Septa and processes: convergent evolution of the orbit in haplorhine primates and strigiform birds

Abstract

According to the “nocturnal visual predation hypothesis” (NVPH), the convergent eyes and orbits of primates result from selection for improved stereoscopic depth perception to facilitate manual capture of prey at night. Within primates, haplorhines share additional derived orbital morphologies, including a postorbital septum and greater orbital convergence than any other mammalian clade. While the homology and function of the haplorhine septum remain controversial, experimental data suggest that septa evolved to inhibit mechanical disturbance of the orbital contents by the anterior temporalis muscle during mastication. According to this “insulation hypothesis,” haplorhines are particularly susceptible to disruption of the orbital contents because they have large and highly convergent eyes and orbits. However, comparative tests of the insulation hypothesis have been hindered by the morphological uniqueness of the haplorhine septum among mammals. Among birds, owls (Strigiformes) exhibit an expanded postorbital process that may be functionally analogous to the haplorhine septum. Here we present a comparative analysis of orbital morphology in 103 avian species that tests two hypotheses: (1) large, convergent orbits are associated with nocturnal visual predation, and (2) the strigiform postorbital process and haplorhine postorbital septum similarly function to insulate the eyes from contractions of mandibular adductors. Strigiforms, as nocturnal visual predators, possess relatively large orbits and exhibit the highest degree of orbital convergence in our sample. Notably, orbital convergence does not scale with orbit size in birds as in mammals. Owls are also unique among the birds examined in possessing extensive, plate-like postorbital processes that largely isolate the orbits from the temporal fossae. Furthermore, dissections of four owl species demonstrate that the expanded strigiform postorbital process deflects the path of mandibular adductors around the eye's inferolateral margin. These findings provide further comparative support for both the NVPH and the insulation hypothesis.