The use of a calcified exoskeleton as a means of protection against predation is common throughout the animal kingdom, especially in the marine environment. Crabs are one of these organisms that have benefited from the protection of a robust carapace. The phenomenon of separate organisms evolving into a crab-like body plan is present in king crabs (Lithodidae), porcelain crabs (Porcellanidae), hairy crabs (Lomis hirta), hermit crabs (Paguroidea), and true crabs (Brachyura) (Morrison et al., 2002). This process is referred to as carcinisation, an example of convergent evolution (Tsang et al., 2011). Convergent evolution is the evolution of similar body forms or features that are not present in a most recent common ancestor. An example of convergent evolution can be seen with flight, which has evolved independently in insects, birds, and bats, from flightless ancestors. Gastropods are the group of organisms that includes all snails and slugs. Gastropods have evolved several times to either fully or partially reduce their protective shells in exchange for mobility, reduced energy needed to create a shell, expanded diets, and increased chemical defenses - with some even secreting acids! The loss of a shell requires other adaptations to provide defense. Here I introduce the idea of "Sluginisation" referring to the convergent evolution of slug-like form, in the same way that the evolution of a crab-like body plan is referred to as carcinisation. As part of this, I will be focusing largely on the main orders of sea slugs: nudibranchs, sacoglossans, pleurobranchs, sea hares and cephalaspideans (headshield slugs).
Snails make tasty treats for many marine organisms, if they can get the soft body beneath the shell (Feder 1963). In this case, a shell is a great form of defense from many would-be predators. A large number of other invertebrates have also evolved to create a calcium carbonate hard skeleton. However, the trade offs to having a shell are also present. The sequestration and deposition of calcium carbonate to create a shell is a metabolically expensive process (Faulkner and Ghiselin, 1983). Furthermore, lugging a heavy shell around is no easy feat. This is one possible explanation as to why there has been a reduction or loss of a shell in at least three classes of molluscs. Cephalopods, except for nautiloids, have traded their protective shell in return for mobility, a trait that some slugs have benefited from too. Some bivalves in the family Galeommatidae have even evolved to lose their shell and mimic slugs! The lack of a shell means that slugs are a seemingly easy source of food. This evolutionary disadvantage is a potential reason for the diversification of slugs.
In gastropods, defensive adaptations have evolved alongside the loss of the shell (Wagele et al. 2005). In fact, most of the defensive adaptations present in slugs do not occur in snails. A majority of slugs obtain their defenses from the food they eat (Faulkner and Ghiselin,1983). Aeolids, when munching on their cnidarian prey likes jellies and anemones, will sequester the unfired nematocysts (the stinging organelle in cnidarians) and store them in the tips of their cerata to deter predators (Wagele and Klussmann-Klob 2005). Furthermore, they may autotomise by shedding their cerata as part of a stress response. Dorids have been shown to sequester toxic compounds from the sponges they eat and concentrate toxins in glands along the mantle, called mantle dermal formations (MDF) (Wagele and Klussmann-Klob 2005, Winterset al. 2018). Sacoglossans store toxic compounds from the algae they eat within their body. Pleurobranchs can even secrete acid compounds to ward off predators. Some slugs with partially reduced shells still have chemical defenses sequestered from food, further supporting the idea that these defenses evolved alongside the loss of the shell. While there are snails with chemical deterences, they are the exception rather than the norm.
Terrestrial slugs are generally a drab brown meant to blend in with their natural habitat of foliage on the forest floor. Many sea slugs are quite the opposite, displaying bright colors as a form of aposematic colouration - a warning sign for potential predators that what they are about to bite into may not be tasty and can be dangerous. Some sea slugs, on the other hand, have gone the way of their terrestrial cousins in blending in with their environment like some Jorunna spp. seamlessly melding with its prey sponge with markings that resemble the sponge. Myja cf. longicornis even have cerata that are meant to mimic its hydroid prey. Other slugs, including many Cephalaspidea live in the muck where they will bury themselves into the sand with the aid of their headshield. Hiding in the sand is a type of camouflage that many slugs use for defense. Some species are so cryptic that they are almost impossible to find in the wild.
This myriad of defensive adaptations may help explain why slugs have such an effective body plan. Shelled gastropods rarely have these adaptations. Predation is something that all animals need to be resilient to, crabs have claws and a thick exoskeleton, snails have shells, and slugs have many adaptations as mentioned before. Adaptations like these are what make slugs so diverse in shape, color, diet, behavior, and are what have allowed sluginisation to occur.
Land snails have a seemingly greater benefit of having a shell. Their shell not only provides shelter and protection against predators but also serves as a method to limit desiccation, the drying out of a snail. However, land slugs still exist! Terrestrial slugs and sea slugs have convergently evolved a shell-less existence. While sea slugs likely lost their shell to save energy, land slugs may have evolved due to lower amounts of calcium in the terrestrial environment (Hausdorf, 2001). This is supported by the fact that terrestrial snails have thinner shells than their marine cousins (Goodfriend 1986) . Slugs, on the other hand, secrete a slimy mucus. While sea slug mucus is often toxic to deter predation, land slugs use their mucus to retain water. Without the ability to retain moisture using a shell, land slugs are also confined to humid environments, limiting somewhat the progression of diversity in land slugs. The benefit they receive from losing this shell is more similar to Cephalopods in that they gain improved maneuverability, allowing them to squeeze into tighter spaces. The selective pressures in land slugs are vastly different to sea slugs. However, both have evolved from a shelled ancestor suggesting that sluginasation is present in both the terrestrial and marine environment.
Although all nudibranchs have completely lost their shell and have become full slugs, other groups of slugs such as sacoglossans and cephalaspidea have species that have only partially reduced their shell. The cephalaspidean superfamilies Bulloidea and Haminoeoidea (bubble snails) have species with a very thin, reduced external shell which they can still withdraw into. Other Cephalaspidea have internalised their reduced shells making the shells almost impossible to see in living specimens. This partial reduction of shells in Cephalaspidea and more primitive traits such as gizzard plates and lack of true rhinophores suggests that cephalaspidea are potentially a more ancestral form of slug that have not fully evolved to lose their shells. In a study of two Cephalaspidean, it was shown that there were more repulsive defensive chemicals in a thicker shelled species than the thin, reduced shell species (Neves et al., 2008). This suggests that while many slugs may have evolved chemical defenses alongside shell reduction, this theory may not apply throughout all shell reduced slugs. Further studies into shell reduction across other groups have to be completed before a precise conclusion can be drawn on a reason for shell reduction.
Gastropods are a varied and diverse class of organisms, though most of what has been discussed so far is about slugs, they make up the minority of gastropods. Although slugs may be an effective evolutionary adaptation, snails are still much more diverse than slugs. This could be as a result of slugs being a more recently adapted form. Or it could also represent the effectiveness of a snail. However, completely shell-reduced slugs are not fossilised, so there is very little paleontological evidence of slugs. Which may mean that a clear conclusion cannot be drawn on whether slugnisation truly represents convergent evolution or whether it is a sign of parallel evolution. While there is some uncertainty in the evolution of slugs, findings can still be drawn based on genetic distinctions. A 2009 paper confirmed that the common ancestor of all slugs is a snail based on genetic taxonomy (Dinapoli and Klussmann-Klob 2009).
Understanding more about sea slugs helps us better understand what we see on a dive or exploring tide pools. Sea slugs are becoming an especially sought-after highlight in many diving communities around the world, with “sea slug hunters” sharing their finds on groups such as Sea Slug Thailand. This charismatic nature of sea slugs have further increased the economic gain in scuba diving by attracting visitors to more “muck habitats” promoting tourism in less visited areas and reducing strain on the reefs (De Brauwer etal., 2017). Similar to trees in the forests, calcifying marine organisms like corals and sponges make up the structure and basis of many marine ecosystems. Ocean acidification, caused in large part by increasing CO2 emissions are a great threat to this foundation. Ocean acidification could potentially have a tremendous effect all calcifying marine organisms (Coleman et al. 2014). Ocean acidification not only affects snail sand slugs but also causes reef building calcifying organisms to expend more energy into creating their skeleton. Slugs are not only just a pretty sight to see while diving, they can also be used as a model species to understand the effects that CO2 emissions have on all marine organisms.
The various forms of slugs are a testament to evolutionary change and the selective pressures that have created so many marvels of nature. Although the selective pressures causing sluginisation are different between land and sea the end result is the same, a slug or semi slug-like form. This is a clear trend throughout many gastropod lineages. Evolution works through selective pressure causing advantageous traits to be passed onto future generations. Convergent evolution is simply selective pressures causing certain forms in a group of organisms, in the crab-like crustacean this is called carcinisation. So can sluginisation be used to represent the trend of gastropod evolution into a slug-like form? Perhaps more investigation into these remarkable animals will tell us!
