The evolution of flight and echolocation in bats: another leap in the dark

Abstract

The earliest known complete bats, from the Eocene (49–53 Mya), were already capable of flapping flight and echolocation. In the absence of direct fossil evidence there have been many speculative scenarios advanced to explain the evolution of these behaviours and their distributions in extant bats. Theories assuming chiropteran monophyly have generally presumed the ancestral pre‐bat was nocturnal, arboreal and insectivorous. Following this assumption hypotheses can be divided into the echolocation first, flight first and tandem development hypotheses, all of which assume that flight evolved only once in the lineage. In contrast, the chiropteran diphyly hypothesis suggests that flight evolved twice. Evidence supporting and refuting the different hypotheses are reviewed. It is concluded that there are significant problems attached to all the current models. A novel hypothesis is advanced, which starts from the assumption that bats are monophyletic and the ancestral pre‐bat was arboreal, but diurnal and frugivorous. After the evolution of flight it is suggested that these animals were driven into the nocturnal niche by the evolution of raptorial birds, and different groups evolved either specialised nocturnal vision (megachiropterans) or echolocation (microchiropterans). A block on sensory modality transfer has retained this distribution of perceptual capabilities ever since, despite some Megachiroptera evolving rudimentary echolocation, and the dietary convergence of some Microchiroptera with the Megachiroptera. The new hypothesis overcomes many of the problems identified in previous treatments.

Evolution of high duty cycle echolocation in bats

“…Fenton et al, 1995;Simmons and Geisler, 1998;Speakman, 2001;Schnitzler et al, 2004). Powered flight is a diagnostic feature that sets bats apart from all other mammals.…”

The evolution of color vision in nocturnal mammals

“…The unique ability of most bats to orient using laryngeal echolocation without the need for vision, coupled with their characteristically small eyes, has led to speculation that laryngeal echolocation and nocturnality coevolved, and that an evolutionary ''tradeoff'' occurred between vision and hearing in bats (12). Using this logic, it is hypothesized that bats have occupied a nocturnal niche for Ͼ52 million years, because this is the age of the oldest bat fossil that shows evidence of echolocation capabilities (13).…”

The developmental basis of bat wing muscle

“…Recent molecular phylogenetic analysis supports the monophyly of bats, suggesting a single origin of powered flight in mammals 3 . It is almost universally accepted that bats evolved from small arboreal mammals 2,4 . However, to date there are no mammalian fossils of intermediate morphology linking bats to gliding or flightless ancestors 5 , implying the sudden appearance of this mammalian lineage with a unique body plan.…”