The echolocation gene

By Sophie Wang (Pomona College) and Arthur Levine (Pitzer College) [edited by Lars Schmitz, as part of BIOL 167 “Sensory Evolution”, an upper division class at the Claremont Colleges]

Prestin and the convergent evolution of high-frequency hearing

Hearing, one of the most important senses, is a specialized form of mechanosensation that allows an organism to perceive and respond to sound waves in air and in water. Many animals have the ability to hear, but the sensory input is not utilized in the same ways for all. Some animals have evolved the specialized ability to use sound to produce images of both themselves and other objects within a setting, much as humans use vision.

Thisability is called echolocation. The neural mechanisms for echolocation are not all understood, but echolocation is basically a process that involves the emission of high or low frequency calls into the environment combined with the perception of the reverberations of those calls off objects in space (prey, predators, walls, water, trees, boats). Organisms that have independently evolved sophisticated echolocation include bats and toothed whales. Both clades have been shown to have developed such sensitive echolocation as to make it indispensable for orientation and food foraging (Ying et al 2010). Given that bats and toothed whales are very distantly related one wonders if the echolocation systems may function under fundamentally different mechanisms.

In a recent paper published in Current Biology, Li et al. tackle this intriguing example of convergent evolution from a molecular perspective. Before moving on, though, we should touch a little on evolutionary biology, and biology in general. The central reductionist view of biological behavior is that all behaviors can be attributed to isolatable biological mechanisms of physiology, genetics, protein molecules, and enzymes. Therefore, it is a valuable endeavor when studying a behavior in biology to attempt to gain an integrative understanding of the mechanisms. The central dogma of molecular biology states that a sequence of DNA leads to a sequence of RNA which leads tocertain proteins which lead to structuring and function allowing for complex mechanisms that can lead to certain behaviors. In addition, biology can be viewed on a macro and generational time scale, which is especially pertinent when looking at evolution over time. For example, we can use phylogenetic trees based on morphological and molecular data for species to determine their relationship to each other in evolutionary time. We can overlay what we learn about comparative molecular biology with the macro-perspective to learn about the relationships between the evolution of behaviors, via the evolution of molecules over time in various species.

In their Current Biology paper, Li et al. studied a specific protein called prestin which is found in the cochleas of most mammals, including humans. The prestin protein is present in the outer hair cells of the cochlea, which are important in amplification of sound but not in actual transmission of soundwave-triggered signals to the brain.

The authors looked specifically at the intriguing relationship between the prestin sequences of two echolocating mammals: bats and toothed whales. Bats and whales, even though both mammals, are not exactly close relatives, but both groups rely heavily on complex echolocation in their lives. How then, if at all, are the prestin sequences of the two groups related? Does prestin play a role in echolocation?

In order to answer these questions, the authors first determined the relationship between the prestin genes of various species. They began by taking the genetic sequences for prestin of 26 different mammal species and constructing a protein tree showing their relationships to one another. They then compared this tree with a well-supported, more general phylogeny constructed from a large aggregate of information. To their surprise, the prestin tree grouped the bottlenose dolphin within the microbats (Figure 1)! (Basically, this means that the genetic sequence for prestin in the dolphin is more similar to bats than to other animals). As you can see from the general phylogeny, dolphins are much more truly closely related to a number of species (including cows) than they are to bats (Figure 2), which makes the closeness of the prestin relationship between bats and dolphins that much more intriguing!

Figure 1: Prestin protein tree showing that the prestin sequences of the echolocating dolphins (in green) are much more closely related to the sequences of the echolocating bats (in black) than to the sequences of non-echolocating whales (in blue) and cows.

Figure 1: Prestin protein tree showing that the prestin sequences of the echolocating dolphins (in green) are much more closely related to the sequences of the echolocating bats (in black) than to the sequences of non-echolocating whales (in blue) and cows.

Figure 2: General phylogeny of mammals showing distant relationship between whales and bats. Whales are outlined in blue and bats are outlined in red.

Figure 2: General phylogeny of mammals showing distant relationship between whales and bats. Whales are outlined in blue and bats are outlined in red.

So how could these prestin sequences have become so similar? In order to determine this, the authors looked at a number of the possibilities that may have caused this to occur only by coincidence in two echolocating groups, including horizontal gene transfer, DNA contamination, and a host of other genetic mechanisms. However, they found that none of these were likely, meaning that the only remaining explanation was a convergence of the sequences resulting from selection of mutations that are beneficial in echolocation. In simpler terms, they found that there was a connection between the convergence of the prestin gene and the deployment of echolocation.

Li et al. went on to further test this by comparing the different parts of the prestin code that are altered in the different species they studied. Again, they saw that some of the same areas were mutated across the echolocating species. Next, the researchers looked at where these altered sites were located within the complete and folded prestin protein. Prestin is an integral membrane protein, and they found that most of the mutations occurred in the extracellular parts of the protein. These parts of the protein are critical in changing the conformation of prestin, and having quick enough conformational changes is likely very important in being able to process the extremely high returning frequencies of echolocation. So we see that prestin is related to echolocation not through the production of sound (as whales and bats do this very differently), but through the collection of sound!

There is little controversy on the story being told by the authors of this paper, though the sample is relatively small (26 species). Their work is very exciting not because it contradicts other work, but because they were able to document an amazing example of convergent evolution at the molecular level (Shen et al 2011; Liu et al 2010; and Rossiter et al 2011).  This protein becomes significantly more interesting because it exists in lots of species, but may have independently conferred on some the ability to have sensitive echolocation. Other studies have shown convergent evolutions of the prestin protein in other bats and confirm the authors suggestion that prestin analysis groups echolocating bats and whales (Ying et al 2010).

Understanding more deeply the molecular underpinnings of the profound system of echolocation is important for learning more about the evolution of such an interesting mechanism. Studying why the molecule prestin is similar in species that are not actually so similar could give great insight into rules for molecular conservation in evolution and function of the protein in a sensory organ. In addition, understanding prestin and its molecular structure and how said structure evolved could give more insight into how it confers its function within the organism. Finally, learning more about the structure and function of this protein and how it may influence other species who normally do not produce it (mice, rats, monkeys etc) may allow us to determine if it has clinical capabilities in recovering hearing deficits in humans, as it is implicated in some hearing loss (Liu 2003). Believe it or not, some humans have gained (some) ability to echolocate after sight loss. Might these rare humans also express a similar form of prestin to bats and whales?

References

Li Y, Liu Z, Shi P, Zhang J. The hearing gene Prestin unites echolocating bats and whales. Current Biology Vol 20 No 2, 2010.

Shen B, Avila-Flores R, Liu Y, et al. J Mol Evol. Prestin shows divergent evolution between constant frequency echolocating bats. 2011 Oct;73(3-4):109-15. doi: 10.1007/s00239-011-9460-5. Epub 2011 Sep 24.

Liu Y, Cotton JA, Shen B, et al. Convergent sequence evolution between echolocating bats and dolphins. Current Biology 2010 Jan 26;20(2):R53-4. doi: 10.1016/j.cub.2009.11.058.

Rossiter SJ, Zhang S and Liu T. Prestin and high frequency hearing in mammals. Commun. Integr. Biol. 2011 Mar-Apr; 4(2): 236–239. doi: 10.4161/cib.4.2.14647

Xue ZL, Ouyang XM, Xia XJ, et al. Prestin, a cochlear motor protein, is defective in non-syndromic hearing loss. Hum. Mol. Genet. (2003) 12 (10):1155-1162.doi: 10.1093/hmg/ddg127

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