Signatures of Divergence, Invasiveness, and Terrestrialization Revealed by Four Apple Snail Genomes

Abstract

The family Ampullariidae includes both aquatic and amphibious apple snails. They are an emerging model for evolutionary studies due to the high diversity, ancient history, and wide geographical distribution. Insight into drivers of ampullariid evolution is hampered, however, by the lack of genomic resources. Here, we report the genomes of four ampullariids spanning the Old World ( Lanistes nyassanus ) and New World ( Pomacea canaliculata , P. maculata , and Marisa cornuarietis ) clades. The ampullariid genomes have conserved ancient bilaterial karyotype features and a novel Hox gene cluster rearrangement, making them valuable in comparative genomic studies. They have expanded gene families related to environmental sensing and cellulose digestion, which may have facilitated some ampullarids to become notorious invasive pests. In the amphibious Pomacea , novel acquisition of an egg neurotoxin and a protein for making the calcareous eggshell may have been key adaptations enabling their transition from underwater to terrestrial egg deposition.

Egg perivitelline fluid proteome of a freshwater snail: Insight into the transition from aquatic to terrestrial egg deposition

“…Although the branch‐site test did not identify an amino acid site with positive selection on subclade B (Table S4, supporting information), the sequence alignment showed a conserved D‐K/Q‐DG‐D/N‐N calcium‐binding motif in subclade B, and a D‐X‐N‐X‐DD motif in subclade A (Figure S2A, supporting information), indicating the conservation of the putative calcium‐binding function in subclade B after gene duplication. The unique presence of CaBP in Pomacea is consistent with the role of the shell in the defense of terrestrial eggs against physical damage and desiccation . Similar studies in other lineages of terrestrial egg‐layinggastropods may unveil the mechanisms of convergent evolution of calcareous eggshell formation in Mollusca.…”

“…Among the orthogroups, 13 were found in all of the four ampullariids, including five PV1 subunits, five immune‐responsive proteins (C1q domain‐containing protein, CD109 antigen, deleted in malignant brain tumors 1, tachylectin‐related protein and soma ferritin), and three other proteins (superoxide dismutase 1, apoptosis‐inducing factor and novel protein). Interestingly, two orthogroups, CaBP that is involved in forming the egg shell, and Kunitz/Bovine pancreatic trypsin inhibitor that inhibits the functioning of multiple digestive proteases, were only detected in the three species of Pomacea. The presence of multiple immunoproteins in the PVF of the four species may indicate their role in defense against pathogens, as has been suggested for the eggs of the pulmonate snail Biomphalaria glabrata .…”

“…In apple snails, previous studies reported the storage of calcium in the albumen gland of Pomacea species and depositing the intracellular calcium in the capsule gland (part of the albumen gland) for egg formation . The high expression of CaBP in the albumen gland and its presence in both the PVF and the aerial eggshell of Pomacea indicate the crucial role of this protein in the eggshell formation . To gain further insight into the evolution of Pomacea CaBP, we identified 29 homologs in the eight ampullariids.…”

“…The acquisition of neurotoxic PV2 in the terrestrial eggs of Pomacea may be an important biochemical defense mechanism against terrestrial predators . A genome analysis of four ampullariids also indicated that the duplication and neofunctionalization contributed to the formation of the neurotoxic PV2‐MACPF and PV2‐tachylectin in P. canaliculata and P. maculate : (1) they show tissue‐specific expression in the albumen gland; (2) they form clades in phylogenetic trees; and (3) their coding protein subunits are present in PVF . To detect the orthologs of PV2‐MACPF and PV2‐tachylectin in P. diffusa , we integrated phylogenetic, transcriptomic and proteomic evidence.…”

“…Phylogenetic analyses have shown that P. canaliculata and P. maculata are very closely related species located in a terminal clade among a large clade that includes most other species of Pomacea , and this large clade is the sister clade that includes M. cornuarietis and species of two other genera ( Asolene and Felipponea ) . A recent study based on 1357 single‐copy orthologous genes estimated that M. cornuarietis and the two species of Pomacea shared a common recent ancestor ~28.3 million years ago (Ma), whereas the divergence between P. canaliculata and P. maculata occurred much more recently at ~3.0 Ma . Because of the terminal positions of the two Pomacea species, and the long divergence time between the genera Pomacea and Marisa , the PVF proteins of P. canaliculata and P. maculata may not represent the diversity of PVF proteins of the genus.…”