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.

Sex allocation and sexual conflict in simultaneously hermaphroditic animals

“…He thereby not only clarified the role of sperm competition (explored more deeply in Charnov 1996), but also recognized the importance of post-copulatory female choice (later termed cryptic female choice, Thornhill 1983), and the potential for sexual conflict and sexually antagonistic coevolution resulting from their interaction. Specifically, post-copulatory sexual selection often leads to sexual conflict (Parker 2006), because donors that have managed to transfer sperm to a recipient should be under strong selection to prevent the recipient from removing that sperm from the fertilization set (see also Koene & ter Maat 2001;Chase & Blanchard 2006).…”

A “Love” Dart Allohormone Identified in the Mucous Glands of Hermaphroditic Land Snails

“…C. aspersum was most appropriate for this study because it had represented the helicid model for defining whether the dart achieves its effect by a mechanical action or by transferring a bioactive substance; injections of C. aspersum mucus from the mucous gland more than doubled paternity relative to injections of saline (10). The use of C. aspersum did also provide us with a relatively large bursa duct that could readily facilitate the experimental hook-up of the T-junction of the copulatory canal (forks with the bursa tract diverticulum and bursa copulatrix) for contraction bioassay.…”

“…Helicid land snail copulation lasts 2-6 h and includes the unique use of calcareous (calcium carbonate) "love" darts that are pierced through the body wall of the mating partner during courtship (7)(8)(9)(10). The mating strategy often requires a precopulatory courtship with associated behaviors.…”

“…Research has implicated the mucus that coats these calcareous love darts as containing compounds that enhance paternity success; thus the love dart is used as a tool for increasing fertilization success of the shooter (10,(13)(14)(15)(16). Love darts are characteristic features of the reproductive tract for the hermaphrodite land snail families of Helicidae and Ariophantidae (12).…”

“…The physiological mechanism of action seems to be through reconfiguration of the spermatophore-receiving organ copulatory canal via peristaltic movements, which in turn increases the number of escaping spermatozoa (13). Because the love darts alone do not increase paternity success, the mucus is implicated as a carrier of the active substance(s) (10).…”