On the effect specificity of accessory gland products transferred by the love-dart of land snails

Abstract

BackgroundSexual selection favours the evolution of male bioactive substances transferred during mating to enhance male reproductive success by affecting female physiology. These effects are mainly well documented for separate-sexed species. In simultaneous hermaphrodites, one of the most peculiar examples of transfer of such substances is via stabbing a so-called love-dart in land snails. This calcareous stylet delivers mucous products produced by accessory glands into the mate’s haemolymph. In Cornu aspersum, this mucus temporarily causes two changes in the recipient. First, the spermatophore uptake into the spermatophore-receiving organ, called diverticulum, is probably favoured by contractions of this organ. Second, the amount of stored sperm increases by contractions of the copulatory canal, which close off the tract leading to the sperm digesting organ. However, it has yet to be determined whether these effects are similar across species, which would imply a common strategy of the dart in increasing male reproductive success.ResultsWe performed a cross-reactivity test to compare the in vitro response of the diverticulum and copulatory canal of C. aspersum (Helicidae) to its own and other species’ mucus (seven helicids and one bradybaenid). We found that the contractions in the diverticulum were only induced by dart mucus of certain species, while the copulatory canal responded equally to all but one species’ mucus tested. In addition, we report a newly-discovered effect causing the shortening of the diverticulum, which is also only caused by dart mucus of certain species. The advantage seems to be a distance reduction to the sperm storage organ.ConclusionsAll these findings are the first to shed light on the evolution of the different functions of accessory gland products in dart-bearing species. These functions may be achieved via common physiological changes caused by the substances contained in the dart mucus, since the responses evoked were similar across species’ mucus. Moreover, while these substances can act similarly in separate-sexed species as in simultaneous hermaphrodites, differences may occur in their evolution between the two sexual systems.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0672-6) contains supplementary material, which is available to authorized users.

High level of sperm competition may increase transfer of accessory gland products carried by the love dart of land snails

“…As a result, sexual selection pressure may either be weaker in this species or it might target other traits than the ones studied here (see Beese, Beier, & Baur, ). Incidentally, this is also in agreement with the recent finding that the effect of the dart mucus of A. arbustorum is not as strong as that of other helicids (Lodi & Koene, ) and a previous study indicating that it does not induce the same end result, that is snails hit by a dart did not store more sperm (Bojat & Haase, ).…”

“…Via these contractions, more sperm escape digestion and the dart user can roughly double its paternity (Chase & Blanchard, ). In other snail species, the dart mucus is also known to cause other effects, like delaying remating of the partner in the bradybaenid Euhadra quaesita (Kimura et al., ) and a temporary contraction that reduces the length of the diverticulum, probably to favor sperm storage, in the helicid Eobania vermiculata (Lodi & Koene, , ).…”

Sex determination and gender expression: Reproductive investment in snails

“…This particular peptide was named love‐dart allohormone (LDA), and is found in both C. aspersum and Theba pisana , the two species investigated by Stewart et al (). The latter agrees with recent work showing that the effects of dart mucus are evolutionarily conserved within a number of dart‐bearing species (Kimura et al, ; Lodi and Koene, ,).…”

“…The brown garden snail C. aspersum is the model species used for much of the work related to the transfer of accessory gland products via hypodermic injection in simultaneous hermaphrodites (Koene and Schulenburg, ; Lodi and Koene, ,). This species mates simultaneously reciprocally, with sperm packages (called spermatophores) being exchanged during a single mating interaction.…”

“…The study by Koene and Chase (; see also Lodi and Koene, ,) has so far been the only research to use control mucus extracts, reporting that mucus of the pedal gland (which produces the mucus trail) evoked a rather similar response. This indicates that the active substance is either a general constituent of mucus or that the two extracts cause a similar effect via different mechanisms.…”