Left–Right Reversal Recurrently Evolved Regardless of Diaphanous-Related Formin Gene Duplication or Loss in Snails

Abstract

AbstractBilateria exhibit whole-body handedness in internal structure. This left–right polarity is evolutionarily conserved with virtually no reversed extant lineage, except in molluscan Gastropoda. Phylogenetically independent snail groups contain both clockwise-coiled (dextral) and counterclockwise-coiled (sinistral) taxa that are reversed from each other in bilateral handedness as well as in coiling direction. Within freshwater Hygrophila,Lymnaeawith derived dextrality havediaphanous related formin(diaph) gene duplicates, while basal sinistral groups possess onediaphgene. In terrestrial Stylommatophora, dextralBradybaenaalso havediaphduplicates. Defective maternal expression of one of those duplicates gives rise to sinistral hatchlings inLymnaeaand handedness-mixed broods inBradybaena, through polarity change in spiral cleavage of embryos. These findings led to the hypothesis thatdiaphduplication was crucial for the evolution of dextrality by reversal. The present study discovered thatdiaphduplication independently occurred four times and its duplicate became lost twice in gastropods. The dextrality ofBradybaenarepresents the ancestral handedness conserved across gastropods, unlike the derived dextrality ofLymnaea. Sinistral lineages recurrently evolved by reversal regardless of whetherdiaphhad been duplicated. Amongst the sevenformingene subfamilies,diaphhas most thoroughly been conserved across eukaryotes of the 14 metazoan phyla and choanoflagellate. Severe embryonic mortalities resulting from insufficient expression of the duplicate in both ofBradybaenaandLymnaeaalso support thatdiaphduplicates bare general roles for cytoskeletal dynamics other than controlling spiralian handedness. Our study rules out the possibility thatdiaphduplication or loss played a primary role for reversal evolution.