What can hearing genes tell us about the evolution of echolocation in dolphins?
Echolocation was a key development in toothed whale evolution, favoring their ecological success and adaptive radiation across multiple habitats. Previous bioacoustic and morphological studies suggest that environmental pressures have influenced the evolution of echolocation in odontocetes. This hypothesis demands further investigation, especially regarding molecular mechanisms involved in odontocetes’ adaptive radiation across multiple habitats. Here we show that the coding sequences of four hearing genes involved in echolocation (CDH23, SLC26A5, TMC1 and CLDN14) have different signatures of molecular evolution among riverine, coastal and oceanic dolphins, suggesting that the evolutionary constraints of these habitats have shaped the genetic diversity underlying toothed whale sonars. Our comparative analysis across 37 odontocete species has revealed patterns of accelerated evolution within coastal and riverine lineages, supporting the hypothesis that these habitats generate specific selective pressures to sonar propagation, which are not found in the ocean (e.g., clutter and reverberation). Specific branches with sites under diversifying selection include: three coastal/estuarine species which have recently diverged from closely-related lineages inhabiting freshwater (Cephalorhynchus commersonii, Sotalia guianensis and Orcaella heinsohni – CDH23), and three species that operate specialized Narrow Band High Frequency Sonars (Phocoena sinus – SLC26A5, Neophocaena phocaenoides and Cephalorhynchus commersonii – CDH23). All positively selected lineages are coastal or estuarine from shallow waters (< 100), corroborating current knowledge on these species’ sonars. Among river dolphin branches, positive selection was found on specific sites of the genes CDH23 and SLC26A5, when compared to other cetaceans and Laurasiatherians. Finally, the detection of sites with different overall substitution rates (dN/dS) among river and marine dolphins, together with the finding of different amounts of positively selected sites in each environmental group, suggests distinct selective pressures acting in these groups in the molecular evolution of echolocation.
Evolutionary dynamics of cetacean communication: connecting genotype and phenotype across different environments
Cetaceans share a unique evolutionary history marked by the transition from land to sea, followed by a rapid diversification across multiple environments, from the open oceans to rivers, estuaries, and the polar waters. One consequence of such dispersion was the evolution of sound-based vocalization systems, more efficient underwater than visual or olfactory signals. Recent studies suggest that key behavioral features to cetacean sound communication, as high and low frequency hearing, specialized sound production and vocal learning, present functional, anatomical and behavioral differences among marine, freshwater and coastal dolphins. Thus, a wide, comprehensive study of cetacean vocal behavior is highly necessary, especially to investigate the genetic basis of environment-related differences among dolphins. We hypothesize that adaptive change within a shared underlying genetic system is the evolutionary mechanism of divergent/convergent vocal behavior across cetacean species inhabiting distinct environments. Our proposal is to investigate the molecular evolution of cetacean
communication across different environments and lineages. To uncover evolutionary pathways leading to distinct vocalization systems, cetacean genomic sequences functionally related with sound production/perception, vocal learning and cochlear development will be tested for adaptive convergence and natural selection, and analyzed for functional enrichment. By investigating these genomic patterns and comparing them against the reported variation on vocal/hearing traits, we expect to uncover new genomic sequences and functions, expand current knowledge and contribute to ongoing discussions on the evolution of cetacean communication. Finally, since communication is a keystone of cetacean culture, our contributions will ultimately allow further understanding of how cetacean societies are structured and maintained.