The hearing gene Prestin unites echolocating bats and whales

Abstract

Echolocation is a sensory mechanism for locating, ranging and identifying objects which involves the emission of calls into the environment and listening to the echoes returning from objects [1]. Only microbats and toothed whales have acquired sophisticated echolocation, indispensable for their orientation and foraging [1]. Although the bat and whale biosonars originated independently and differ substantially in many aspects [2], we here report the surprising finding that the bottlenose dolphin, a toothed whale, is clustered with microbats in the gene tree constructed using protein sequences encoded by the hearing gene Prestin.

Figure 1.

Parallel evolution of prestins of echolocating bats and bottlenose dolphin. (A) The maximum-likelihood (ML) tree reconstructed using the prestin protein sequences of 25 mammals, under the model of JTT-f with a gamma distribution of substitution rate variation among sites (shape parameter =0.14). Numbers on interior branches are bootstrap percentages from ML, maximum-parsimony (MP), and neighbor-joining (NJ) analyses. The bootstrap value from an analysis is indicted as “-” when the branch does not exist in that analysis. The scale bar shows 0.01 amino acid substitution per amino acid site. (B) The species tree of 18 mammals. Tree branches are not drawn to scale. Parallel substitutions were examined between the red branch and the branches labeled 1, 2, and 3. The amino acid (N: Asn; T: Thr) at position 7 of prestin is shown for each interior and exterior node. (C) Locations of evolutionarily interesting amino acid sites in the structural model of prestin with 10 transmembrane domains. Numbers associated with colored circles are the amino acid positions in the dolphin prestin sequence, with the residues observed in dolphin indicated. Sets I, II, and III are the most important sites responsible for the misplacement of both dolphin and the two purple-labeled microbats in panel A, misplacement of dolphin, and misplacement of the two microbats, respectively, and are listed in the order of their support of the gene tree relative to the species tree (from high to low). Sets 1, 2, and 3 are sites that have experienced parallel amino acid substitutions between the dolphin branch (red in panel B) and branches 1, 2, and 3, respectively. Parallel-evolution sites are shown in red, while the other sites are shown in blue.