Utter basics of snails (+ a comparison of writing styles)

This blog has made me a target for many e-mails from people seeking help or literature or recommendations, which I almost always answer (if they make it through my tyrannical spam filters).  These are usually  undergrads or teachers, but once in a while I get an e-mail that melts my otherwise solidified charcoal heart. Case in point:

Adorable. I usually don’t bother publishing my replies because there is often a lot of context that needs to be stripped away, but I thought it’d be interesting to do it in this case, to contrast writing for a 10 year old with writing for my usual audience. So here you will find my reply to this e-mail (minus extra links and recommendations), followed by the same thing written for a more advanced audience. (Sidenote: I have great difficulties writing for young children, although I have no problem explaining things to them in person, as I do when teaching. It requires a special talent and style to write for young kids.)

---

10 year old:

Snails are molluscs. They’re related to animals like octopi and squid (cephalopods) and oysters (bivalves). We know they are related because these three groups of animals have a shell and a radula, which is a structure used for scraping food off the ground and that looks like a tongue with many small teeth in it.

The biggest difference between snails and other molluscs is that the snail body twists when it’s developing. This is called torsion. It is why a snail shell is coiled and also why the genitalia and anus of the snail are at the front of the animal. Another difference is that snails have a pair of tentacles on the head that they use like insects use their antennae.

Snails are the second most diverse group of animals (first is insects). There are 6 big groups of snails:

• Patellogastropoda: limpets;
• Vetigastropoda: e.g. top shells;
• Neritimorpha: nerites;
• Coccunilida: cocculinoids;
• Caenogastropoda: e.g. periwinkles, whelks, cones, abalones;
• Heterobranchia: e.g. slugs, majority of terrestrial gastropods.

Snails are found everywhere in the oceans, even the extreme environments like the super-hot hydrothermal vents. They are the only molluscs on land and are also found everywhere (except Antarctica).

Snails have always been a big part of our culture. Archaeologists have found jewellery thousands of years old made from snail shells. They are also edible – land snails are a delicacy of French cooking, and marine snails are also regular food in countries where people collect them from rock pools or at low tide.

---

Public/Undergrad:

Gastropods, commonly known as snails, are molluscs. We know this because they share several key molluscan traits:

• A shell secreted by the mantle;
• An open circulatory system;
• The circulatory system doubles as a hydrostatic skeleton;
• A radula for feeding;
• A muscular foot;

The head of gastropods bears a pair of eyes, with the unique addition of a pair of tentacles, all used for sensing their environment. Another key difference between gastropods and other molluscs is that gastropods undergo torsion during late development – a 180° rotation of the body, minus head and foot, that ultimately causes the typical coiling of the shell. In some families, the rotation is only 90°.

Torsion has its most major effect on the internal anatomy of the gastropod, making it completely different from anything you’d see in a cephalopod or bivalve despite all the structures and organs being the same. Symmetry is lost in everything, with most organs being displaced to one side of the body and any counterparts on the other side reduced or absent (see: Lindberg & Ponder (2001)). Also, the anus and genitals go to the front of the animal.

Gastropods are the most species-rich animal group after the insects, and all known gastropod species fall into one of these taxa:

• Patellogastropoda: limpets;
• Vetigastropoda: e.g. top shells;
• Neritimorpha: nerites;
• Coccunilida: cocculinoids;
• Caenogastropoda: e.g. periwinkles, whelks, cones, abalones;
• Heterobranchia: e.g. slugs, majority of terrestrial gastropods.

In the oceans, they’re present in all habitats, including extreme ones like hydrothermal vents. Additionally, many families have convergently invaded freshwater and conquered land – the latter a significant feat making gastropods the only known terrestrial molluscs. Land snails are as successful as their marine counterparts, found on all continents except Antarctica.

Being both species-rich and conspicuous automatically makes gastropods important in human culture. We have evidence from archaeology showing humans using them and their shells in much the same uses as today: mostly jewellery and eating. Everyone knows the escargots of French cuisine, but many marine species are also edible. Abalones, periwinkles, whelks, and many other groups with species easily found in rock pools or intertidal zones are regular food sources in many coastal areas of the world. They’re also great if you’re doing fieldwork and have run out of canned food and can’t be bothered to smear yourself in dung and sharpen a spear to hunt a wild deer.

Top Research of 2012: Zoology

Jump to: Arthropods; Botany; Developmental Biology; Ecology; Evolution; Environmental; Geology; Historical Geology; Human Evolution; Palaeontology.

Last but not least, my picks for the top 10 zoology papers of the year, with the caveat that I took the majority of stuff I follow, because nobody is really interested in the ultrastructure of annelid sperm-producing cells. So the papers listed here have some sort of general appeal, or so I hope. The revised master list contains 42 papers. [OA] indicates open access papers.

---

10. How does the blue-ringed octopus (Hapalochlaena lunulata) flash its blue rings?

Everyone’s at least heard of the blue-ringed octopus, famed for its deadly toxicity. Like most venomous animals though, they advertise it using the name-giving blue rings, of which there are 60. When threatened, the octopus flashes them to produce blue iridescence. Octopi have two ways to produce colour: iridophores, cells with plaques that reflect light in wonky ways; or chromatophores, sacs which produce colours chemically with pigments. This paper finds that the blue rings are made by iridophores, but with a twist: the iridophores aren’t just found on the surface, they’re integrated into special skin pouches. So when under threat, the muscles will automatically contract, turning the iridophores on mechanically. This contraction will also cause brown chromatophores to form a ring around the iridophores, thus increasing the intensity of the blue. This is also why the blue-ringed octopus flash is so extremely quick: it takes 1/3 of a second for the flash to be produced, and the speed is due to this smart mechanical system.

---

9. The erection mechanism of the ratite penis.

Just catering to fellow fans of juvenile humour. Although, to be fair, bird penises are fairly interesting, as exemplified by the explosive erections of ducks.

---

8. A multi-gene phylogeny of Cephalopoda supports convergent morphological evolution in association with multiple habitat shifts in the marine environment. [OA]

This paper presents a phylogeny of the cephalopods. It’s fairly comprehensive with 188 species and only a handful of families missing, and the topology doesn’t contradict previous research. The authors then plotted 6 characters and did ancestral trait reconstructions, as seen above, where coliur represents presence, white repesents absence, and black represents unknown. From left to right, these are: accessory nidamental gland; cornea; autogenic photophore; bacteriogenic photophore; branchial canal; and right oviduct. On the right, they did the same but with depth: grey represents benthic lifestyles, white are pelagic, and black is unknown. This exercise gives two main results, which you cans ee for yourself as well: in the evolution, cephalopods moved a lot between habitats, and with the shifts followed many convergent losses and gains of certain traits.

Speaking of evolution of depth preferences in cephalopods, Vestigial phragmocone in the gladius points to a deepwater origin of squid (Mollusca: Cephalopoda) looks at the gladius of squid and homologises it with fossil belemnite features, which, together with the decalcification of squid, hints at a deep water origin of squid.

---

7. An Asian Elephant Imitates Human Speech. [OA]

An elephant that can speak Korean. No kidding. Check the B graph above, and you’ll see that this male Asian elephant can pretty much identically imitate the frequency of the respective vowels. The imitation is so good that Koreans can understand and transcribe what the elephant is saying. It won’t be long until they can start understanding nuclear weapon schematics, and knowing the aggression of elephants, that’s not a good thing. Be afraid, everyone.

If, for some strange reason, you have an affinity for elephants, then you’ll be interested in What Is the Use of Elephant Hair? [OA] for giving you the answer to that titular age-old question. Spoiler alert: it helps with heat loss, something that elephants need to sustain their size.

---

6. Evolution of the turtle bauplan: the topological relationship of the scapula relative to the ribcage.

Turtles are known as an all-around zoological mindfuck. Their phylogeny is all over the place, their shell is unique, as is the position of the shoulder girdle. In this paper, the authors document the shoulder girdle’s position and relation to the ribcage and shell in all major amniote groups. The result is that the turtle condition isn’t the wonky one – it’s actually the basal condition from which the shoulder girdle of the other amniotes evolved. This has numerous implications, on the one hand for our conception of amniote evolution, and on the other hand for the way we study turtles. Nowadays, we compare the development of the turtle with development in chickens and mice. But, as this paper shows, mice and chickens are completely unsuitable because they’re evolutionarily too derived to be of any use for the question (that’s also a criticism I level to almost all model organism-centered research, but that’s outside the scope here).

More support for this model can be found in some phylogenies that find that lizards and turtles are closely related. These have traditionally been a subset of morphological phylogenies, but now a molecular one, MicroRNAs support a turtle + lizard clade, has been published too.

---

5. The oyster genome reveals stress adaptation and complexity of shell formation. [OA]

Oysters may look peaceful, but their lives are very stressful. They live in an environment where their shell is the only defence against predators, and where they are subjected to drastic environmental changes when at low tide. A lot of their coping mechanisms are epigenetically-mediated, e.g. the number of size of spines on spiny oysters are a function of how many predators are around, but there is a lot of underlying genomic machinery enabling those. This paper presents a draft genome of the oyster Crassostrea gigas and finds that they have a lot of unique genes related to stress tolerance (see diagram above) and controlling the formation of the shell. I’d be interested in comparing with other oysters that may not live in intertidal habitats.

---

4. Metazoan opsin evolution reveals a simple route to animal vision.

Whatever challenges once existed to explain the evolution of vision have all crumbled away. While I find the popular explanation a bit lacking and simplistic for my tastes, the full version of the morphological explanation is clear. This paper takes care of the molecular side by showing that opsins, one of the main photopigment classes, evolved as parsimonioulsy as one could imagine: it can all be explained with just two duplications in the neuralian stem, and one earlier on, as shown in the diagram above.

But why limit ourselves to opsins? Vision is even found in the sponges, those nerve-less animals. As Blue-light-receptive cryptochrome is expressed in a sponge eye lacking neurons and opsin shows, the sponge larva can follow light and uses a cryptochrome pigment in a ring structure to do so. This ring structure thus counts as an eye.

Speaking of eyes, A Unique Advantage for Giant Eyes in Giant Squid tells us why giant squid have giant eyes: to detect predators more than 100 meters away, even in the deep sea.

---

3. The First Record of a Trans-Oceanic Sister-Group Relationship between Obligate Vertebrate Troglobites. [OA]

The awesome result fo this paper is based on a new molecular phylogeny of the gobies. The result is shown in the diagram above: the genera Typhleotris and Milyeringa are sisters, I.e.t hey descend from the same common ancestor. Both of thes egenera are troglobitic, living in caves. But here’s the spectacular thing: one genus is endemic to Australia, the other to Madagascar. That these two are sister means that they split from each other back when eastern Gondwana broke up in the mid-Cretaceous, so this is a case of long-term vicariance. Although there is the alternate possibility that the split happened afterwards in the proto-Indian Ocean, either case is a testament to the importance of integrating (palaeo)geography into evolutionary studies.

---

2. Evolution of a Novel Muscle Design in Sea Urchins (Echinodermata: Echinoidea). [OA]

The picture above shows the position and details of a type of muscle found in some sea urchins, called frilled protractor muscle. It’s a strange type of muscle found interacting with Aristotle’s Lantern (the “teeth” of a sea urchin), and this study looks at its taxonomic distribution in detail using MRI. The main difference between these muscles and the others are that these ones have frills, which in turn allows more muscle fibers to reach a greater area – it’s basically increasing the surface area to volume ratio. There is no certain function for them yet: the authors found no correlation except that the species that have them also have keeled teeth, so it may be related to feeding; otherwise, the surface area:volume ratio increase could provide a metabolic advantage. However, without a robust phylogenetic tree for the sea urchins (doesn’t exist yet), nothing can be said for sure yet, although the authors tentatively say it’s a monophyletic feature (I’d say it’s the opposite, but a phylogenetic tree is needed to confirm anything!). In any case, any new type of muscle is a cool finding, which is why this gets a top spot. Another reason is for demonstrating that methodological advances always happen in zoology (nowadays, use of such advanced imaging techniques), so we zoologists do need funding.

Independent evolution of striated muscles in cnidarians and bilaterians is somewhat related in that it also deals with new muscle types, finding that the genetic core underlying striated muscles are already present way back in the unicellular protozoans, and are even expressed in sponges. Analysis of the genetic repertoire and expressions of these necessities for striated muscle then showed that cnidarians and bilaterians evolved them convergently, with cnidarians missing some key aspects of bilaterian striated muscle, and expressing those genes for purposes other than striated muscle.

---

1. Neural Correlates of a Magnetic Sense.

That birds can sense the magnetic field has long been known. Recently, experiments have shown that they detect the magnetic field through magnetic pigments in one of their eyes. Now this paper adds more pieces to the puzzle by finding how the information is encoded for transmitting to the brain of the homing pigeon. Basically, there are 53 single neurons in the brainstem that record the direction, intensity, and polarity of the magnetic field.

Another interesting brain- and locomotion-related paper is Specialized brain regions and sensory inputs that control locomotion in leeches, which experimentally finds out which brain regions control which aspects of swimming and crawling in a leech.

---

Well, that’s it for the “2012 in review” series. Hope you enjoyed it, and you can expect a repeat at the end of this year.

Jump to: Arthropods; Botany; Developmental Biology; Ecology; Evolution; Environmental; Geology; Historical Geology; Human Evolution; Palaeontology.

Elysia and Other Photosynthetic Sea Slugs

Elysia is an “opisthobranch” sea slug famous on the internet for its remarkable ability to photosynthesise, giving it the nickname of “solar-powered sea slug”. It does this by kleptoplasty – stealing plastids from its algal food. If you note the greenish colour in E. asbecki above (Wägele et al., 2010), the green comes from the harvested chloroplasts. This post will look at this process, and generally at the biology of the genus.

Before starting, it’s worth noting that while Elysia is the most famous of these examples on the internet, it’s definitely not the only animal that can photosynthesise by symbiosis with algae. Falkowski & Knoll (2007) have a three page-long table (pp. 90-92) listing various eukaryotes where this has been documented, including sponges, corals, ascidians, flatworms, and bivalves.

E. chlorotica, if internet fame is anything to go by, is probably the poster child for the phenomenon, and also the one that exhibits it the best. It can harvest the chloroplasts from any number of ulvophycean and xanthophyte algae, but the most successful relationship is with the xanthophyte alga, Vaucheria litorea. The chloroplasts get sequestered intracellularly in the digestive epithelium, and stay functional for over 14 months (Rumpho et al., 2006). This isn’t just an opportunistic relationship, but one that has evolved into a real symbiosis, as evidenced by the identification of lateral transfer of V. litorea nuclear genes into the E. chlorotica genome (Schwartz et al., 2010), most tellingly the transfer of the oxygenic photosynthesis gene, psbO, and fcp, associated with light-harvesting complexes (Rumpho et al., 2008). This is also the reason why naming it a symbiosis may be a mistake, as it doesn’t involve two genetically independent organisms (Law & Lewis, 1983). Nomenclature aside, the chloroplast is hugely beneficial for the slug, as it provides “free” carbohydrates at times when food isn’t available (e.g. in winter, when host algae don’t grow).

Interestingly, the algal chloroplast loses its host membrane and outer two of the four chloroplast membranes (Rumpho et al., 2000) and is found free-living in the cytoplasm in adults after getting phagocytosed (Rumpho et al., 2000). In juveniles, they are bound within a special membrane.

Elysia contains over 120 species, accounting for ~40% of all sacoglossans. In fact, the phenomenon was first discovered in E. atroviridis, not E. chlorotica (Kawaguti & Yamasu, 1965), with functionality of chloroplasts documented by Taylor (1967) and evidence that the chloroplasts contribute to the animal’s metabolism by Trench et al. (1972). Other Elysia species do not nearly have E. chlorotica‘s efficiency, with most retaining the chloroplast for a couple of months at best, after which the chloroplasts degrade and get enveloped in phagosomes and presumably digested (Marín & Ros, 1993). Feeding allows chloroplasts to get replaced, but this is limited by the presence of algae. It is however notable that chloroplasts from multiple species can get sequestered (Curtis et al., 2006), so it’s not necessarily a specific interaction.

Elysia belongs to the Plakobranchidae, a family where long-term plastid retention is autapomorphic (Händeler et al., 2009) and lasts over a couple of weeks generally, but outside of the family, the association lasts for no more than a week. Individuals behaviourally try to control light intensity in order to maximise the lifespan of the inherited chloroplasts and to regulate photosynthesis rate (Casalduero & Muniain, 2008), but at some point, the chloroplasts just stop working.

A very valid question to ask is how such an association can arise. The ability to acquire plastids from food is most probably an ancestral one in sacoglossans, and is linked to one of the main autapomorphies of the Sacoglossa, a radula with only one row of teeth and one median tooth (Mikkelsen, 1996; pictured above from E. asbecki from Wägele et al. (2010)), which is what allows the animal to pierce the algal cell and suck out the plastids (Jensen, 1997). This is a feeding style that is highly-specialised and not found anywhere else in the molluscs, and underlies the reason why sacoglossans feed only on septate and siphonous algae, with only some also feeding additionally on other plants such as seagrass (Jensen, 1981). Each species, depending on their specificity, can also have further modifications to fit the radula perfectly to its host plant (Jensen, 1994), and it’s likely that host shifts can play a role in diversification and speciation, as hinted at by Trowbridge & Todd (2001)‘s work on the shifting of a Scottish subpopulation of E. viridis to feeding on an invasive alga within the past 50 years.

The retention of plastids can be imagined as having considerable fitness benefits, for example a free food source in the winter when algae don’t grow, or conferring a defensive adantage as camouflage – once they ingest the chloroplasts, the slugs turn green, identical to the background, and this is a tremendous advantage considering their lack of shell. There is also some evidence that their food gives them defensive compounds to sequester as well as chloroplasts, for example chlorodesmin, a fish repellent (Hay et al., 1989).

On to Elysia‘s general biology. The monophyly of the genus is not known for sure, and is strongly supported only by molecular phylogenies (Händeler et al., 2009). Truly diagnostic macroscopic features are not to be found, as is clear from field guides, where sacoglossans are all lumped together as unidentified morphospecies. So if you happen to catch one (your best bet is to look carefully in algal meadows, at any depth, keeping in mind that they will be well-camouflaged), your best bet is to consult an expert or trawl through seaslugforum.net.

As all gastropods, Elysia mating involves “love darts”. Schmitt et al. (2007) describe the process in E. timida, where it basically amounts to a synchronised shooting of hypodermic love darts, followed by a short period of standard vaginal impregnation aided by glandular fluids. You can view3 videos from that paper here. Elysia‘s life cycle involves a planktonic larval stage, with the veliger larva having a sinistral shell and dispersing for a couple of weeks or more. The metamorphosis to the adult takes place when the veliger attaches itself to a film of microorganisms growing in an alga-rich habitat.

If you enjoy my blog, please consider supporting my scientific research by sharing and/or donating to my Petridish project. Thank you!

References:

Casalduero FG & Muniain C. 2008. The role of kleptoplasts in the survival rates of Elysia timida (Risso, 1818): (Sacoglossa: Opisthobranchia) during periods of food shortage. Journal of Experimental Marine Biology and Ecology 357, 181-187.

Curtis NE, Massey SE & Pierce SK. 2006. The symbiotic chloroplasts in the sacoglossan Elysia clarki are from several algal species. Invertebrate Biology 125, 336-345.

Falkowski PG & Knoll AH. 2007. Evolution of primary producers in the sea.

Green BJ, Li W-J, Manhart JR, Fox TC, Summer EJ, Kennedy RA, Pierce SK & Rumpho ME. 2000. Mollusc-Algal Chloroplast Endosymbiosis. Photosynthesis, Thylakoid Protein Maintenance, and Chloroplast Gene Expression Continue for Many Months in the Absence of the Algal Nucleus. Plant Physiology 124, 331-342.

Händeler K, Grzymbowski YP, Krug PJ & Wägele H. 2009. Functional chloroplasts in metazoan cells – a unique evolutionary strategy in animal life. Frontiers in Zoology 6, 28.

Hay ME, Pawlik JR, Duffy JE & Fenical W. 1989. Seaweed-herbivore-predator interactions: host-plant specialization reduces predation on small herbivores. Oecologia 81, 418-427.

Jensen KR. 1981. OBSERVATIONS ON FEEDING METHODS IN SOME FLORIDA ASCOGLOSSANS. Journal of Molluscan Studies 47, 190-199.

Jensen KR. 1993. Morphological adaptations and plasticity of radular teeth of the Sacoglossa (= Ascoglossa) (Mollusca: Opisthobranchia) in relation to their food plants. Biological Journal of the Linnean Society 48, 135-155.

Jensen K. 1997. Evolution of the Sacoglossa (Mollusca, Opisthobranchia) and the ecological associations with their food plants. Evolutionary Ecology 11, 301-335.

Kawaguti S & Yamasu T. 1965. Electron microscopy on the symbiosis between an elysioid gastropod and chloroplasts of a green alga. Biological Journal of Okayama University 11, 57-65.

Law R & Lewis DH. 1983. Biotic environments and the maintenance of sex–some evidence from mutualistic symbioses. Biological Journal of the Linnean Society 20, 249-276.

Marín A & Ros J. 1993. ULTRASTRUCTURAL AND ECOLOGICAL ASPECTS OF THE DEVELOPMENT OF CHLOROPLAST RETENTION IN THE SACOGLOSSAN GASTROPOD ELYSIA TIMIDA. Journal of Molluscan Studies 59, 95-104.

Mikkelsen PM. 1996. The evolutionary relationships of Cephalaspidea s.l. (Gastropoda: Opisthobranchia): a phylogenetic analysis. Malacologia 37, 375-442.

Rumpho ME, Summer EJ & Manhart JR. 2000. Solar-Powered Sea Slugs. Mollusc/Algal Chloroplast Symbiosis. Plant Physiology 123, 29-38.

Rumpho ME, Dastoor FP, Manhart JR & Lee J. 2006. The Kleptoplast. Advances in Photosynthesis and Respiration 23, 451-473.

Rumpho ME, Worful JM, Lee J, Kannan K, Tyler MS, Chattacharya D, Moustafa A & Manhart JR. 2008. Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. PNAS 105, 17867-17871.

Schmitt V, Anthes N & Michiels NK. 2007. Mating behaviour in the sea slug Elysia timida (Opisthobranchia, Sacoglossa): hypodermic injection, sperm transfer and balanced reciprocity. Frontiers in Zoology 4, 17.

Schwartz JA, Curtis NE & Pierce SK. 2010. Using Algal Transcriptome Sequences to Identify Transferred Genes in the Sea Slug, Elysia chlorotica. Evolutionary Biology 37, 29-37.

Taylor DL. 1967. THE OCCURRENCE AND SIGNIFICANCE OF ENDOSYMBIOTIC CHLOROPLASTS IN THE DIGESTIVE GLANDS OF HERBIVOROUS OPISTHOBRANCHS. Journal of Phycology 3, 234-235.

Trench RK, Trench ME & Muscatine L. 1972. Symbiotic Chloroplasts; Their Photosynthetic Products and Contribution to Mucus Synthesis in Two Marine Slugs. Biological Bulletin 142, 335-349.

Trowbridge CD & Todd CD. 2001. HOST-PLANT CHANGE IN MARINE SPECIALIST HERBIVORES: ASCOGLOSSAN SEA SLUGS ON INTRODUCED MACROALGAE. Ecological Monographs 71, 219-243.

Wägele H, Stemmer K, Burghardt I & Händeler K. 2010. Two new sacoglossan sea slug species (Opisthobranchia, Gastropoda): Ercolania annelyleorum sp. nov. (Limapontioidea) and Elysia asbecki sp. nov. (Plakobranchoidea), with notes on anatomy, histology and biology. Zootaxa 2676, 1-28.

Research Blogging necessities :)

Katharina Händeler1, Yvonne P Grzymbowski, Patrick J Krug, & Heike Wägele (2009). Functional chloroplasts in metazoan cells – a unique evolutionary strategy in animal life Frontiers in Zoology DOI: 10.1186/1742-9994-6-28
Mary E. Rumpho, Elizabeth J. Summer, & James R. Manhart (2000). Solar-Powered Sea Slugs. Mollusc/Algal Chloroplast Symbiosis Plant Physiology DOI: 10.1104/pp.123.1.29
Mary E. Rumpho, Farahad P. Dastoor, James R. Manhart, & Jungho Lee (2006). The Kleptoplast Advances in Photosynthesis and Respiration DOI: 10.1007/978-1-4020-4061-0_23