Molecular Evidence for the Parallel Evolution of Anosmia in Multiple Odontoceti (Toothed Whales) Clades

Background/Objectives. Living odontocetes are the only extant mammals that lack anatomical features associated with olfaction. A leading hypothesis for the presumed complete loss of smell (i.e., anosmia) in odontocetes is that olfaction was lost in the common ancestor of the crown clade. An alternative hypothesis is that olfaction was lost in parallel in different odontocete lineages. Methods. A data set that includes complete coding sequences for three olfactory-specific genes (CNGA2, CNGA4, OMP) was assembled for 65 odontocete, 14 mysticete, and 28 outgroup species. The phylogenetic distribution of inactivating mutations in these genes was documented, and selection (dN/dS) analyses were performed with codeml to determine if selection intensity has been the same or different on three different branch categories within Odontoceti: intact, transitional, and fully pseudogenic. Results. There are no inactivating mutations that are shared by all odontocetes or either of the basal clades within Odontoceti. Fifty-four of 65 taxa exhibit at least one inactivating mutation, and all 11 species that lack inactivating mutations are ziphiids. Selection analyses indicate that dN/dS values are elevated on all branch categories within Odontoceti relative to both mysticete and outgroup branches. However, the odontocete dN/dS values are lowest on intact branches, intermediate on transitional branches, and highest on fully pseudogenic branches. Conclusions. The results of selection analyses, coupled with the absence of inactivating mutations on the most basal odontocete branches, support the hypothesis that olfaction was gradually reduced across Odontoceti prior to the complete ablation of this sense in independent lineages within this clade.