The Fossil Record and Evolutionary History of Hylobatids

Abstract

Gibbons and siamang (family Hylobatidae ) are the smallest of the extant apes and have geographically always been restricted to Asia. Their origin dates back to the beginning of the middle Miocene about 16.2 mya, a critical time when ape and human ancestors greatly diversified and when hominoids had left the African continent for the first time. The early Miocene was a warm period with equatorial forests expanding northward allowing early hominoids to colonize Europe and, through the Arabian-Indian corridor, also reach Asia. In contrast to the early Miocene, the late Miocene became a time of change caused by tectonic activity, changes in water currents, and cooling temperatures, which significantly impacted the World’s climate and in Asia led to the development of the characteristic monsoons, bringing pronounced seasonality to the region. At the end of the Miocene, many hominoid lineages had perished, but the small apes of Asia prospered and began to diversify. We suggest three key adaptations that were responsible for hylobatids success and survival: (1) perfection of forelimb suspensory locomotion (FSL) including regular, continuous ricochetal brachiation , (2) reduction of group size to small 2–4 adult groups, and (3) reduction in body size . These adaptations probably already characterized stem hylobatids since these traits are present in all extant hylobatids, before the family, after ~10.5 mya rapidly diversified into the four monophyletic genera Nomascus , Symphalangus , Hoolock , and Hylobates . The three key adaptations of hylobatids were probably all related to an overall net reduction of energy expenditure, which we hypothesize was the ultimate road to hylobatids’ success and survival under ecological conditions that were becoming increasingly challenging for large-bodied apes toward the late Miocene and into the Pliocene. In an arboreal environment, suspensory and ricochetal brachiation are more energy efficient than plantigrade quadrupedalism. In addition, brachiation increases access to difficult-to-reach, ripe fruit because it allows foraging along the thin twigs of a tree’s terminal branches. Perfection of the ancestral hominoid suspensory locomotion thus had a double-positive effect: it reduced energy expenditure and allowed hylobatids to become more competitive in fruit acquisition compared to less agile primates. Reducing average group size probably allowed hylobatids to decrease daily travel and within-group feeding competition, both mechanisms potentially adding to a decrease of net energy expenditure for foraging. Territoriality is a common corollary of pair-living in mammals and is also a characteristic of hylobatids, which further boosted a positive energy balance for the small Asian apes , because territoriality allows optimizing foraging efficiency through long-term knowledge of the spatiotemporal distribution of food sources and increased predictability of food availability. Finally, we hypothesize that the reduction in body size was perhaps the most important single adaptive response to the pressures of decreasing temperature and increasing aridity of Asian environments during the Miocene–Pleistocene transition. Body size reduction not only lowered absolute caloric need, particularly for females, but simultaneously facilitated optimizing forelimb suspensory locomotion to feed in terminal branches, which becomes uneconomical beyond the hylobatid body size. A small body may also have been the ultimate precondition for the evolution of small group size , because once females started to live in separate territories apart from each other for ecological reasons, it probably became inefficient for males to aim to defend more than one female. Pair-living may have relaxed sexual selection pressures on male morphology , which is so common in primates living in single-male/multi-female and multi-male/multi-female groups and also characterizes the large-bodied apes where large male body size often correlates with access to more females. The suite of morphological but also socio-ecological traits seen in hylobatids differ in significant ways from many traits seen in the great apes and comprehensively explain the extraordinary evolution of the small Asian apes .