Hylobatid Evolution in Paleogeographic and Paleoclimatic Context

East and Southeast Asia has one of Earth’s most complex geo-climatic histories. The region formed in a multi-step process lasting from the Paleozoic to nearly the end of the Oligocene . A profound event in the area’s history was the joining of the Afro-Arabian and Eurasian tectonic plates in the early Miocene , which enabled for the first time in history substantial exchanges of flora and fauna across the Gomphotherium Landbridge . The warm and humid climate of the Eocene had facilitated a far northerly expansion of megathermal forests, which African stem hominoids probably utilized on their migration out of Africa, through the Afro-Arabian terrestrial corridor and into Europe and Asia. Although Earth’s temperature had continuously decreased after the Eocene climatic maximum, warm-wet conditions prevailed once again during the early Miocene , which likely contributed to hominoid diversification and radiation at this time. In Asia, primate-friendly ecological conditions may have spurred the divergence of stem hylobatids from Asian stem hominoids. Following the middle Miocene climatic optimum , however, the climate changed dramatically. Average global temperature decreased while aridity increased leading to more patch-distributed forest habitats, interspersed with fast-growing grasslands. Asia’s flora and fauna were further impacted by an increasing seasonality due to intensifying monsoon seasons after the East and South Asian monsoon systems became coupled by ~17 mya. In the aftermath of the Eocene Indian-Eurasian plate collision, the Himalayan Plateau significantly rose in height at 15 mya and then again in 13 mya. Each height increase likely caused an increase in monsoon seasonality. While several Afro-Eurasian hominoids went extinct during Miocene times due to climate changes, stem hylobatids prooved to be rather resilient and adaptable: By the end of the Miocene ~6 mya, the lineage had diversified into the four genera Nomascus , Symphalangus , Hoolock , and Hylobates known today. We propose that stem hylobatids responded to climatic and ecological changes with strategies that decreased energy expenditure, and suggest that even before the emergence of the four hylobatid genera, stem hylobatids had increased their foraging efficiency by optimizing brachiation to afford them access to the terminal-branch feeding niche, and had reduced net energy demands by a decrease in body size and breeding female group size. These adaptations allowed Miocene stem hylobatids to flourish when larger bodied stem hominoids perished. As the Miocene climate deteriorated and tropical forests became compressed and fragmented, some hylobatid populations may have retreated to, or were trapped in, the climatically sheltered, deep mountain valleys of the ancient Hengduan Mountains where they, relatively unscathed, evolved into distinct lineages. The Hengduan Mountain valleys may have functioned as refugia for stem hylobatids, because the valley bottoms microclimate was less seasonal and more temperate-like. Isolation of populations was facilitated by the steepness of the Hengduan Mountains and the large rivers that drain the Tibetan Plateau and Southern Himalayas. An initial speciation and probable radiation wave, within the genera Nomascus and Hylobates , was prompted by a short period of warmer global climate during the middle Pliocene . This warmer climate led to less ocean water trapped in ice sheets and a corresponding increase in sea level of about 22 ± 10 m above current sea-levels. Island formation during this time was probably responsible for some diversification within hylobatids because proposed speciation times of Hainan gibbons, as well as Kloss gibbons and the separation of Bornean and Javan gibbons, coincide with times of relatively high sea-level stands. During the Pleistocene glaciation-interglaciation cycles a second speciation wave within Nomascus and Hylobates occurred, but this is tentatively unrelated to changing sea levels or island formation, but rather may have been a consequence of geographic separation by large paleorivers . During times of glaciations, Sundaland was a large landmass dissected by large rivers, several of which have persisted until today. Rivers continue to represent important barriers to hylobatid distribution and species separation, for example in crested gibbons, who radiated from a proposed northern latitude southward, and are now separated by large rivers. In conclusion, hylobatid evolution has been complex and inextricably linked to geologic events, which included mountain building and the formation of isolated valleys, such as those of the southern Himalayas; sea-level changes, and the creation of islands; as well Asia’s great rivers, which since the Pleistocene have played a major role in separating hylobatid populations.