Slipper Snails Slide Between Sexes in Stacks

Or, Crepidula fornicata say, “Trans Rights!”

…if they don’t get eaten by their siblings first.

by Sabrina Spiher Robinson

Slipper snails, Crepidula fornicata, are a common find for shell collectors along the American east coast, and in some places on the west coast as well, where they have been accidentally introduced as an invasive species. But just because they’re common, doesn’t mean they’re not interesting – in fact, they’re one of the most well-studied marine snails, and all of that study has revealed a creature with a fascinating life cycle.

Crepidula are protandrous hermaphrodites – this means that all slipper snails begin their lives as male, and end their lives as female. As juveniles, they wander over the substrate, preferring hard surfaces like rocks, dock pilings, other shells, and even horseshoe crabs. But most C. fornicata will choose to settle on top of another C. fornicata, who might be settled atop another, and another, and so on. They live in stacks, sometimes of up to a dozen animals, one balancing on top of the next until their shells grow around each other, and they can no longer move, becoming sessile (stationary) by default.

Of course, a stack of all males won’t get very far reproductively. So, it’s time for at least a few C. fornicata to begin the next stage in their lives, and transition to females. Several things influence when the change takes place, primarily the animal’s size, because producing gametes is energetically costly: more sperm takes more energy than less sperm, and eggs take more energy than sperm altogether. But it’s not so straightforward as just growing to a certain size and changing sex. If there are no females around, for instance, some males will transition to females at smaller sizes than they usually would.¹  Alan Carillo-Boltodano and Rachel Collin write:

“In our experiment, pairs of snails (one small and one large) were kept in cups, either together or partitioned off with fine or coarse mesh, or partitioned, but switched from side to side to allow contact with the cup mate’s pedal mucus. The larger snails that were allowed contact with the smaller companions grew faster, and generally changed sex sooner, than did the larger snails in the barrier treatments, which allowed no physical contact. The smaller snails that were allowed contact with the larger cup mate delayed sex change compared to those separated from their cup mates … Our results suggest that the cue that affects size and time to sex change requires some kind of physical interaction that is lost when the snails are separated. Furthermore, contact with another snail’s pedal mucus does not compensate for the loss of physical contact.”²

In other words, when the slipper snails are in actual contact with each other, they seem to send signals to one another that help to coordinate growth and sex change.

In general, though, males will wait until they’re a certain size to transition, because larger males are more reproductively successful than smaller males, as determined by experiments that genetically test offspring to see whose genes were most successful in the stack. There’s one exception to this though – sneaky little guys! Male Crepidula inseminate females directly, so in general the male right on top of the female at the bottom of the stack will be the most successful fertilizer, and then the male on top of him, and then the others on top of them can’t reach and are out of luck for the moment. But! The smallest juvenile Crepidula, who have not yet chosen a stack of their own, have been found to sneak up on the substrate next to the female, inseminate her, and sneak away, using a strategy that gets around “bigger = more sperm.”³

Larger males might have more reproductive success than smaller males, but no one has more reproductive success than slipper snails who have transitioned to females. Eggs are a much bigger energy investment for an animal than sperm are, and so becoming a female requires a certain size to make the transition worthwhile. But once a slipper snail is female, she has a couple reproductive advantages: in the first place, she can hoard sperm for a long time, including her own from when she was a male, so she always has plenty of material to fertilize her eggs. This also means that while only a third or a quarter of the embryos will have a given male’s DNA, they’ll all have hers. Secondly, Crepidula females brood their young. Unlike many marine mollusks, who release their eggs and sperm into the water column where they meet and the embryo has to grow up among the plankton, at risk of becoming a meal for many things before they ever even get to grow into larvae, Crepidula keep their eggs in brooding pouches. Females keep between 15 and 20 pouches inside their shells, each containing between 50 and 450 embryos. She’ll brood them until they turn into larvae that can swim about on their own, keeping them safe to grow at least for a little while.

And thus, every Crepidula fornicata begins their life as a tiny, and sometimes sneaky, roaming male, sowing his wild oats; eventually he finds a nice stack to settle down on to become a dad; and then they transition sexes and live out her days as mother and base of the stack, brooding little babies in safety until they’re ready to hatch into larvae. Slipper snails make small stacks, but big happy families.

However, perhaps nowhere is safe. Once the eggs are brooding in their capsules, the mother slipper snail has no way to transfer additional nutrients or oxygen to the embryos.  This environment of scarcity leads some species of Crepidula embryos to start cannibalizing each other! The embryos of Crepidula coquimbensis, a species of Crepidula first described in Chile, have at least been found to be choosy about eating their brothers and sisters. Brood capsules are fertilized by multiple males, meaning all the embryos have the same mother, but not every embryo has the same father. It was discovered that cannibalistic embryos were much more likely to eat their half-siblings than their full siblings, thus protecting embryos they shared a complete set of DNA with. It’s still not known how these embryos recognize kinship, though.⁴ In another species of Crepidula, Crepidula navicella, a gene in some of the embryos in each capsule switches on and arrests their development, basically turning them into meals for their siblings, a genetic predisposition to being either a cannibalizer or a cannibalizee.⁵

Of course, once the larvae are released into open water, all bets are off, and a lot of filter-feeding animals, including other mollusks, including other Crepidula, might eat them. However, Jan Pechenik reports:

“… in our study the same adults usually ingested their own larvae at much slower rates than predicted from the rates at which they cleared water of phytoplankton. These slower rates may in part reflect an inability or reluctance of adults to ingest particles of such large size …  However, most of the larvae that we observed being entrained into adult feeding currents were ingested, and later appeared in feces, and adults were capable of ingesting larvae that were larger … Thus, lower than predicted rates of [larvae eating] by C. fornicata more likely reflect larval behavior – deliberate or not – reducing the likelihood of [getting drawn] into the adult feeding current, as suggested previously from studies with [other marine filter feeders].”⁶

At least baby Crepidula, once free, seem to have developed a way to avoid being eaten by their parents, if not their siblings!

Sabrina Spiher Robinson is Collection Assistant for the Section of Mollusks at Carnegie Museum of Natural History.

References:

[1] Proestou, Dina A., Goldsmith, Marian, Twombly, Sarah (2008) “Patterns of Male Reproductive Success in Crepidula fornicata Provide New Insight for Sex Allocation and Optimal Sex Change.” The Biological Bulletin (Lancaster), vol. 214, no. 2, 2008, pp. 194–202, https://doi.org/10.2307/25066676.

[2] Carrillo-Baltodano, Allan, and Collin, Rachel (2015). “Crepidula Slipper Limpets Alter Sex Change in Response to Physical Contact with Conspecifics.” The Biological Bulletin (Lancaster), vol. 229, no. 3, 2015, pp. 232–42, https://doi.org/10.1086/BBLv229n3p232.

[3] Broquet, Thomas, et al. “The Size Advantage Model of Sex Allocation in the Protandrous Sex-Changer Crepidula fornicata: Role of the Mating System, Sperm Storage, and Male Mobility.” The American Naturalist, vol. 186, no. 3, 2015, pp. 404–20, https://doi.org/10.1086/682361.

[4] Brante A, Fernández M, Viard F (2013) Non-Random Sibling Cannibalism in the Marine Gastropod Crepidula coquimbensis. PLoS ONE 8(6): e67050, doi:10.1371/journal.pone.0067050

[5] Lesoway, MP, Collin, R, Abouheif, E. (2017) “Early activation of MAPK and apoptosis in nutritive embryos of calyptraeid gastropods.” J. Exp. Zool. (Mol. Dev. Evol.) 328B: 449–461. doi:10.1002/jez.b.22745.

[6] Pechenik, Jan, Blanchard, Michel, Rotjan, Randi (2004) “Susceptibility of Larval Crepidula fornicata to Predation by Suspension-Feeding Adults.” Journal of Experimental Marine Biology and Ecology., vol. 306, no. 1, 2004, pp. 75–94, https://doi.org/10.1016/j.jembe.2004.01.004.

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