5 Sex and the Single Snail
Friedrich Christian Lesser, a German clergyman whose hobby was to observe snails, gave us one of the earliest descriptions of two land snails mating and laying eggs. In his treatise Testaceo Theologica, published in 1744, Lesser was at pains to link his observations to his Christian faith. The act of sexual union was portrayed as an example of God’s greatness and ingenuity that extended even to the lowliest of his creations, snails.1 As for that union resulting in new offspring, Lesser must have felt conflicted since the accepted teaching, approved by the Church, followed Aristotle in believing that ‘lesser animals’, like snails, were spontaneously generated. Little did he realize that the encounter he had witnessed was not between a male and female, but between two hermaphrodites.
The word ‘hermaphrodite’ comes from the name of the Greek god Hemaphroditos, an androgynous being, product of the union between Hermes and the goddess of love, Aphrodite. It is applied to those creatures that have both male and female sex organs together in the same body, the situation in the majority of land snails. Gypsies believed that a land snail, because it was capable of ‘mutually giving and taking pleasure’, could be used as a charm against witchcraft. Some believed that a girl could win ‘illicit love’ by persuading someone of the opposite sex to carry a snail shell about his person, one that had been treasured by the girl. Indeed, to present a snail shell was to make a direct and not so subtle declaration of love.2
Hermaphroditism has a lot to commend it as a means of passing on genetic material, particularly when encounters between animals of the same species are potentially infrequent. The chance of an encounter producing any offspring is increased by the mutual exchange of sperm and this is exactly the situation amongst most land snails. Oliver Goldsmith in his History of the Earth and Animated Nature (1810) puts it nicely: ‘Every [land] snail is at once male and female; and while it impregnates another, is itself impregnated in turn.’3 Land snails, as well as being hermaphrodite, are also promiscuous, mating with different partners in the course of a reproductive season. Since fertilization involves just one sperm and one egg and since snails store sperm from their different sexual encounters, it is reasonable to suppose that a selection process is at work in which sperm from one animal is favoured over sperm from another. To understand this it is useful to go into more detail about how land snails mate. The most studied example is the common garden snail, Helix aspersa.
The two penises seem impossibly twisted in this early picture of two snails mating from Swammerdam’s Biblia Naturae.
A gentle showering of darts is seen here as a precursor to mating in snails.
Two snails, having made contact, line up head to head with their mouths and tentacles touching. They execute slight sideways movements of their heads. The common genital opening lies on the right side, behind the head of each animal. Out of this is protruded the genitalia, followed by a deliberate head movement to the right in both animals so that the mouth of one snail comes into contact with the genitalia of the other. The animals then go through a ritual in which they bite one other, resulting in a sharp withdrawal followed by a slower resumption of courtship. This foreplay can go on for an hour or more. Next, each snail approximates its genitals to the genitals of its partner and, at this point, something really bizarre happens. A dart, or telum amoris (literally, ‘weapon of love’), equipped with four blades, is forcibly ejected from one snail into the body of the other. It can hit the recipient on the head, in the genital area or on the foot with sufficient force to penetrate the skin to such a depth that it remains lodged there and visible to the human eye. Within half an hour of the snail’s first dart being shot, another dart is shot out, this time from the snail’s mate. This is a cue for the exchange of sperm to begin. Each snail inserts its penis into its partner’s female tract, a process that can be repeated many times.4 This ritualistic reproductive behaviour is puzzling. Is it part of species recognition? Is it a way of stimulating each snail to engage in sex, or does it have some other function? It is a question that has exercised biologists for a long time.
Henry Gerbault, La Colimaconne or Snail Lady – a hybrid animal. |
Ronald Chase, Professor of Biology at McGill University in Canada, has come up with a neat answer. His explanation involves sexual competition. Chase and his colleagues found that a snail that succeeds in lodging darts in its mate has a much greater chance of fathering offspring than one that does not, irrespective of which one has mated first. The successful dart shooter influences the recipient into choosing their sperm rather than sperm from other matings which are stored ready for fertilizing the eggs. In effect the dart shooting is a sexual competition determining which sperm will be used.
Subsequent work has demonstrated that the love dart is a hypodermic device that injects a chemical that selectively inhibits the digestion of the sperm that has just been introduced by the successful darter, increasing the chance that his sperm, rather than any other snail’s, will fertilize the eggs.5
The hollow nature of each dart can be seen from these photographs from different species of snail. |
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Sperm can be stored for several months in the recipient snail but it is the snail with the effective love dart whose sperm ultimately fertilize the eggs. Love darts vary according to the species of land snail. While only a minority of land snails use darts, multiple mating is common. It is conceivable that the snails without darts use other methods to achieve the same result, competition being the rule in sexual encounters between animals. Steve Jones speaks of the struggle in passing on genetic material:
Sex is a market place for natural selection. As a merger between genetic enterprises it is, like any other business with two partners, liable to discord. To find a mate, fight off the opposition, suffer sexual congress and pregnancy, and raise a brood, are all expensive and dangerous. Each involves subtle differences in the share-dealing strategy of the parties involved. Sometimes there is sexual war that may lead to traits that seem opposed to the interests of those who bear them. They are a reminder that the biological battle goes much further than the search for food or for light; there is, in addition, an unavoidable struggle to pass on genes.6
Passing on one’s genetic material is not secured simply by fertilization but, in addition, by anything that improves the chances of the offspring’s survival. They, after all, are the carriers of the genetic material. Newly fertilized eggs released into the world are in immediate danger of being eaten or of being killed by unfavourable local conditions. Without a mother to protect them, the future of fertilized snail eggs is precarious. Land snails usually coat their eggs in a protective layer of albumin before laying them in a hole in the soil, in a suitable hidden spot beneath a stone, on a piece of wood or among vegetation. Tree-living snails use the axils of branches or leaves as suitable places to deposit their eggs, and occasionally go further and glue them on to vegetation. Even then their future is uncertain.
However, not all snails abandon their eggs once laid. Amongst the ‘endodontoid’ snails living in the Pacific Ocean are some that carefully place their eggs in the umbilicus of the parent shell – that central hole created by the spiral of the shell – then cover the opening with a temporary, protective plate. In this ‘brood chamber’ the young grow and in time, with total disregard for their parent’s home, chew their way out through the parental shell. The river snail Viviparus viviparus, which so excited Swammerdam, actually carries its eggs inside it until they are mature enough to cope with an independent existence. As a strategy this is uncommon, but occasionally happens in a few species of land snail when environmental conditions are unfavourable.
Young sea snails have to cope with additional dangers to those of land snails since many of them go through an intermediate or larval phase in their development. Ocean currents carry the larvae, so widely distributing them. They have ready access to food in the form of floating plant plankton. They, in turn, are readily eaten by predatory small fish. The first larva to appear is a ‘trochophore’, shaped like a spinning top with a band of beating hairs around its waist and a tuft at its apex. It bears a close resemblance to the larva of certain segmented worms and provides evidence that snails and annelid worms are close in evolutionary terms. Next, the ‘trochophore’ develops into a ‘veliger’, described in the poem by Walter Garstang reproduced in the Appendix.7
In contrast, land and freshwater snails go through the whole of their development inside the egg. In this respect they resemble several species of sea snails where a free-swimming larval stage no longer occurs. The received wisdom used to be that, once lost during the process of evolution, the larval stage could not be re-acquired. However, as with shell-coiling, this is now known to be incorrect. Rachel Collin, at the Smithsonian Institute, has shown that in the group of sea snails called Crepipatella the motile, feeding larva was lost as a developmental stage, only to re-emerge later in the snail’s evolutionary history. This re-emergence is fundamentally important, as Collin explains, since ‘it shows that animals may carry the potential for evolutionary change around with them. When the environment changes, new life forms may be able to regain abilities that were lost earlier in evolutionary history.’8
In land snails we have seen how the use of love darts is part of competition between sperm after multiple mating. Before mating, so long as the snails are of the same species and coiled in the same way, no competition exists. Among sea snails, where male and female snails are distinct, competition occurs between the male sperm. Two strategies exist among them when it comes to producing offspring. In the first, the male sheds numerous sperm into the sea in the hope that some will find suitable eggs to fertilize. In some cases sperm is discharged to coincide with the release of eggs from the female. In the second, the male snail engages in internal fertilization with a female snail, placing sperm in direct proximity to the female’s eggs. Whatever the parental strategy, sperm from one sea snail compete with sperm from others for the privilege of fertilizing a female’s eggs. Even when placed inside a willing recipient, fertilization is not guaranteed, since sperm from previous sexual encounters may already be there, and only one sperm can complete the job.
When not using its flotation raft of bubbles, lanthina, a sea snail, clings to floating jellyfish. It can secrete a purple dye that imparts a colour to the shell. |
The majority of hermaphrodite land snails mate with another individual, but occasionally, in a few species, self-fertilization can occur. ‘Selfing’, as it is known, is a last resort when, perhaps due to population decline, the chances of meeting a mate are reduced. Sex with another snail is abandoned altogether. As a result of this ‘selfing’ genetic diversity in the offspring is reduced and hence the ability to respond to changing circumstances. However, ‘selfing’ increases the ability of a species to colonize a favourable area when its population density is low.
So far we have discussed hermaphrodites of the simultaneous sort where a single organism has both male and female organs working at the same time. However, some species of snail show a different type of hermaphroditism, consecutive hermaphroditism, where the sex of the animal changes during the lifetime of the snail. An example of this is the slipper limpet Crepidula fornicata, which changes gender during the course of its life. This sea snail stays fixed in one place, either attached to rocks or, more commonly, to other limpets forming a chain of five or six individuals. Together the limpets feed on the plankton that drifts past in the water. At the bottom of the chain, often clinging to an empty shell, is the oldest member, while the youngest and smallest sits at the top. The chain is a more or less permanent structure, with the male members being the youngest, and the females the oldest. In between are individuals who are in the process of changing sex from male to female. The males copulate with the females below until their male organs atrophy. For a time, they assume an inter-sex phase, finally ending up as females.
On each side of a pebble, a chain of slipper limpets has formed.
Crepidula’s shell has a pronounced shelf and resembles a slipper; hence its name, ‘slipper limpet’.
An example of the extraordinary reproductive apparatus of slugs, from Martin Lister’s 1685 De Cochleis, tam Terrestribus, quam Fluviatilibus, Exoticis . . . |
Sex poses problems for the single snail and its offspring every bit as complex as for our own species. Why have sex at all, one might reasonably ask? For slugs, which are also hermaphrodites, sex with other slugs, according to Steve Jones, stops at Preston. Cold places, he argues, aren’t conducive to sexual union: ‘Faced with the predictable enemies of frost and starvation, it is better to evolve a single set of hardy genes that are never broken up by admixture with others.’9 So the northern slug is an identical replica of its parent, no mate is required and clones can be produced so long as the hermaphroditic animal can self-fertilize.
It’s certainly more straightforward when sex isn’t involved, but less interesting too! Consider the ever-more complex and bizarre mating patterns in slugs that do mate with other slugs. ‘Limacid’ slugs mate suspended by a mucus thread, their long penises intertwining, while the banana slug Ariolimax dolichophallus occasionally bites off the penis of its mate after copulating.
Sex in snails and slugs is certainly a complicated matter. We have hermaphrodites, snails of definite sex and even ones whose sex is in an intermediate phase. We have snails that pass on genetic material by mating and cross-fertilization and others that do without mating and self-propagate. And when the new life is produced, we have snails that undergo a larval phase that is absent in the development of other snails. What remains sure in every case is there is no hiding place from conflict and competition. When Friedrich Lesser stumbled into a conflict of ideas when it came to explaining what he saw in the natural world, he also mirrored a different conflict, that between individuals of the same species struggling to pass on their genes.