Proteomic analyses reveal the key role of gene co-option in the evolution of the scaly-foot snail scleritome

Abstract

Biomineralization, a key driving force underlying dramatic morphological diversity, is widely adopted by metazoans to incorporate inorganic minerals into their organic matrices. The scaly-foot snail Chrysomallon squamiferum from deep-sea hot vents uniquely possesses hundreds of sclerites on its foot in addition to a coiled shell, providing an exclusive case to study the formation of evolutionarily novel hard parts. Here, we identified the matrix proteins present in the exoskeletons of C. squamiferum and Gigantopelta aegis, a confamilial species from the same vent habitat but lacking sclerites, to uncover the genes and proteins presumably involved in the sclerite formation processes. Comparative multi-omics analyses suggest that C. squamiferum co-opted a diverse range of metazoan biocalcifying proteins through sclerite formation in a possibly deep homology scenario, and the up-regulated biomineralization-related genes in the foot imply alternative sources of sclerite proteins. The sclerite-secreting epithelium employs and utilizes genes considerably older than those in the mantle, which supports the predominant contribution of co-option in C. squamiferum sclerite formation. Our results highlight the importance of gene co-option in shaping novel hard parts in C. squamiferum and indicate that lineage-specific gene incorporation is a possible key factor leading to the rapid evolution of a novel hard structure in this vent-endemic species.