Sea slug regrows entire body from just the decapitated head, or “autotomy with kleptoplasty”

March 9, 2021 • 9:45 am

Imagine if Robespierre, after being guillotined during the Terror in France, was able to regrow his entire body just from his head alone. Well, that’s the equivalent of what some sea slugs can do, as reported in the new issue of Current Biology (click on screenshot below to access article, pdf here, and reference at the bottom).

In fact, two species of sacoglossan sea slugs, members of a group of shell-less mollusks, can not only grow a new body from just the head, but can do it twice in a row. Amazingly, the body that gets regrown includes the heart and the digestive system, which makes one wonder: how can they regrow a whole body without the nutrients gleaned from digestion? And how can the head live without a heart to supply it with oxygen. Well, that’s part of a very cool story.

Two Japanese researchers found that a substantial proportion (33%) of two species of sea slugs (Elysia cf. marginata and E. atroviridis) were observed in the laboratory to shed their own heads (“autotomy”, a fancy word for “self amputation”). Moreover, the heads regenerated new bodies—and quite quickly: within 20 days or so. The shed bodies, which did not regenerate new heads but died, contained the heart and the digestive systems.  The heads, meanwhile, closed the wound after “voluntary” separation, began nibbling on algae within hours, and the regeneration of the entire body was done within three weeks.

Here’s a shot of four phases of the autotomy from the paper (as is the caption):

A) Head and body of Elysia cf. marginata (individual no. 1) just after autotomy (day 0), with the pericardium (heart) remaining in body section (arrow). (B) day 7, (C) day 14, (D) day 22, showing whole-body regeneration.

 

The 10 mm scale bar is about 0.4 inches.  By day 22 they’re fully whole again, with a beating heart and a digestive system. See the green color? Those are algae that live in the mollusk’s cells: a key to how they might get the energy to regenerate.

Here’s a tweet with a video of the separated head and body. It’s just bizarre!

But wait! There’s more! The authors collected 82 sea slugs from the ocean that were all parasitized by the copepod Arthurius, which lives in the body (not the head) and inhibits the sea slug’s reproduction. Many of the parasitized slugs got rid of their bodies when brought to the lab. Here’s the parasite:

(J) Arthurius sp., the internal parasitic copepod of Elysia atroviridis.

This gives a clue as to why they’re ditching their bodies: to get rid of a parasite that lives in the body and impedes reproduction of the sea slug. Thus, it might be adaptive to discard your body along with a parasite, even if it takes substantial energy to regrow a new body.

Of 82 parasitized individuals collected from the wild, 41 shed their bodies. Of these, 13 regenerated those bodies, but the rest died. So there’s no guarantee that you’ll survive if you shed your parasite-laden body. But if you’re permanently sterilized by the parasite, or your reproduction is severely reduced, it may still be adaptive to take the chances and break apart; your net fitness may be higher that way. After all, the regenerated bodies, lacking parasites, are perfectly fertile.

More indication that this trait is adaptive is that these sea slugs have a “transverse groove” at their neck—the line where the breakage occurs. This implies that parasitism and body-shedding was a regular feature of the sea slugs’ past. Here’s the groove, which you can see if you look closely:

(I) Healthy individual of Elysia cf. marginata with a ‘breakage plane’ at their neck (dotted line).

When the authors tied nylon string around the groove, the slugs broke apart at this position, shedding a body that represents 80-85% of their total weight. When mock predator attacks took place, however, like pinching the head and cutting parts of the body, they did not break apart. This suggests that autotomy, if it’s an adaptation, is an adaptation to get rid of parasites and not to escape predators. (Many animals shed body parts when attacked, like lizards and salamanders that drop their tail when a predator grabs it.)

One question remains: where do the severed heads get the energy to regenerate an expensive body? The answer is another fancy word: kleptoplasty. Here’s how the authors explain it:

Why these sacoglossans can regenerate their body even if they lose most organs remains unclear, but we suspect involvement of kleptoplasty. In Elysia, a highly branched digestive gland is spread over the majority of its body surface, including the head, and the gland is lined by cells that maintain ingested algal chloroplasts. Thus, these sacoglossans can obtain energy for survival and regeneration from photosynthesis by kleptoplasts, even when they cannot digest food.

My question in response to this is: “do they get everything they need to regrow a body from the algal chloroplasts, including amino acids, sugars, and fats?”  I suspect they do: where else could they get them? But perhaps a little digestion occurs in the mouth as well.

Where does this fit into biology? The phenomenon of autotomy is well known, as is the ability of many animals to regrow lost parts (you may have done such an experiment with flatworms when you were in high school). What’s unusual here is the regeneration of the entire complex body after it’s jettisoned, including the heart, which you would think was needed to keep the head alive! The authors say this:

Both Elysia cf. marginata and E. atroviridis shed the main body, including the heart. Some other sea slugs also autotomise, but they shed minor body parts such as tails, parapodia, or dorsal papillae. Other invertebrates (e.g., cnidarians, planarians, and asteroids) can regenerate their main body following division. Also, some amphibians are known to have a high regeneration capacity, including tails, limbs, eyes, and even the heart ventricle. However, autotomy in this study is remarkable in that animals with complex body plans can survive even if they lose the main body, including the heart, and subsequently regenerate the whole lost area. The reason why the head can survive without the heart and other important organs is unclear. We have succeeded in a complete rearing of Elysia cf. marginata for multiple generations — thus, they can be used as a model system for studying autotomy and regeneration of the body.
Now it’s no surprise that the animal has the potential to regenerate the body: after all, every cell in a sea slug contains all the genetic information necessary to produce another entire sea slug. But the trick is how to mobilize that information, which is usually inactivated in the wrong parts of the body. (We don’t activate the genes producing a liver, for instance, where our heart is supposed to be.) Somehow there is a mechanism here that makes the regenerating cells totipotent: capable of producing any part of the body starting at time zero. If we could figure out how they do this, we might be able to do it to ourselves, regrowing lost or diseased organs. But that is pure speculation; after all, we are not invertebrates—except for George Bridges at The Evergreen State College.

 

h/t: Matthew

_____________

Mitoh, S. and Y. Yusa. 2021. Extreme autotomy and whole-body regeneration in photosynthetic sea slugs. Current Biology 31:R233-R234.

25 thoughts on “Sea slug regrows entire body from just the decapitated head, or “autotomy with kleptoplasty”

  1. Chloroplasts are only able to provide photosynthate, which is fixed carbon in the form of sugars. I don’t know where they get the fats and amino acids; perhaps as Jerry suggests through the head.

  2. Incredible! This article has introduced me to a fascinating new subject that I hadn’t thought of before — regeneration. Imagine the possibilities of what today seems impossible!

  3. Very cool science, thanks!

    The phenomenon of autotomy is well known, as is the ability of many animals to regrow lost parts

    I vaguely recall that limb regeneration is common enough that it may be more apt to say that most if not all mammals have lost the ability, rather than exclaim how remarkable it is that other types of animals have it.

    As to why we would lose it, my WAG would be that regrowth isn’t all that fitness-improving in big mammals (uh…pre-20th century technology). You most likely die faster than you can regrow it (and in many cases – immediately from blood loss). It’s probably most useful for animals who can either regrow limbs fast, or who can find ways to ‘hole up’ and greatly reduce their food requirements while they go through regrowth.

    1. The human infant allegedly has a limited degree of regenerative ability – limited replacing to the tips of digits if lost before the age of (several years). I’m not sure if the ability extends to below the level of the nail bed, or past the distal finger bone. Including a new tissue not present at the wound would be a challenge.
      It’s an area of active research. But I recall it having been an area of research in the late 1970s, and I haven’t heard much progress in the subject between then and now. Which doesn’t bode well for dramatic advances this side of next Friday.
      Further out into the vertebrates, but still within the air-breathing vertebrates, people have been investigating the ability of “salamanders” (I’m not sure how closely defined) to regenerate an entire stereotypical pentadactyl limb from severance in the first bone (humerus/ femur equivalent). That’s another topic of investigation that goes back 30 plus years (in my memory) and probably a lot further.
      Hmmm. I’m wondering if the palaeontological record includes any evidence of a partly-regrown limb. I can’t recall such – and if I had read of such, I’m sure it would have gone into my head with trumpet fanfares and marching bands (Sousa marches?). There is plenty of fossilised evidence of partly or completely healed lesions, both traumatic and disease-formed (idiopathic?), on the skeletons of fossil vertebrates. And invertebrates.

      1. Complete regrowth of meaty part of fingertip at 7 happened to a childhood friend. [I know this because it was I who closed a door without looking where his hands were. Life’s lessons.:-/]

        This was recent news to me:

        Newborn mice and piglets exhibit natural heart regeneration after myocardial infarction (MI). Discovering other mammals with this ability would provide evidence that neonatal cardiac regeneration after MI may be a conserved phenotype, which if activated in adults could open new options for treating ischemic cardiomyopathy in humans.

        [ https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7017245/ ]

        1. Who learned a lesson more strongly? Your friend learning to be careful of door edges, or you learning to be careful of closing doors? Or as … was it Tolkein? … once said, “the burned hand teaches best”. (Looks at molten lead scar on one forearm, and “the chainsaw was definitely sharper after I’d finished” scar across the other hand. Where can I get X-rays of my education in traffic?)
          The MI information is news to me, but the neonatal heart goes through some drastic changes as the plumbing is re-plumbed in the minutes around birth. It is less than surprising that it is more tolerant to changes in this time interval than, say, 40 years later. After all, if your heart has made it to 40 years, your genes have probably had an opportunity to propagate by another generation, and your phenotype is less important to the genes now. A chicken being an egg’s way of making another egg.

  4. Fascinating! It’s so strange to see the head wondering around the body in that tweet above. Very weird ability.
    Thanks for this incredible information.

  5. Thank you. The story of the regeneration is very popular, but I hadn’t previously seen anything about the parasites, which is the main story.

    1. I agree, the ‘shedding of the body’ to get rid of parasites impeding replication is the most fascinating part.
      I wish I could do that, shedding my body and grow a new one!

      1. “He cut off his body to save his head.” There’s an SF story in there. And it has been followed at least once, in the aptly named Procrustes . Not to be confused with the story of Procrustes, oh no sirree!
        Note the bed in this vase composition.

  6. Truly astonishing – feeding having abandoned the digestive system and growing a new one? “There are more things in Heaven and Earth, Horatio, than are dreamt of in your philosophy.”

  7. Regeneration in humans, like other mammals, is pretty limited. Besides much of the liver, you can regenerate the tips of your fingers or toes. So imagine an accident with a lawn mover… If you want to see gruesome pictures, you can look this up online.

  8. I have a similar point to Stephanie (above) of whether the symbiotic algae can biosynthesize all of the necessary amino acids and lipids (let’s assume carbohydrates are covered). I found an analogous paper that algae appear to supply anemones with amino acids, determined using 14C labeling experiments. A simple experiment seems to be infect these sea slugs with the parasite and grow them in the dark. No photosynthesis, no algae, no regeneration. Whether some or all of the nutrients come from bacteria would require more study.

    https://link.springer.com/article/10.1007/s002270050619

  9. There was a British TV series-I think called The Strangerers-about plant like aliens who took human form to visit Earth (well England anyway). When one got bowled by a truck they put his head in one of those crocus jars so he could grow grow new legs. The show got very bad reviews as I recall but I thought it was quite amusing in an anthropological way of strangers arriving in a society they knew little or nothing about and trying to adapt.

  10. What an incredible creature. I wonder if it feels any pain during the process. I also wonder if a successful autonomy actually extends the slug’s life. After all, it’s a brand new body…though I guess the head would still age. 🤔

  11. The copepod looks fascinating too.

    My question in response to this is: “do they get everything they need to regrow a body from the algal chloroplasts, including amino acids, sugars, and fats?” I suspect they do: where else could they get them? But perhaps a little digestion occurs in the mouth as well.

    Maybe not so little, depending on how that gland works:

    Several species of Sacoglossan sea slugs capture intact, functional chloroplasts from algal food sources, retaining them within specialized cells lining the mollusc’s digestive diverticula. The longest known kleptoplastic association, which can last up to ten months, is found in Elysia chlorotica,[2] which acquires chloroplasts by eating the alga Vaucheria litorea, storing the chloroplasts in the cells that line its gut.[9] Juvenile sea slugs establish the kleptoplastic endosymbiosis when feeding on algal cells, sucking out the cell contents, and discarding everything except the chloroplasts. The chloroplasts are phagocytosed by digestive cells, filling extensively branched digestive tubules, providing their host with the products of photosynthesis.[10] It is not resolved, however, whether the stolen plastids actively secrete photosynthate or whether the slugs profit indirectly from slowly degrading kleptoplasts.[11]

    [ https://whyevolutionistrue.com/2021/03/09/sea-slug-regrows-entire-body-from-just-the-decapitated-head-or-autotomy-with-kleptoplasty/ ]

  12. Truly fascinating post! Thanks Jerry!
    The wide range of topics covered makes this one of the most interesting and informative web sites.

Leave a Reply