The Prestin Gene and the Evolution of Ultrasonic Hearing in Cetaceans

The two major lineages of whales diverged from each other some 36 to 34 million years ago. One whale lineage, the baleen whales (Mysticeti), evolved a filter feeding strategy where vast quantities of tiny prey are strained from the water using rows of comb-like baleen plates (see Vaughan et al., 2010 for details). The second lineage, the toothed whales (Odontoceti), including dolphins and killer whales, evolved a strategy of hunting larger prey (Figure 1). At great depths and in murky waters, vision is limited and members of this lineage evolved echolocation as a means of locating their prey.

killer_whale
Figure 1. A killer whale (Orcinus orca) breaches in the Pacific Northwest. (From Christopher Michel/Flickr)

In toothed whales, echolocation is coupled with the specializations of the inner ear for detecting the high-frequency sounds produced during echolocation. The same coupling of echolocation and ultrasonic hearing have also evolved independently in bats. In both lineages, the
Prestin gene appears to play a major role.

Prestin is a motor protein specifically expressed in outer hair cells of the cochlea, and is essential in auditory processing in the mammalian inner ear. Thus, the Prestin gene is believed to play a critical role in the evolution of echolocation in both bats and toothed whales.

Liu and colleagues (2010) studied the amino acid sequences of Prestin motor proteins in toothed whales and echolocating bats. Evidently, Prestin underwent two independent bouts of accelerated evolution in these two groups of mammals. Surprisingly, there was a high degree of amino acid sequence convergence (i.e. identical amino acid site replacements) in whales and bats, with over 25 amino acid changes shared between toothed whales and bats.

This research also shows that Prestin evolution is linked directly to the evolution of high-frequency hearing in toothed whales. For example, the pygmy sperm whale (
Kogia breviceps), which echolocates at much higher frequencies than its more familiar cousin the sperm whale (Physeter macrocephalus), showed the largest number of amino acid replacements. This suggests that changes at several keys sites in the Prestin motor protein helped “tune” the hair cells to higher-frequency sounds.

Within the toothed whale lineage, Prestin proteins underwent two rounds of accelerated evolution. The first occurred after toothed whales split off from baleen whales (i.e. on the ancestral branch of all toothed whales). A second round of Prestin evolution occurred on the branch leading to a clade comprising dolphins and beaked whales (Figure 2).

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Figure 2. Amino acid changes mapped onto the cetacean phylogeny (for details see Liu et al., 2010).

Thus, the Prestin gene experienced positive selection in bats roughly 52 to 39 million years ago, leading to specialized ultrasonic hearing in echolocating bats. In contrast, toothed whales experienced rapid evolution in their Prestin gene more recently, roughly 36 to 34 million years ago. Both bats and whales evolved similar amino acid changes, but toothed whales, (especially dolphins) apparently were on a fast track for ultrasonic hearing because they did it in less time (5 to 15 million years less).


References

Vaughan, T., Ryan, J., and N. Czaplewski. 2010.
Mammalogy, 5th edition, Jones & Bartlett, Sudbury, MA.

Yang Liu, Stephen J. Rossiter, Xiuqun Han, James A. Cotton, and Shuyi Zhang (2010) Cetaceans on a Molecular Fast Track to Ultrasonic Hearing,
Current Biology, 20:1834-1839, DOI:10.1016/j.cub.2010.09.008.