Systematics of Miocene apes: State of the art of a neverending controversy

The term ‘ape’ is sometimes used as a synonym of ‘hominoid’—i.e., a member of the superfamily Hominoidea, which includes the families Hylobatidae (gibbons and siamang) and Hominidae (orangutans, gorillas, chimpanzees, and humans; Groves, 2017), plus their extinct relatives. However, following the most common usage of ‘apes’ as opposed to both ‘monkeys’ and ‘humans’ (e.g., Alba, 2012; Tuttle, 2014; Andrews, 2020; Almécija et al., 2021), we restrict the former term to hominoids exclusive of the human lineage (i.e., nonhominin hominoids). Originally, the term ‘ape’ broadly referred to all nonhuman anthropoids, so that nonhuman hominoids were referred to as ‘manlike apes’ (Huxley, 1863) or ‘anthropomorphous apes’ (Darwin, 1871; Huxley, 1872). Huxley (1872) formalized the term ‘anthropomorph’, subsequently used by other authors (e.g., Pocock, 1926; Delson, 1977; Szalay and Delson, 1979), but currently in disuse in the English literature. Hylobatids and nonhominin hominids are customarily referred to as ‘lesser apes’ and ‘great apes’, respectively, in allusion to their size differences (Tuttle, 2014). Extant hylobatids include more than a dozen species classified in four genera, while hominids similarly include four genera but a lower number of species (Groves, 2001, 2017). The restricted diversity of extant hominoids contrasts with that of both extant Old World monkeys and extinct apes. The latter attained a much wider geographic distribution (including Europe and mainland Asia) during the Miocene (e.g., Alba, 2012; Fleagle, 2013; Begun, 2015). As a result of the decimated current genus diversity of hominoids, making sense of their evolutionary history constitutes a monumental challenge from both adaptive and phylogenetic viewpoints (see review in Almécija et al., 2021).

This review focuses on apes recorded from the Miocene—the first geological epoch of the Neogene period, being formally divided into Early (23.04–15.99 Ma), Middle (15.99–11.65 Ma), and Late (11.65–5.33 Ma) Miocene (Raffi et al., 2020). This epoch witnessed important environmental and biotic changes (Zachos et al., 2001; Blois and Hadly, 2009; Raffi et al., 2020). The closure of the Tethys Seaway, due to the collision of the Afro-Arabian and Eurasian plates, enabled intermittent intercontinental dispersals through the Middle East from ∼19 Ma onward (Harzhauser et al., 2007), although they were temporarily interrupted during the Langhian transgression at the beginning of the Middle Miocene (∼16 Ma; Rögl, 1999). The mid-Miocene climatic optimum, a global warming event that peaked at ∼17–15 Ma, was followed by the Middle Miocene climate transition, a stepwise cooling phase that continued throughout the Late Miocene and had a profound impact on terrestrial ecosystems and mammalian communities (Flower and Kennett, 1994; Zachos et al., 2001; Kürschner et al., 2008; Foster et al., 2012; Pound et al., 2012). The geographic spread of woodland and savanna biomes throughout the Old World, and the associated Pikermian chronofauna adapted to more open and arid environments, started around the Middle to Late Miocene transition and peaked at ∼7.5 Ma (Eronen et al., 2009; Kaya et al., 2018). Toward the end of the Miocene, beginning at ∼6 Ma, a combination of tectonic and glacioeustatic factors repeatedly isolated the Mediterranean Sea from the Atlantic Ocean during the Messinian Salinity Crisis (Krijgsman et al., 1999), which favored the spread of open landscapes around the Mediterranean and the establishment of additional dispersal routes between Europe and Africa (Gibert et al., 2013).

As for many other groups, the factors outlined above played a major role in shaping hominoid evolution and adaptation (Andrews, 1992, 1996; Andrews and Bernor, 1999; Andrews and Kelley, 2007). Several books (Tuttle, 2014; Andrews, 2015; Begun, 2016) and reviews (Wood and Harrison, 2011; Begun, 2013, 2015; Andrews, 2020; Almécija et al., 2021) have been devoted to Miocene apes during the last decade, and the general picture is quite clear. Hominoids originated in Africa during the late Oligocene, experienced the first radiation in that continent during the Early and Middle Miocene, and later dispersed into Eurasia, where they experienced a second radiation during the Middle to Late Miocene. Subsequently, from the Late Miocene onward, many hominoid genera went extinct and the geographic distribution of hominoids progressively shrank to equatorial Africa and southeastern Asia—with the remarkable exception of members of the human lineage, which radiated during the Plio-Pleistocene and ultimately dispersed throughout the globe. Nevertheless, many uncertainties still persist, particularly regarding the origin of hylobatids and crown hominids (Almécija et al., 2021).

This review aims to synthesize current knowledge of Miocene ape diversity as well as to critically review their taxonomy, phylogeny, and paleobiogeography in light of the cladistic analyses published during the last decade, with emphasis on hylobatid and hominid origins. A first section with the necessary historical background is followed by an updated classification of Miocene apes and an analysis of their paleobiodiversity dynamics. Various controversial issues (the origin of hylobatids, the relationships of Oreopithecus, and the pongine–hominine divergence) are then discussed in the light of phylogenetic uncertainties highlighted by the contradictory cladistic results obtained from craniodental and postcranial data separately. We finally discuss future directions of research with an emphasis on phylogenetic inference methods.

Besides Oligocene and Plio-Pleistocene apes, which are excluded from this review by definition, Early and Middle Miocene small-bodied catarrhines from Africa of uncertain affinities have also been left out. These include dendropithecids, which have been variously considered stem catarrhines (Harrison, 2010a, 2013; Nengo et al., 2017; Gilbert et al., 2020a) or stem hominoids (Rae, 1999, 2004; Zalmout et al., 2010; Alba et al., 2015; Begun, 2015; Rossie and Hill, 2018), because we consider that currently available evidence leans against considering them hominoids—albeit recognizing that more complete remains would be required to more conclusively assess their systematic position (see Section 3.5).

Two small-bodied genera from Eurasia of debated affinities have also been excluded. Kapi ramnagarensis Gilbert et al., 2020a, based on an isolated M3 from the Middle Miocene (13.8–12.5 Ma) of India, was originally recovered as a stem hylobatid (Gilbert et al., 2020a), but subsequently reinterpreted as a pliopithecoid (Ji et al., 2022). Similarly, Pliobates cataloniae Alba et al., 2015 from the Middle/Late Miocene (11.6 Ma) of Spain, known on the basis of a partial skeleton, was originally considered a stem hominoid (Alba et al., 2015) but alternatively interpreted as a possible pliopithecoid (Benefit and McCrossin, 2015; Nengo et al., 2017; Gilbert et al., 2020a, 2020b). Pliobates displays a mosaic of plesiomorphic (stem catarrhine-like) and derived (crown hominoid-like) features (Alba et al., 2015; Bouchet et al., 2021), but work in progress by the authors supports the hypothesis that it is a stem catarrhine postcranially convergent with hominoids.

The hominin status of the Late Miocene genera Ardipithecus White et al., 1995 (∼5.8–4.4 Ma; White et al., 1994, 2009; Haile-Selassie, 2001; Haile-Selassie et al., 2004, 2009), Orrorin Senut et al., 2001 (Pickford et al., 2002; Gommery and Senut, 2006; Almécija et al., 2013), and Sahelanthropus Brunet et al., 2002 (∼7 Ma; Zollikofer et al., 2005; Guy et al., 2005; Macchiarelli et al., 2020; Daver et al., 2022) has sometimes been questioned (Wolpoff et al., 2002; Wood and Harrison, 2011; Macchiarelli et al., 2020). However, here these genera have been excluded based on the general view (e.g., Harcourt-Smith, 2010; Simpson, 2010, 2013; Pugh, 2022)—further supported by most recent cladistic analyses (Mongle et al., 2019; Pugh, 2020)—that they are early hominins.

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