From 2015... The love-darts of simultaneous hermaphrodites like land snails seem to have evolved as a result of conflict over the fate of donated sperm

The love-darts of land snails: integrating physiology, morphology and behaviour. Monica Lodi, Joris M. Koene. Journal of Molluscan Studies, Volume 82, Issue 1, February 2016, Pages 1–10, August 25 2015. https://doi.org/10.1093/mollus/eyv046

Abstract: Several land-snail species of the helicoid and limacoid superfamilies possess one or more love-darts, which seem to have evolved as a result of conflict over the fate of donated sperm and/or as a way to select the most fit sperm donor. A love-dart is a calcareous stylet used during mating encounters to pierce the partner's body wall. When used, it carries accessory gland mucous products that influence the partner's physiology. Most of the knowledge on the effects of the glands' mucus derives from a single well-studied species, Cornu aspersum, in which the mucus increases the male reproductive success of the dart user. However, detailed descriptions on the use of the dart are limited to just a few other species. Hence, here we compare physiological, morphological and behavioural aspects concerning love-darts in several dart-bearing species. Patterns in the use of the dart are identified according to family and we discuss the coevolution of the morphology of the dart and anatomical traits of the reproductive system. The reported physiological effects caused by the dart's mucus suggest a common function of the dart in increasing male reproductive success. Nevertheless, caution is needed when generalizing the use and effects of the love-dart, which are predominantly based on one model organism.

CONCLUSION

The comparative approach taken here indicates that the common feature in dart shooting across families is the enhancement of male reproductive success by transferring mucus from the shooter to the recipient, inhibiting the destruction of received sperm. The precise mechanisms may be family-specific or conserved across families (e.g. Kimura et al., 2013; Kimura et al., 2014, respectively). In vivo and in vitro investigations in this direction have only just begun, but are already showing promising results by highlighting differences and commonalities with the well-studied species Cornu aspersum. In this respect, particular families of interest to be investigated are the Helminthoglyptidae and Hygromiidae and the superfamily Limacoidea, for which no information is available.

The relationship between the shape and size of the dart, its manner of use and other traits of reproductive anatomy show some consistent differences among families. While the patterns are all consistent with expectations based on sexual conflict (Koene & Schulenburg, 2005), the evolution of such coadaptations cannot yet be traced. The relationships between dart-bearing families are still unclear and thus the ancestral conditions cannot be determined. While there is an ontogenetic homology in the tissues forming the dart and its accompanying structures, darts as such might have evolved more than once as a strengthening of noninjurious, external hormonal secretions. More work on phylogeny is needed.

More behavioural observations on the use of the dart are also necessary, especially for those species with multiple love-darts (e.g. the helicoid Humboldtiana). The quantification of the costs of receiving a dart has only just begun (Kimura & Chiba, 2015) and needs to be done for different species; it would be desirable to measure any immune or stress response following dart receipt (e.g. resulting from any bacterial infection due to the wounding by the dart). In our opinion the most promising and fruitful direction of investigation among all the aspects reviewed here is the physiological response of the receiver induced by the mucus delivered with the dart. As suggested by recent results, the dart seems to cause physiological changes that favour male reproductive success in more species than just C. aspersum. A broader study in this direction should assess the function of the dart in multiple species. Not only complete mucus extracts, but also the recently discovered LDA peptide (responsible for one of the physiological changes in both C. aspersum and Theba pisana), could be used experimentally. This opens up a new area of study that can investigate the expression and similarity of LDA in different dart-bearing species. This will enable a comparison across families at the allohormone level and is expected to shed light on the evolution of such substances. Such analysis can be further expanded when the peptides and proteins in the mucus responsible for different responses are identified, such as for muscular contractions, mating inhibition and increased sperm storage or paternity. To broaden our understanding of love-darts, a comparative approach across superfamilies will provide more reliable general conclusions than can at present be drawn based mainly on studies of C. aspersum.