Phylogenies, fossils and functional genes: the evolution of echolocation in bats

Abstract

Introduction Bats are one of the most successful orders of mammals on this planet. They account for over 20% of living mammalian diversity (~ 1200 species), and are distributed throughout the globe, absent only from the extreme latitudes (Simmons, 2005). Bats are the only living mammals that are capable of true self-powered flight, and likewise they are the only mammals capable of sophisticated laryngeal echolocation (Macdonald, 2006). Their global success is largely attributed to these novel adaptations (Jones and Teeling, 2006). Echolocation occurs when a bat emits a brief laryngeal-generated sound that can vary in duration (0.3–300 ms) and in frequency (8–210 kHz) and interprets the returning echoes to perceive its environment (Fenton and Bell, 1981; Thomas et al ., 2004). Calls and echoes can be separated either in time or in frequency (Jones, 2005). Some bats (e.g., horseshoe bats, leaf-nosed bats and mustached bats) emit long constant-frequency calls with Doppler shift compensation (CF/DSC) by taking the velocity of their flight into account and adjusting the frequency of their outgoing calls to ensure that the incoming echoes return at a specific frequency (Thomas et al ., 2004; Jones, 2005). Most other bats emit low-duty-cycle frequency-modulated calls, and separate outgoing calls and incoming echoes temporally (Thomas et al ., 2004; Jones, 2005). Echolocation calls show a great diversity in shape, duration and amplitude, and are correlated with the parameters of a bat's environment (Jones and Teeling, 2006; Jones and Holderied, 2007). The auditory capabilities of bats are extraordinary. Bats produce and interpret some of the “loudest” naturally produced airborne sounds ever recorded (130 dB; Jones, 2005), and are also capable of hearing some of the “quietest” sounds of any mammal (~-20 dB; Neuweiler, 1990). Despite the magnitude and functionality of this spectacular form of sensory perception, the evolutionary history of echolocation is still controversial. This has stemmed from inconsistent and unresolved phylogenies (Simmons and Geisler, 1998; Van Den Bussche and Hoofer, 2004; Eick et al ., 2005; Teeling et al ., 2005), and an incomplete (Teeling et al ., 2005; Eiting and Gunnell, 2009) and differentially interpreted fossil record (Simmons et al ., 2008; Veselka et al ., 2010) that allows for alternate interpretations of gain and loss of auditory function, and lack of molecular echolocation signatures (Teeling, 2009).