The gastropod shell has been co-opted to kill parasitic nematodes

Abstract

Exoskeletons have evolved 18 times independently over 550 MYA and are essential for the success of the Gastropoda. The gastropod shell shows a vast array of different sizes, shapes and structures, and is made of conchiolin and calcium carbonate, which provides protection from predators and extreme environmental conditions. Here, I report that the gastropod shell has another function and has been co-opted as a defense system to encase and kill parasitic nematodes. Upon infection, cells on the inner layer of the shell adhere to the nematode cuticle, swarm over its body and fuse it to the inside of the shell. Shells of wild Cepaea nemoralis, C. hortensis and Cornu aspersum from around the U.K. are heavily infected with several nematode species including Caenorhabditis elegans. By examining conchology collections I show that nematodes are permanently fixed in shells for hundreds of years and that nematode encapsulation is a pleisomorphic trait, prevalent in both the achatinoid and non-achatinoid clades of the Stylommatophora (and slugs and shelled slugs), which diverged 90–130 MYA. Taken together, these results show that the shell also evolved to kill parasitic nematodes and this is the only example of an exoskeleton that has been co-opted as an immune system.

Save your host, save yourself? Caste‐ratio adjustment in a parasite with division of labor and snail host survival following shell damage

“…Snails are often infected by helminth parasites (Bayne, ). The gastropod shell provides little defense against helminth infections, although a few striking examples have shown that the shell can successfully kill nematode parasites (Rae, ; Williams & Rae, ). For example, there are probably tens of thousands of species of trematodes (Trematoda: Digenea), the vast majority of which utilizing gastropods as obligatory hosts in their life cycles (van der Knaap & Loker, ).…”

“…Snails are often infected by helminth parasites (Bayne, 1983). The gastropod shell provides little defense against helminth infections, although a few striking examples have shown that the shell can successfully kill nematode parasites (Rae, 2017;Williams & Rae, 2016).…”

Golden Apple Snail Shell (<i>Pomacea canaliculata</i>) as Prospective Agent in Absorbing Lead (pb) in Water

“…They also contain small amounts of protein. The shells consist of calcium carbonate crystals organized within a matrix of protein thus making GAS shells as an effective absorber [16].…”

My favourite nematode – Phasmarhabditis hermaphrodita

“…Snails such as Achatina fulica (Williams and Rae, 2015) and Cepaea nemoralis (Williams and Rae, 2016) can actively trap, encase and kill nematodes using their shell. This whole process is remarkably efficient at killing nematodes, often hundreds at a time and is evolutionary conserved across the phylogeny of the Stylommatophora (terrestrial slugs and snails) (Rae, 2017b). An exciting opportunity has indirectly arisen from this research that 4 may allow us to actually track the evolution of nematodes at the molecular level over time.…”

“…An exciting opportunity has indirectly arisen from this research that 4 may allow us to actually track the evolution of nematodes at the molecular level over time. Snail shells that are hundreds of years old present in museums have been shown to have nematode encased in their shells (Rae, 2017b(Rae, , 2018. As nematode DNA can be extracted from shells this may facilitate genomic analysis over time using these preserved 'fossilised' specimens.…”