The snail's love-dart delivers mucus to increase paternity

Abstract

Many of the seemingly bizarre animal behaviours can be understood only by acknowledging the power of sex to shape evolution. A case in point is the so-called love-dart that some terrestrial molluscs shoot at their prospective sexual partners. Given that the likelihood of copulation is not different after solid hits than after complete misses, why do these suitors act so violently towards their chosen mates? Previously, it was shown that successful dart shooting enhances paternity. We conducted an experiment to determine whether the dart achieves its effect by a purely mechanical action or by transferring a bioactive substance. We found that injections of mucus from a gland associated with the dart more than doubled paternity relative to injections of saline. These results support the hypothesis that the dart transfers a substance capable of reconfiguring the spermatophore-receiving organs. While dart shooting probably evolved as the result of sperm competition, a role for cryptic female choice cannot be excluded. Our results imply that if cryptic female choice is operating in this system, it is likely to be based on the properties of the mucus and not on properties of the dart itself. Since we also found evidence of early-male sperm precedence, we conclude that snails can optimize their reproductive success by mating with virgins and shooting their darts accurately.

Figure 1

Two snails, Cantareus aspersus, in reciprocal copulation. During courtship, the snail at the top of the photograph shot a dart through the head of the snail at the bottom (pointed white object at left).

Figure 2

Paternity assignments per egg clutch from an experiment in which needle injections replaced dart shooting. Future mothers were mated twice. In one mating, sperm transfer was accompanied by an injection of mucus from the dart gland and in the other mating sperm transfer was accompanied by an injection of saline. Mean+s.e.m. is shown. First donor: F_1,35=5.086, p=0.030; second donor: F_1,36=10.652, p=0.002.

Figure 3

Early-male sperm precedence. Outside fathers mated with a mother prior to the collection of snails for this study. Subsequently, the same mother mated with two genotyped sperm donors as part of our experiment. Because the snails were held in isolation prior to the start of the experiment, the sperm of outside donors had already been stored for at least 61.5±17.6 days at the time of the first experimental mating. Mean+s.e.m. is shown.