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

Abstract

Animals have evolved many ways to enhance their own reproductive success. One bizarre sexual ritual is the "love" dart shooting of helicid snails, which has courted many theories regarding its precise function. Acting as a hypodermic needle, the dart transfers an allohormone that increases paternity success. Its precise physiological mechanism of action within the recipient snail is to close off the entrance to the sperm digestion organ via a contraction of the copulatory canal, thereby delaying the digestion of most donated sperm. In this study, we used the common garden snail Cornu aspersum to identify the allohormone that is responsible for this physiological change in the female system of this simultaneous hermaphrodite. The love dart allohormone (LDA) was isolated from extracts derived from mucous glands that coat the dart before it is stabbed through the partner's body wall. We isolated LDA from extracts using bioassay-guided contractility measurement of the copulatory canal. LDA is encoded within a 235-amino acid precursor protein containing multiple cleavage sites that, when cleaved, releases multiple bioactive peptides. Synthetic LDA also stimulated copulatory canal contractility. Combined with our finding that the protein amino acid sequence resembles previously described molluscan buccalin precursors, this indicates that LDA is partially conserved in helicid snails and less in other molluscan species. In summary, our study provides the full identification of an allohormone that is hypodermically injected via a love dart. More importantly, our findings have important consequences for understanding reproductive biology and the evolution of alternative reproductive strategies.

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

“…Nevertheless, besides these morphological traits, other types of adaptations will also be relevant to investigate. Physiologically, for example, dart mucus composition could be altered to make the paternity enhancing effect more effective (e.g., new manipulative proteins or modification of the existing ones; Eberhard, ; Stewart et al., ). Consequently, it will now be extremely interesting to test whether mucus quality changes according to the level of sperm competition and whether it affects fertilization success.…”

Sex determination and gender expression: Reproductive investment in snails

“…Irrespective of whether or not a mucus component from other sources evokes a similar effect, this would only indicate that the active component is possibly also used in a different context than dart shooting—which is not unusual for accessory gland products (e.g., Yi and Gillott, ). The latter scenario is strengthened by the identification of the digitiform gland component that induces one of the muscular contractions in the spermatophore receiving organ: the active peptide turns out to resemble buccalin, a known modulator of which different forms are used to change muscle contractions in freshwater and marine molluscs (Stewart et al, ). 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 scenario is strengthened by the identification of the digitiform gland component that induces one of the muscular contractions in the spermatophore receiving organ: the active peptide turns out to resemble buccalin, a known modulator of which different forms are used to change muscle contractions in freshwater and marine molluscs (Stewart et al, ). 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, ,).…”

Polymorphism of a genital organ under sexual selection in Monacha kuznetsovi from the Caucasus (Gastropoda: Hygromiidae)

“…The latter hypothesis could be corroborated by experimental studies (Chase, ). It has been shown that the dart transfers an allohormone produced by the glands of the dart apparatus, the glandulae mucosae, into the body of the recipient (Stewart, Wang, Koene, Storey, & Cummins, ). This allohormone inhibits the intake of the spermatophore into a digesting organ so that more sperm can reach the sperm‐storing organ and fertilize eggs.…”