Molecular metabarcoding reveals an omnivorous diet in Smaragdinella haminoeid snails and sheds light on their unique evolution

Abstract

Smaragdinella marine snails are the only members of the family Haminoeidae and the order Cephalaspidea that inhabit hard substrates in the upper tidal zone, making them of special evolutionary interest. To investigate whether possible novel trophic adaptations coupled with unique morphological traits may underlie this ecological shift, we analysed the gut contents and microbiota of Smaragdinella viridis using DNA metabarcoding (COI and 16S rRNA) and scanning electron microscopy (SEM). COI metabarcoding revealed a diverse assemblage of dietary components dominated by diatoms, rotifers, small arthropods, and fungi. SEM observations partially corroborated these findings, indicating an omnivorous feeding strategy rather than strict herbivory. The gut bacterial community was dominated by Firmicutes (Mycoplasma), Proteobacteria (Vibrio, Photobacterium), and Fusobacteriota (Psychrilyobacter, Propionigenium), taxa associated with the degradation of complex carbohydrates and proteins. Morphological traits in Smaragdinella, including an increased number of gizzard plate ridges, a flattened ovoid shell, and an enlarged foot, most likely facilitate the processing of diverse food items and survival in wave-exposed environments. In addition, the functionality of the gut microbiome may contribute to dietary flexibility enhancing survival in dynamic, resource-variable tidal habitats. The adaptation of these snails to tidal hard bottom habitats could have been prompted by the acquisition of novel morphological features and by a diet shift, but the data do not permit to establish a causal relationship and alternative hypotheses may have to be considered.