No genome-wide protein sequence convergence for echolocation

Abstract

Toothed whales and two groups of bats independently acquired echolocation, the ability to locate and identify objects by reflected sound. Echolocation requires physiologically complex and coordinated vocal, auditory, and neural functions, but the molecular basis of the capacity for echolocation is not well understood. A recent study suggested that convergent amino acid substitutions widespread in the proteins of echolocators underlay the convergent origins of mammalian echolocation. Here, we show that genomic signatures of molecular convergence between echolocating lineages are generally no stronger than those between echolocating and comparable nonecholocating lineages. The same is true for the group of 29 hearing-related proteins claimed to be enriched with molecular convergence. Reexamining the previous selection test reveals several flaws and invalidates the asserted evidence for adaptive convergence. Together, these findings indicate that the reported genomic signatures of convergence largely reflect the background level of sequence convergence unrelated to the origins of echolocation.

Keywords: bat; convergent evolution; dolphin; neutral evolution.

Fig. 1.

No genome-wide signatures of protein sequence convergence associated with echolocation. (A) Hypotheses and corresponding tree topologies. H0, species tree; H1, clustering of the two groups of echolocating bats; H1′, clustering of echolocating Yangochiroptera bats and nonecholocating Yinpterochiroptera bats; H2, clustering of echolocating bats and dolphin; H2′, clustering of echolocating bats and cow. In H1, H1′, H2, and H2′, the tree topology for “all other mammalian lineages” is the same as in the species tree. Echolocating species are indicated with an echo symbol. The six branches where convergent sites are counted in table 1 are marked by I–VI. (B) Frequency distributions of ΔL_H0-H1 and ΔL_H0-H1' among the 2,326 proteins are not significantly different. ΔL refers to the per site logarithm of the likelihood ratio between two hypotheses for a protein. (C) Frequency distributions of ΔL_H0-H2 and ΔL_H0-H2' among the 2,326 proteins are not significantly different. In (B) and (C), the P-values are from Kolmogorov–Smirnov tests.