Geologic Activity and Climate Change in the Miocene
The Miocene Epoch was a time of mammalian diversification and extinction, global climate change, and ecological turnover. In the Miocene, there was an initial warming trend across the globe with the expansion of subtropical forests, followed by widespread cooling and drying with the retreat of tropical forests and replacement with more open woodlands and eventually grasslands. It was also a time of major geologic activity. On one side of the globe, South America experienced the rise of the Andes Mountains. On the other side, the Indian subcontinent collided with mainland Asia, resulting in the rise of the Himalayan Mountains. In Africa, volcanic activity promoted the development of the East African Rift System. Critical to the story of ape evolution was the exposure of an intercontinental landbridge between East Africa and Eurasia, permitting a true planet of apes (Figure 8.19).
Figure \(\PageIndex{1}\): Map of the world in the Miocene, highlighting fossil ape localities.
Geographic Distribution: Africa, Asia, Europe
The world of the Miocene had tremendous ape diversity compared to today. The earliest records of fossil apes are from Early Miocene deposits in Africa. However, something dramatic happened around 16 million years ago. With the closure of the ancient Tethys Sea, the subsequent exposure of the Gomphotherium Landbridge, and a period of global warming, the Middle–Late Miocene saw waves of emigration of mammals (including primates) out of Africa and into Eurasia, with evidence of later African re-entry for some (Harrison 2010). Some of the mammals that dispersed from Africa to Eurasia and back were apes. Though most of these early apes left no modern descendants, some of them gave rise to the ancestors of modern apes—including hominins (Figure 8.20).
Figure \(\PageIndex{1}\): Representative Miocene apes set against a geologic time scale. Casanova-Vilar et al. (2011).
Where Are the Monkeys? Old World Monkey Diversity in the Miocene
Figure \(\PageIndex{3}\): Skull of Victoriapithecus macinnesi (Musee d’Histoire Naturelle, Paris).
Whereas the Oligocene deposits in the Fayum of Egypt have yielded the earliest-known catarrhine fossils, the Miocene demonstrates some diversification of Cercopithecoidea. However, compared to the numerous and diverse Miocene apes (see below), monkeys of the Miocene are very rare and restricted to a single extinct family, the Victoriapithecidae (Table 8.1). This family contains the earliest definite Old World monkeys. These monkeys are known from northern and eastern Africa between 20 million and 12.5 million years ago (Miller et al. 2009). The best known early Old World monkey is Victoriapithecus (Figure 8.21; Table 8.1), a small-bodied (approximately 7 kg; 15 lbs.), small-brained monkey with a long sloping face and round, narrowly spaced orbits. Victoriapithecus shares some cranial features with Aegyptopithecus; for example, both have a deep malar region of the zygomatic bone and a well-developed sagittal crest (Benefit and McCrossin 1997; Fleagle 2013). Beginning in the Early Miocene, and certainly by the Middle Miocene, bilophodonty, known to be a hallmark of molar teeth of modern Old World monkeys, was present to some extent. Although this dental feature is often indicative of increased leaf-processing efficiency in modern Old World monkeys, Victoriapithecus has been reconstructed as being more frugivorous and perhaps spent more time on the ground (terrestrial locomotion) than in the trees (arboreal locomotion; Blue et al. 2006). The two major groups of Old World monkeys today are cercopithecines and colobines. The earliest records demonstrating clear members of each of these two groups are at the end of the Miocene. Examples include the early colobine Microcolobus from Kenya and the early cercopithecine Pliopapio from Ethiopia.
The Story of Us, the Apes
African Ape Diversity
The Early Miocene of Africa has yielded around 14 genera of early apes (Begun 2003). Many of these taxa have been reconstructed as frugivorous arboreal quadrupeds (Kay 1977).
One of the best studied of these genera is the East African Proconsul (Family Proconsulidae; Table 8.1), a short-faced ape with generalized dentition and above-branch locomotor behaviors (Begun 2007). Several species have been described, with body mass reconstructions ranging from 17 to 50 kg (approximately 37–110 lbs.). A paleoenvironmental study reconstructed the habitat of Proconsul to be a dense, closed-canopy tropical forest (Michel et al. 2014). One of the most interesting questions about this taxon is whether or not it possessed a tail, a lack of which is an important characteristic for distinguishing living apes from Old World monkeys. No caudal vertebrae (tail bones) have been found in direct association with Proconsul postcrania, and the morphology of the sacrum is consistent with Proconsul lacking a tail (Russo 2016; Ward et al. 1991).
Overall, the African ape fossil record in the Late Miocene is sparse, with seven fossil localities dating between eleven and five million years ago (Pickford et al. 2009). Nevertheless, most species of great apes live in Africa today. Where did the progenitors of modern African apes arise? Did they evolve in Africa or somewhere else? The paucity of apes in the Late Miocene of Africa stands in contrast to the situation in Eurasia. There, ape diversity was high. Furthermore, several Eurasian ape fossils show morphological affinities with modern hominoids (apes). This has suggested to some paleoanthropologists that the ancestors of modern African great apes recolonized Africa from Eurasia toward the end of the Miocene (Begun 2002). However, discoveries of Late Miocene hominoids like the Kenyan Nakalipithecus (9.9 million to 9.8 million years ago) and the Ethiopian Chororapithecus (10.7 million to 10.1 million years ago) fuel an alternative hypothesis—namely that African hominoid diversity was maintained throughout the Miocene and that one of these taxa might, in fact, be the last common ancestor of extant African apes (Kunimatsu et al. 2007). The previously underappreciated diversity of Late Miocene apes in Africa might be due to poor sampling of the fossil record in Africa.
Eurasian Ape Diversity
With the establishment of the Gomphotherium Landbridge (a result of the closure of the Eastern Mediterranean seaway; Rögl 1999), the Middle Miocene was an exciting time for hominoid radiations outside of Africa (see Figure 8.20). Eurasian hominoid species exploited their environments in many different ways in the Miocene. Food exploitation ranged from soft-fruit feeding in some taxa to hard-object feeding in others, in part owing to seasonal fluctuations and the necessary adoptions of fallback foods (DeMiguel et al. 2014). For example, the molars of Oreopithecus bambolii (Family Hominidae) have relatively long lower-molar shearing crests, suggesting that this hominoid was very folivorous (Ungar and Kay 1995). Associated with variation in diet, there is great variation in the degree to which cranial features (e.g., zygomatic bone or supraorbital tori) are developed across the many taxa (Cameron 1997); however, Middle Miocene fossils tend to exhibit relatively thick molar enamel and relatively robust jaws (Andrews and Martin 1991).
Figure \(\PageIndex{4}\): Cast of the mandible of Gigantopithecus blacki.
One of the most extreme examples of ape robusticity is the Asian hominoid, Gigantopithecus (Table 8.1). Known only from teeth and jaws (e.g., Figure 8.22), this ape probably weighed as much as 270 kg (595 lbs.) and was likely the largest primate ever (Bocherens et al. 2017). Because of unique features of its teeth (including molarized premolars and patterns of wear) and its massive size, it has been reconstructed as a bamboo specialist, somewhat like the modern panda. Small silica particles (phytoliths) from grasses have been found stuck to the molars of Gigantopithecus (Ciochon et al. 1990). Recent studies evaluating the carbon isotope composition of the enamel sampled from Gigantopithecus teeth suggest that this ape exploited a wide range of vegetation, including fruits, leaves, roots, and bamboo (Bocherens et al. 2017).
In Spain, the cranium with upper dentition, part of a mandible, and partial skeleton of Pliobates (Family Pliobatidae), a small-bodied ape (4–5 kg; 9–11 lbs.), was discovered in deposits dating to 11.6 million years ago (Alba et al. 2015). The authors of the study reconstructed this European catarrhine as a frugivore that overlapped in relative brain size with modern cercopithecoids. The fossilized postcrania of Pliobates suggest that this ape might have had a unique style of locomotion, including the tendency to walk across the branches of trees with its palms facing downward and flexible wrists that permitted rotation of the forearm during climbing. However, the anatomy of the distal humerus differs from those of living apes in ways that suggest that Pliobates was less efficient at stabilizing its elbow while suspended (Benefit and McCrossin 2015). Two other recently described apes from Spain, Pierolapithecus and Anoiapithecus, are known from relatively complete skeletons. Pierolapithecus had a very projecting face and thick molar enamel as well as some skeletal features that suggest (albeit controversially) a less suspensory locomotor style than in extant apes (Moyà-Solà et al. 2004). In contrast to Pierolapithecus, the slightly younger Anoiapithecus has a very flat face (Moyà-Solà et al. 2009).
Figure \(\PageIndex{5}\): Skeleton of Oreopithecus bambolii.
Postcranial evidence for suspensory or well-developed orthograde behaviors in apes does not appear until the Late Miocene of Europe. Primary evidence supporting these specialized locomotor modes includes the relatively short lumbar vertebrae of Oreopithecus (Figure 8.23) and Dryopithecus (Maclatchy 2004). The Late Miocene saw the extinction of most of the Eurasian hominoids in an event referred to as the Vallesian Crisis (Agustí et al. 2003). Among the latest surviving hominoid taxa in Eurasia were Oreopithecus and Gigantopithecus, the latter of which held out until the Pleistocene in Asia and was probably even sympatric with Homo erectus (Cachel 2015).
The Origins of Extant Apes
The fossil record of the extant apes is somewhat underwhelming: it ranges from being practically nonexistent for some taxa (e.g., chimpanzees) to being a little better for others (e.g., humans). There are many possible reasons for these differences in fossil abundance, and many are associated with the environmental conditions necessary for the fossilization of bones. One way to understand the evolution of extant apes that is not so dependent on the fossil record is via molecular evolutionary analyses. This can include counting up the differences in the genetic sequence between two closely related species to estimate the amount of time since these species shared a common ancestor. This is called a molecular clock, and it is often calibrated using fossils of known absolute age that stand in for the last common ancestor of a particular clade. Molecular clock estimates have placed the split between Hylobatidae and Hominidae between 19.7 million and 24.1 million years ago, followed by an African ape and Asian ape split between 15.7 million and 19.3 million years ago, and, finally, with the more recent radiation of Hylobatidae into its current genera between 6.4 million and 8 million years ago (Israfil et al. 2011).
Lesser Ape Origins and Fossils
Unfortunately, the fossil record for the lesser apes is meager, particularly in Miocene deposits. One possible early hylobatid is Laccopithecus robustus, a Late Miocene catarrhine from China (Harrison 2016). Although it does share some characteristics with modern gibbons and siamangs (including an overall small body size and a short face), Laccopithecus most likely represents a primitive stem catarrhine and is therefore distantly related to extant apes (Jablonski and Chaplin 2009). A more likely candidate for the hylobatid stem is another Late Miocene taxon from China, Yuanmoupithecus xiaoyuan (Table 8.1). Interpretation of its phylogenetic standing, however, is complicated by contradicting dental features—some of them quite primitive—which some believe best place Yuanmoupithecus as a stem hylobatid (Harrison 2016). The history of Hylobatidae becomes clearer in the Pleistocene, with fossils representing extant genera.
Great Ape Origins and Fossils
The most extensive fossil record of a modern great ape is that of our own genus, Homo. The evolution of our own species will be covered in the next chapter. The evolutionary history of the Asian great ape, the orangutan (Pongo), is becoming clearer. Today, orangutans are found only on the islands of Borneo and Sumatra. However, Pleistocene-aged teeth, attributed to Pongo, have been found in Cambodia, China, Laos, Peninsular Malaysia, and Vietnam—demonstrating the vastness of the orangutan’s previous range (Ibrahim et al. 2013; Wang et al. 2014). Sivapithecus from the Miocene of India and Pakistan is represented by many specimens, including parts of the face. Sivapithecus is very similar to Pongo, especially in the face, and it probably is closely related to ancestral orangutans (Pilbeam 1982). Originally, jaws and teeth belonging to the former genus Ramapithecus were thought to be important in the origin of humans (Simons 1961), but now these are recognized as specimens of Sivapithecus (Kelley 2002). Postcranial bones of Sivapithecus, however, suggest a more generalized locomotor mode—including terrestrial locomotion—than seen in Pongo (Pilbeam et al. 1990).
In Africa, the first fossil to be confidently attributed to Pan, and known to be the earliest evidence of a chimpanzee, was described based on teeth found in Middle Pleistocene deposits in the Eastern Rift Valley of Kenya (McBrearty and Jablonski 2005). Paleoenvironmental reconstructions of this locality suggest that this early chimpanzee was living in close proximity to early Homo in a closed-canopy wooded habitat. Similarly, fossil teeth and mandibular remains attributed to two species of Middle-Late Miocene apes—Chororapithecus abyssinicus (from Ethiopia; Suwa et al. 2007) and Nakalipithecus nakayamai (from Kenya; Kunimatsu et al. 2007)—have been suggested as basal members of the gorilla clade.
Clearly, more work is needed to fill in the large gaps in the fossil record of the nonhuman great apes. The 20th century witnessed the discovery of many hominin fossils in East Africa, which have been critical for improving our understanding of human evolution. While 21st-century conservationists fight to prevent the extinction of the living great apes, perhaps efforts by 21st-century paleoanthropologists will yield the evolutionary story of these, our closest relatives.
Review Questions
Compare three major hypotheses about primate origins, making reference to each one's key ecological reason for primate uniqueness.
List some euprimate features that plesiadapiforms have and some that they lack.
Contrast adapoids and omomyoids in terms of anatomy and life habits.
Discuss the biogeography of the origins of African great apes and Asian great apes using examples from the Miocene ape fossil record.
