Research Study 1: Larval defenses

Post-torsional veliger larva of an abalone Haliotis tuberculata.  Note that the operculum can now close up tight like a hatch cover.

All marine gastropods undergo torsion during larval development.  This is a 180^o rotation of the shell and viscera relative to the head and foot of the veliger.  It usually occurs in two stages, the first being a quick twist effected by unequal contraction of retractor muscles; the second being a slow growth of body parts to complete the rotation. Shown here is a post-torsional veliger of an abalone Haliotis tuberculata (a European species). 

NOTE sometime referred to as ontogenetic torsion; in other words, occurring during the development of the snail – but, as this is the only time it does occur, it seems to be unnecessary jargon

NOTE the role of the retractor muscles in torsion is considered in abalones Haliotis kamtschatkana in Research study 3 below. For review see Page 1997 Acta Zoologica 78: 227 

Research Study 2: Larval defenses

Drawings of hypothetical pre-torsional adult snail and a contemporary post-torsional adult snail.

Courtesy Ghiselin 1966 Evolution 20: 337

There has been much conjecture about the function of torsion, and opinion is divided as to whether it benefits primarily the larva or the adult.  The major consequence to the veliger larva is that it can now retract its head and foot into the shell and seal it with the operculum (the operculum is produced at the same time as torsion occurs). Since this ability (see Right-hand drawing) carries over into the adult and provides protection for the adult against predators, drying, UV irradiation, and so on, there is no quarrel as to its post-metamorphic importance.  The intitial hypothesis for its function, proposed in the 1920s, is that it primarily benefits the larva (rather than the adult) by enabling it to protect its sensitive soft parts (head and velum) from being nipped off by planktonic predators.  But is this realistic?  Wouldn’t most predators either swallow veligers whole or crush their weak shells and then swallow the parts?  The idea for a larval function for torsion has lasted many decades and has many contemporary adherents.

Research Study 3: Larval defenses

Series showing normal torsion in a snail Calliostoma ligatum.

Series showing abnormal torsion in a snail Calliostoma ligatum caused by exposure to antibiotics.  Note absence of retractor muscles.

Shown on upper Left is normal torsion in a veliger larva of the trochid snail Calliostoma ligatum (the larva is about 300µm in shell diameter). The retractor muscles attach the larval body to the shell and allow the body to be pulled in (usually only partly, before torsion).  In the Pre-Torsion drawing, the foot is facing to the Right. At Mid-Torsion the foot has rotated 90^o, while at Final Torsion the foot has rotated almost 180^o and an operculum has formed. The larva is now able to pull into its shell and close off the opening. The scientist who originated the larval-defense theory, Walter Garstang, thought that a sudden mutation imposed an asymmetry on these muscles in an otherwise symmetrical ancestral larva, thus torquing the larval body and producing torsion.  In this theory, the condition, with its presumed benefits, produced a new evolutionary line leading to present-day gastropods.  However, several scientists have questioned the role of the retractor muscles in torsion.  

In the study considered here, antibiotics employed to control bacterial infection during embryonic culture of keyhole limpets Diodora aspera and trochid snails Calliostoma ligatum are found to interfere with the attachment of the retractor muscles to the inner wall of the larval shell, yet torsion still occurs. Such observations, and others, place into question the fundamental tenents of Garstang’s theory regarding the larval function of torsion.  For information on torsion in other gastropods, including the caenogastropods Amphissa columbiana and Euspira lewisii see Bondar & Page 2003 Invert Biol 122: 28.

Research Study 4: Larval defenses

Snail Margarites pupillus (formerly Pupillaria pupillus).

In adddition to the retractor-muscle issue, other studies cast doubt on Garstang’s hypothesis.  For example, torsion in the west-coast species Margarites pupillus could not be caused by contraction of the retractor muscles because the larval shell is not fully calcified at this time and could not hold up to the stress.

Research Study 5: Larval defenses

ea-hare Aplysia punctata veligers showing loose fastening of mantle fold in the veliger larvae.

Note in the drawings that on withdrawal into the shell, the mantle fold "slips" down, making room for the velum and foot. The implication of this is that this space would be available for the larva to withdraw its “fragile” head/velum into regardless of whether torsion happened or not; thus, according to this author, the position and volume of the mantle cavity is irrelevant. Further, on microscopic examination the head and velum appear no more “fragile” than the foot; thus, there is no need to invoke the “special” protective strategy conferred by torsion.  The observations in these and other Research studies question several basic tenents of Garstang’s theory.  None of these criticisms by themself is enough to discount Garstang’s theory, but together they cast a sense of “reasonable doubt”.  

NOTE Garstang's idea of a sudden macromutation leading to torsion and a new evolutionary line is also criticised (for a consideration of this idea and a review of older literature see Ghiselin 1966 Evolution 20: 337). At least one author agrees that torsion could have originated as a single mutation or “macromutation” leading to a major evolutionary advance, namely, Goodhart 1987 J Moll Stud 53: 33)

Research Study 6: Larval defenses

Consumption of pre-tort and torted veliger lavae of abalone Haliotis kamtschatka by several different planktonic predators.

What about a test of the hypothesis?  The first and possibly only test¹ of Garstang’s larval-benefit hypothesis, at Friday Harbor Laboratories, Washington, assesses rates of predation by 7 planktonic predators from 4 phyla on pre-torted and torted veliger larvae of abalone Haliotis kamtschatkana.  The torted larvae at this time are only 90^o twisted, but can fully retract² and seal the shell aperture with the operculum, and are similar in size and swimming ability to the pre-torted larvae.  The null hypothesis in the experiment is that there will be no difference in numbers of pre-torted and torted veligers eaten by the predators.  The predators include megalops larvae (decapod crustacean), copepods, hydromedusae3, ctenophorans, and juvenile pink salmon.  Results show that all but one predator (a ctenophore species) eat significant numbers of Haliotis larvae.  Only two predator species, however, eat significantly more of one veliger type or another.  Megalopae eat more torted larvae and one species of medusa eats significantly more pre-torted larvae. The authors conclude that torsion in Haliotis does not function defensively⁴ and that other selective pressures have maintained the trait.  

NOTE¹  tests are run in 1-liter jars with 50 veligers and one predator except for: megalopae (5 individuals), copepods (5 individuals), and salmon (2 individuals) over a 15h period.  Each combination is replicated five times.  “Number eaten” is corrected for veliger losses in control jars (without predators).  Two runs are done, one with pre-torted veligers and one with torted veligers.  The authors culture the larvae of Haliotis kamstschatkana to a 48h stage (pre-torted) and 120h stage (torted).  Although not specifically mentioned in the study, it is presumed that predators are not re-used, thus avoiding possible learning (dietary conditioning) effects

NOTE²  many (or most) species cannot fully withdraw into the larval shell until torsion is completed 

NOTE³  the authors test 2 species of medusae but, as one species ate so few of either type of larvae, the data are not included here

NOTE⁴  one guesses that not all researchers will support the authors’ conclusion.  At least one scientist criticises the choice of abalone larvae in the experiments, based on the fact that Haliotis is one of only a few gastropods with a free-living pre-torsional larva (most undergo torsion before hatching).   Also the generally “inconclusive” results obtained in the experiments (only two predators are recorded as eating significantly more of one type or another of the larvae...see red asterisks in the histograms) are open to criticism

Research Study 7: Larval defenses

As noted above, there are other objections to the larval-benefit theory and other ideas regarding torsion, but only the single experimental test.  The authors of the Haliotis study acknowledge the possibility that torsion may protect veligers from adverse physical conditions, but do not explain.  One such example may relate to the behaviour of swimming veligers that have undergone torsion.  When the larvae bump into something, they immediately withdraw into their shells and sink down.  Even the boundary layer of freshwater overlying seawater in a test-tube causes this response – either acting as a physical or chemical obstruction, or both.  So, even though torsion may not protect veligers from predators, it may protect them from surface haloclines or similarly averse chemicals.  

NOTE  in fact, this behaviour forms the basis for Garstang’s theory, and is eloquently described in the first verse of his delightful poem, The ballad of Veliger, or how the gastropod got its twist (Garstang 1962 p. 36 In, Larval Forms with other zoological verses Basil Blackwell, Oxford; see Research Study 9 below for more on Garstang and his poetry) :

    Veliger’s a lively tar, the liveliest afloat,
    A whirling wheel on either side propels his little boat;
    But when the danger signal warns his bustling submarine,
    He stops the engine, shuts the port, and drops below unseen. 

NOTE  this is easily set up by gently pouring freshwater into a test-tube containing swimming veligers of any kind in seawater, and observing the behaviour of the veligers under a stereomicroscope.  For greater contrast the freshwater can be coloured with a vital dye such as methylene blue 

Research Study 8: Larval defenses

Turbinid snail Pomaulax gibberosa with symbiotic worm.

A feature that seems to be ignored in this veliger/torsion research, or at least not given the attention that it deserves, is the operculum.  It appears in post-torsional larvae and, while perhaps not so important (it seems) for survival of the veliger stage, is of critical importance for survival of juvenile and adult stages.  The shell and operculum are arguably the two most important morphological features enabling colonisation of intertidal and land habitats by gastropod molluscs. 

Research Study 9: Larval defenses

Walter Garstang 1868-1949.

Book of poetry "Larval forms and other zoological verses" by Walter Garstang 1962.

In addition to being knowledgeable about marine-invertebrate larvae and fervently interested in the role of larvae in evolution of invertebrates, Walter Garstang had a delightful knack of presenting his ideas, and some quite serious ones at that, in the form of light-hearted verse.  These are collected in a book of poetry, published in 1962.  In addition to the perennial favourite “The ballad of Veliger...”, are the equally enjoyable and evolutionarily provocative poems "The amphiblastula and the origin of sponges", "The invaginate gastrula and the planula","Mülleria and the ctenophore", "Tornaria’s water-works",and many others.  Because the book is several decades out of print and may not be readily available, the poem most germane to this section of the ODYSSEY is presented in full, with identical spelling to the original:

The ballad of Veliger, or how the gastropod got its twist:

Veliger's a lively tar, the liveliest afloat,
A whirling wheel on either side propels his little boat;
But when the danger signal warns his bustling submarine,
He stops the engine, shuts the port, and drops below unseen.

He's witnessed several changes in pelagic motor-craft;
The first he sailed was just a tub, with a tiny cabin aft.
An Archi-mollusk fashioned it, according to his kind,
He'd always stowed his gills and things in a mantle-sac behind.

Young Archi-mollusks went to sea with nothing but a velum -
A sort of autocycling hoop, instead of pram - to wheel 'em;
And, spinning round, they one by one acquired parental features,
A shell above, a foot below - the queerest little creatures.

But when by chance they brushed against their neighbours in the briny,
Coelenterates with stinging threads and Arthropods so spiny,
By one weak spot betrayed, alas, they fell an easy prey -
Their soft preoral lobes in front could not be tucked away!

Their feet, you see, amidships, next the cuddy-hole abaft,
Drew in at once, and left their heads exposed to every shaft.
So Archi-mollusks dwindled, and the race was sinking fast,
When by the merest accident salvation came at last.

A fleet of fry turned out one day, eventful in the sequel,
Whose left and right retractors on the two sides were unequal:
Their starboard halliards fixed astern alone supplied the head,
While those set aport were spreadabeam and served the back instead.

Predaceous foes, still drifting by in numbers unabated,
Were baffled now by tactics which their dining plans frustrated.
Their prey upon alarm collapsed, but promptly turned about,
With the tender morsal safe within and the horny foot without!

This manoeuvre (vide Lamarck) speeded up with repetition,
Until the parts affected gained a rhythmical condition,
And torsion, needing now no more a stimulating stab,
Will take its predetermined course in a watchglass in the lab.

In this way, then, Veliger, triumphantly askew,
Acquired his cabin for'ard, holding all his sailing crew -
A Trochosphere in armour cased, with a foot to work the hatch,
And double screws to drive ahead with smartness and despatch.

But when the first new Veligers came home again to shore,
And settled down as Gastropods with mantle-sac afore,
The Archi-mollusk sought a cleft his shame and grief to hide,
Crunched horribly his horny teeth, gave up the ghost, and died. 
                                                  - Walter Garstang 1928

Summary comment: 

Although torsion may seem more suited as a topic for philosophical discussions in turn-of-the-century drawing rooms, it is actually one of the more dynamic and interesting controversies in marine-invertebrate study. A dialogue of opinion and argument has been on-going for 80 years! Students interested in such things (and in torsion) should additionally read the references cited in Pennington & Chia (1985)  and Page (2002)