Molecular evolution of toothed whale genes reveals adaptations to echolocating in different environments

Abstract

Echolocation was a key development in toothed whale evolution, favoring their ecological success and adaptive radiation across multiple habitats, from shallow, murky rivers in South America to deep oceans in East Asia. 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.