Evolution of Traditional Aerodynamic Variables in Bats (Mammalia: Chiroptera) within a Comprehensive Phylogenetic Framework

Abstract

Chiroptera is the only group of mammals capable of powered flight. The mechanical basis of bat flight is well established, but evolution of its constituent aerodynamic variables remains poorly understood. Here, we determine the macroevolutionary patterns of traditional aerodynamic variables (wing loading, aspect ratio, tip shape index) in a comprehensive phylogeny of Chiroptera using an extensive dataset including key Eocene fossils. We optimized variables as continuous characters and fit models of character evolution to identify shifts in character optima. The reconstructed ancestral chiropteran morphotype presented low wing loading and low-to-intermediate aspect ratio, and remained unaltered for much of the first half of bat evolution (Paleogene). This evolutionary pattern may be explained by stabilizing selection responding to the strong constraints imposed by echolocation and flight on body size, and the physical constraints regarding aerodynamic efficiency acting on wing shape. Posterior specialization in some groups permitted divergence toward novel aerodynamic morphotypes in the second half of chiropteran evolutionary history (Neogene). We linked the most notable aerodynamic changes to ecological release from echolocation constraints (Pteropodidae), dietary-foraging shifts (Phyllostomidae, Noctilionidae), or advantage in face of environmental changes (Molossidae, Taphozoinae). The independently-evolved specialization of fast, enduring flight that allowed Molossidae and Taphozoinae (Emballonuridae) to perform aerial hawking of swarming insects in open spaces was linked to significant shifts in the optima of both wing loading and aspect ratio. These shifts were probably associated with the gradual spread of open-mosaic landscapes at a global scale since the Oligocene.