The mucus of a land snail love-dart suppresses subsequent matings in darted individuals

Kimura, Kazuki; Shibuya, Kaito; Chiba, Satoshi

doi:10.1016/j.anbehav.2012.12.026

Cited by 24 publications

(32 citation statements)

References 28 publications

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“…Also, injections of mucous gland homogenate decreases courtship duration of sexually receptive snails, whereas gland homogenate increases the size of the recipient's genital eversion, and retards locomotion (39). In addition, the mucus appears to affect the sperm recipient in other ways, as demonstrated in the snail Euhadra quaesita, in which the mucus suppresses subsequent matings and promotes oviposition in their partners (40), suggesting that the LDA and/or other as yet uncharacterized peptides have other physiological functions. Similarly, seminal FIGURE 6.…”

Section: Discussionmentioning

confidence: 99%

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

Stewart

Wang

Koene

et al. 2016

Journal of Biological Chemistry

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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.

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Section: Discussionmentioning

confidence: 99%

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

Stewart

Wang

Koene

et al. 2016

Journal of Biological Chemistry

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“…Promoting shortterm egg laying in a mating partner, which is a well-known sperm competition strategy (e.g. [38,39]), can contribute to overcoming this potential fitness loss in dart shooters, although it is still unclear whether snails adopt such strategy [22,40]. This viewpoint of long-term fitness in shooter individuals needs to be examined in future research.…”

Section: Discussionmentioning

confidence: 99%

“…20 matings: K.K. 2012, unpublished data) as in C. aspersum [30] and E. quaesita [22]. However, virgin snails of this species perform this mating behaviour without shooting their dart.…”

Section: Materials and Methods (A) Study Speciesmentioning

confidence: 99%

“…Subsequent studies have found that either successful dart shooting or experimental injection of the dart mucus alone increased sperm storage and paternity of the sperm donor in C. aspersum [10,20,21]. Furthermore, a recent study has reported that the mucus decreases the likelihood of remating by darted individuals in Euhadra quaesita [22]. Therefore, dart shooting is considered to be a reproductive strategy for sperm competition.…”

Section: Introductionmentioning

confidence: 99%

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The direct cost of traumatic secretion transfer in hermaphroditic land snails: individuals stabbed with a love dart decrease lifetime fecundity

Kimura

Chiba

2015

Proc. R. Soc. B.

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Several taxa of simultaneously hermaphroditic land snails exhibit a conspicuous mating behaviour, the so-called shooting of love darts. During mating, such land snail species transfer a specific secretion by stabbing a mating partner's body with the love dart. It has been shown that sperm donors benefit from this traumatic secretion transfer, because the secretions manipulate the physiology of a sperm recipient and increase the donors' fertilization success. However, it is unclear whether reception of dart shooting is costly to the recipients. Therefore, the effect of sexual conflict and antagonistic arms races on the evolution of traumatic secretion transfer in land snails is still controversial. To examine this effect, we compared lifetime fecundity and longevity between the individuals that received and did not receive dart shooting from mating partners in Bradybaena pellucida. Our experiments showed that the dart-receiving snails suffered reduction in lifetime fecundity and longevity. These results suggest that the costly mating behaviour, dart shooting, generates conflict between sperm donors and recipients and that sexually antagonistic arms races have contributed to the diversification of the morphological and behavioural traits relevant to dart shooting. Our findings also support theories suggesting a violent escalation of sexual conflict in hermaphroditic animals.

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“…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, , ).…”

Section: Introductionmentioning

confidence: 99%

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

Lodi

Στάικου

Janssen

et al. 2017

Ecology and Evolution

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Postcopulatory adaptations that increase reproductive success compared to rivals, like the transfer of accessory gland products that promote paternity, are common when sperm competition occurs among males. In land snails, the dart shooting behavior and its adaptive significance, in promoting individual fitness through enhanced paternity of the successful dart shooter, have been considered such an adaptation. The fitness result gained is mediated by the transfer of mucus components on the love dart capable of altering the physiology of the receiver's reproductive tract. In this context, dart shooting and mucus transfer could be considered as processes targeted by sexual selection. While the effect of dart mucus is beneficial for the dart user, so far it has remained unknown whether its transport is greater when snails experience a higher level of sperm competition. Here, we report results of a study on inter‐ and intraspecific variations of dart and mucus gland morphometry, considered to be traits reflecting the ability of snails to adjust the production and transfer of mucus under varying sperm competition scenarios. We investigated four populations with different densities from four dart‐bearing species, Arianta arbustorum, Cepaea nemoralis, Cornu aspersum, and Helix lucorum. The results indicate that different adaptations of these traits occur among the studied species that all seem to achieve the same goal of transferring more mucus when sperm competition is higher. For example, the presence of longer and more branched mucous glands or an increase in dart surface most likely reflect increased mucus production and enhanced ability of mucus transport, respectively. Interestingly, the species for which the use of the dart is reported to be facultative, A. arbustorum, did not show any variation among the examined traits. To conclude, sexual selection in the form of sperm competition intensity seems to be an important selective force for these simultaneously hermaphroditic dart‐bearing snails, driving differences in sexual traits.

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The mucus of a land snail love-dart suppresses subsequent matings in darted individuals

Cited by 24 publications

References 28 publications

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

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

The direct cost of traumatic secretion transfer in hermaphroditic land snails: individuals stabbed with a love dart decrease lifetime fecundity

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

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