Coordinated adaptations define the ontogenetic shift from worm- to fish-hunting in a venomous cone snail

Abstract

Marine cone snails have attracted researchers from all disciplines but early life stages have received limited attention due to difficulties accessing or rearing juvenile specimens. Here, we document the culture of Conus magus from eggs through metamorphosis to reveal dramatic shifts in predatory feeding behaviour between post-metamorphic juveniles and adult specimens. Adult C. magus capture fish using a set of paralytic venom peptides combined with a hooked radular tooth used to tether envenomed fish. In contrast, early juveniles feed exclusively on polychaete worms using a unique “sting-and-stalk” foraging behaviour facilitated by short, unbarbed radular teeth and a distinct venom repertoire that induces hypoactivity in prey. Our results demonstrate how coordinated morphological, behavioural and molecular changes facilitate the shift from worm- to fish-hunting in C. magus, and showcase juvenile cone snails as a rich and unexplored source of novel venom peptides for ecological, evolutionary and biodiscovery studies.

Prey Shifts Drive Venom Evolution in Cone Snails

“…Both molluscivorous and vermivorous species also formed distinct clusters except for the vermivorous Conus imperialis , which grouped with the molluscivores. We included conotoxin expression data from juvenile Conus magus , a species from the Pionoconus clade of which the adults are piscivorous, while juveniles are vermivorous ( Nybakken and Perron 1988 ; Rogalski et al 2023 ). The juvenile C. magus grouped with vermivorous snails from the Lautoconus clade and C. bayani , showing that the C. magus venom changes ontogenetically in accordance with its shifting prey preference.…”

Predatory and Defensive Strategies in Cone Snails

“…In the case of vertebrate venomous animals, such as snakes, both preys (often small vertebrate mammals, but also reptiles and birds) and predators (mostly higher vertebrates) share a very conserved physiology, explaining how by a fortunate coincidence, the same toxins would be effective both in capturing prey and in defending against a predator [ 88 ]. To the contrary, cone snails had to deal with more complicated venom uses (very diverse vertebrate/invertebrate preys and predators), stimulating the evolution of distinct strategies [ 89 ]. We, therefore, encourage future studies to investigate predatory venoms on laboratory animals more closely related to prey types, such as zebrafish (piscivorous), Lymnaea or Aplysia snails (molluscivorous), and any worms (vermivorous), including Caenorhabditis elegans , although annelids would be preferable over nematodes.…”

Slowly Making Sense: A Review of the Two-Step Venom System within Slow (Nycticebus spp.) and Pygmy Lorises (Xanthonycticebus spp.)

“…Cone snails ( Conus spp.) have one of the most complex venom systems recognised by the scientific literature [ 2 , 33 , 152 ]. They are able to produce toxins more suited for predation and toxins more suited for defence at different parts along their venom duct.…”

“…These include identifying major ontogenetic shifts in venom composition in cone snails ( Conus spp.) [ 33 ]; discovering that venom within Araneae has evolved from silk glands rather than salivary glands [ 34 ]; and even the recognition of new venomous species in neglected groups like the mammals [ 35 ].…”