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

Challenges accessing or rearing juvenile cone snails have limited our understanding of their developmental biology. This study reveals how complex morphological, behavioural and molecular changes facilitate the ontogenetic shift from worm- to fish-hunting in the extensively-studied Conus magus.
Coordinated adaptations define the ontogenetic shift from worm- to fish-hunting in a venomous cone snail

It was the summer 2018, I was just a few weeks into my PhD with Prof. Richard Lewis who has spent most of his career studying venomous marine cone snails. During a routine inspection of our aquariums, I noticed several rows of white flattened pouches hidden under a rock in one of the cone snail tanks. Upon closer inspection, each pouch appeared to contain hundreds of white balls about the size of a pinhead. These were eggs, encased within semi-rigid capsules deposited the night before by a female cone snail. Like most marine gastropods, cone snails start their life as benthic eggs which develop into swimming larvae that will eventually settle on the ocean floor and metamorphose into benthic, crawling juveniles. 

Cone snails have a biphasic life cycle. Eggs are deposited in semi-rigid egg capsules (a) from which small planktonic larvae (b) emerge. The larvae will eventually settle and metamorphose into benthic, carnivorous juveniles (c). Credit: A. Rogalski

My excitement at the idea of growing cone snails in the laboratory was quickly tempered by the lack of literature on their developmental biology – the result of the minute size of early life stages, which makes them virtually impossible to spot on the reef, and the difficulty to culture them in captivity. Culturing molluscs in the laboratory is notoriously challenging. Most species breed once a year and lay eggs from which small, planktonic larvae emerge. In most cases, the larvae must feed on microalgae for several days, weeks or even months before settlement. In addition, most species require specific cues (biological, physical or chemical) to initiate settlement, which is followed by metamorphosis. This process drives the transition from free-swimming larva to benthic juvenile and is marked by high mortality rates, even in well established aquaculture facilities. While rearing methods have been developed for several species of commercial interest (such as scallops, oysters or mussels), the bulk of literature on cone snail culture is limited to the work of Perron in the early 1980’s. However, the difficulty to reproduce these experiments has limited subsequent studies to the exploration of embryonic and larval stages, leaving a significant knowledge gap.

But my curiosity was piqued when I came across a study from the late 80’s in which the authors suggested that Conus magus – source of the FDA-approved analgesic Prialt® – may experience an ontogenetic dietary shift from worm- to fish-hunting, based on the discovery of worm remnants in the stomach of wild-caught juveniles. Remarkably, over 30 years later, empirical evidence was still lacking due to the difficulty to access or culture early juveniles, prompting me to focus my efforts on this extensively-studied species. It was only 1.5 years later, in February 2020, that I witnessed the first successful metamorphosis of a cone snail larva into a benthic juvenile, a single individual out of 500 larvae that had been nurtured for several weeks. A few months (and many endless nights in the aquarium room) later this number grew to over a hundred juveniles – finally enough to carry out behavioural, histological, transcriptomic and proteomic studies. For the first time, this work provides empirical evidence for the shift from worm- to fish-hunting in Conus magus, which was marked by coordinated behavioural, morphological and molecular changes. While adults rely on a set of paralytic venom peptides and a hooked harpoon to quickly immobilise and tether fish, juveniles feed exclusively on small polychaete worms using a unique venom repertoire that induces hypoactivity. Our results show how laboratory-reared specimens can provide a valuable insight into the ecology of secretive life stages. Additionally, this work showcases juvenile cone snails as a rich and unexplored source of novel bioactive peptides, even in extensively-studied species. We hope that the ability to rear cone snails in the laboratory will provide a sustainable access to specimens for research facilities and the ornamental trade, reducing the toll on wild populations which are under the growing threat of habitat loss and destruction.

(a) Adult Conus magus engulfing a fish. (b) Laboratory-reared, vermivorous  juvenile. (c) Juvenile C. magus preying on a polychaete worm. Credits: R. J. Lewis (a), J. Yum (b) and A. Rogalski (c).

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