 1979. Ear ossicle of Australopithecus robustus. Nature, 279: 62-63.

Sarmiento E. E., 1987. Long bone torsions of the lower limb and its bearing upon the locomotor behavior of australopithecines. American journal of Physical Anthropology, 72: 250-251.

Senut B., 1981. Humeral outlines in some hominoid primates and in Pliopleistocene hominids. American journal of Physical Anthropology, 56: 257-283.

Stern J. T. & Susman R. L., 1983. The locomotor anatomy of Australopithecus afarensis. American Journal of Physical Anthropology, 60: 279-317.

Tardieu C., 1986. The knee joint in three hominid primates: application to Plio-Pleistocene hominids and evolutionary implications. In: D. M. Taub & F. A. King, eds. Current Perspectives in primate Biology, pp. 182-192, Van Nostrand Reinhold, New York.

Walker A., Leakey R. E., Harris J. M. & Brown F. H., 1986. 2.5-Myr Australopithecus boisei from west of Lake Turkana, Kenya. Nature, 322: 517-522.

Zihlman A.L., Cronin J. E., Cramer D. L. & Sarich V. M., 1978. Pygmy chimpanzee as a possible prototype for the common ancestor of humans, chimpanzees and gorillas. Nature, 275: 744-746.

5. Letter to the Editor

Human Evolution 2: 381, 1987

Sir,

The aquatic ape theory states that our hominid ancestors spent a considerable part of their day swimming end diving in a river, lake or sea, and, at least partially, are aquatic food. The AAT is supported by our lack of body hair, our thick fat-layer and several other features absent in nonhuman primates, but widespread among aquatic mammals (Hardy, 1960; Morgan, 1982; Verhaegen, 1985).

The ability to speak is a uniquely human character. Innumerable attempts explaining it have been made, but the question how language emerged has not yet been solved. Recently it has been suggested that the origin of speech was facilitated by our aquatic past (Morgan, 1982, pp. 92-105; Morgan & Verhaegen, 1986). All aquatic mammals control their breathing «voluntarily», i.e. through the primary motor cortex. When surfaced they open the airway whenever they went to inhale air, and they can hyperventilate and then close the airway whenever they intend to dive.

The human primary motor cortex (area 4) is much larger than that of apes, mostly due to the expansion of the areas for the musculature of mouth, throat end breathing. Just in front of that enlarged area 4 lies the typically human Broca’s area. In present-day man, it coordinates the activities of the enlarged area 4, to produce the right sound on the right time. Brcoca’s area may have been originated in a previous aquatic phase to coordinate the muscles commanded by the enlarged area 4, to make the right airway muscle contract on the right time: just before, during or just after a dive. In order to use this voluntary control for improving his vocalizations, our ancestor must have been able to interpret his own sound production (feedback). This was improved by the evolution of the arcuate fasciculus, a typically human pathway between Broca’s area end Wernicke’s area (Geschwind, 1972). Wernicke’s area, a primary language area used for decoding spoken language, lies dorsal to primary auditory cortex end to the principal sensory areas for mouth end throat. In Wernicke’s area, connections could be made with other nearby association trees, and a certain sound or combination of sounds could be associated with something that our ancestor was aware of (hearing, seeing, feeling, doing) at the same time. Compared with a chimp’s brain our association areas are enormously enlarged. These areas amplified the possibilities of the sound producing apparatus: they act as the hardware of the computer, whereas the sound analysing end producing areas act as the input/output apparatus; the particular language is the software.

Most authors discussing language origins try to explain our speech capacity by an enormous improvement of vocalizing abilities that already existed in rudimentary form in prehuman primates, but fail to explain how exactly this could have occurred. In my opinion, most of these problems are readily solved by the application of the aquatic theory to the vocal and breathing apparatus.

Geschwind N., 1972. Language and the brain. Scient. Amer., 226: 76-83.

Hardy A. C., 1960. Was man more aquatic in the past? New Scient., 7: 642-5.

Morgan E., 1982. The aquatic ape. London: Souvenir.

Morgan E. & Verhaegen M., 1986. In the beginning was the water. New Scient., 1498: 62-63.

Verhaegen M., 1985. The aquatic ape theory: evidence and a possible scenario. Med. Hypoth., 16: 16-32.

PostScript REMARK: at the time these publications were written, it was believed that Taung was 1 Mya. However, Taung is probably 2 Mya or older.

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