Love Darts Research Articles

Sexual inactivation induced by the mucus that covers land snail love darts: sexual selection and evolution of allohormones in hermaphrodites.

The transfer of male accessory gland secretions is a well-investigated reproductive strategy for winning in sexual selection. An example of such a strategy is the conspicuous mating behaviour of simultaneously hermaphroditic land snails, the so-called shooting of love darts, whereby a snail drives a love dart(s) into the body of its mating partner. In the land snail Euhadra quaesita, it has been shown that a specific mucus which coats the love dart is transferred into the partner's haemolymph and that it suppresses subsequent matings in the darted individual. However, how the mucus of the love dart suppresses rematings remains unclear. In the present study, we tested the hypothesis that by injection of the dart mucus, love-dart shooters manipulate the physiology of a dart recipient and make the individual sexually inactive. In an experiment in which snails were provided with opportunities to encounter a potential mating partner, we found that the latency period to achieve sexual arousal was longer in snails injected with the dart mucus than in snails of the control treatments. This finding indicates that the dart mucus delays sexual arousal in injected snails. This delay in arousal is a novel example of the effects of the mucus in simultaneously hermaphroditic land snails. The remating suppression effect of the dart mucus is likely to occur through sexual inactivation.

Insights into the Evolution of Shells and Love Darts of Land Snails Revealed from Their Matrix Proteins.

Over the past decade, many skeletal matrix proteins that are possibly related to calcification have been reported in various calcifying animals. Molluscs are among the most diverse calcifying animals and some gastropods have adapted to terrestrial ecological niches. Although many shell matrix proteins (SMPs) have already been reported in molluscs, most reports have focused on marine molluscs, and the SMPs of terrestrial snails remain unclear. In addition, some terrestrial stylommatophoran snails have evolved an additional unique calcified character, called a “love dart,” used for mating behavior. We identified 54 SMPs in the terrestrial snail Euhadra quaesita, and found that they contain specific domains that are widely conserved in molluscan SMPs. However, our results also suggest that some of them possibly have evolved independently by domain shuffling, domain recruitment, or gene co-option. We then identified four dart matrix proteins, and found that two of them are the same proteins as those identified as SMPs. Our results suggest that some dart matrix proteins possibly have evolved by independent gene co-option from SMPs during dart evolution events. These results provide a new perspective on the evolution of SMPs and “love darts” in land snails.

Terrestrial gastropods - how do they reproduce?

Molluscs are the most diverse group in respect of sexual systems and strategies. They can be dioecious with separate sexes or hermaphroditic. Within hermaphroditism, it is possible to distinguish a number of modifications of this type of reproduction, such as protandry, protogyny, sex reversal, or protandry with some overlap. It is thought that dioecy was ancestral because it occurs in most classes of molluscs. Hermaphroditism evolved independently several times, and sequential and simultaneous hermaphroditism are more closely related to each other than to dioecy. This publication presents a general review of sexual systems and strategies in terrestrial gastropods with special emphasis on mating, fertilization, presence of love darts, reproductive strategies (semelparity vs. iteroparity) and modes (oviparity, ovoviviparity, viviparity), production of eggs and egg cannibalism.

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

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.

Love dart goo gives snail sperm a head start

For simultaneous hermaphrodites – equipped with both male and female reproductive organs – reproduction is more complex than the conventional ‘boy meets girl’ story. For a start, each protagonist can fertilize the eggs of the other. Common garden snails, Cornu aspersum, seem to improve their chances of becoming fathers – and this might not sound terribly romantic – by spearing their partner with a so-called ‘love dart’, smeared in mucus. Once in the partner's blood stream, the mucus improves the chances of the biological father's sperm successfully fertilising their partner's eggs by closing off the entrance to a structure that digests unused sperm and causing the sperm to be pumped into a storage organ for later use. But it wasn't clear whether this pragmatic approach to reproduction was peculiar to the common garden snail or whether other species also took advantage of the love dart's benefits. To remedy the situation, Kazuki Kimura and Satoshi Chiba from Tohoku University, Japan, working with Joris Koene from Vrije University, The Netherlands, investigated another species equipped with love darts, the distantly related Japanese Euhadra peliomphala snail, to find out whether the love dart mucus that they inject into their partners also provides a fertility advantage (p. 1150).Having collected snails from a nearby local park, the team extracted the glands that produce the love dart mucus from some of the animals and produced a mucus gland extract to test on the remaining snails. They then simulated the love dart stabbing action of an ardent snail with a syringe needle coated in the extract before injecting a minute volume of coloured water that mimicked semen into the snail's genital tract to find out whether the mucus gland extract altered the fluid's fate.The team tested whether any of the fluid made it into the organ that digests sperm and they found that it was closed in the snails that had been injected with the mucus gland extract. In a real-life situation, the mucus would have saved the semen from destruction, and Kimura and colleagues say, ‘This indicates that in various dart-bearing species the mucus from the dart glands targets the same organ’.So, having added another species to the list of simultaneous hermaphrodite snails that improve their chances of becoming fathers through the use of love dart mucus, Kimura and colleagues wonder whether these hermaphrodites benefit from sexual selection. ‘Because of the relatively limited literature on sexual selection in hermaphrodites, it was unclear how important sexual selection has been for the evolution of their reproductive behaviours’, they say. However, the fact that love dart mucus targets the same organ in distantly related snails suggests that simultaneous hermaphrodites do benefit from sexual selection. The team adds, ‘This result supports the idea that this conspicuous reproductive trait of land snails had evolved through a conflict over sperm digestion between sperm donors and recipients’.

Common effect of the mucus transferred during mating in two dart-shooting snail species from different families

Several taxa of pulmonate land snails exhibit a conspicuous mating behaviour, the shooting of so-called love darts. During mating, such land snail species stab a mating partner with a mucus-coated dart. It has previously been shown that the sperm donor physiologically influences the sperm recipient via the mucus covering the dart and thereby decreases the number of sperm digested by the recipient. However, the generality of this effect of the dart's mucus is unclear, because almost all the previous studies on the effect of the mucus used the brown garden snail Cornu aspersum from the family Helicidae. Therefore, the relationship between the acquisition of the mucus effect on the recipient and the evolution of the dart itself, and its mucus, is still open to debate. To test the commonality of the physiological effect of the dart mucus, we examined this in Euhadra peliomphala, a species from the Bradybaenidae family, and compared our findings with the results of previous work using C. aspersum. Our experiments showed that in E. peliomphala, the dart mucus had a physiological effect and lowered the accessibility of the gametolytic organ, as found in C. aspersum. This indicates that in various dart-bearing species the mucus from the dart glands targets the same organ and that the inhibition of sperm digestion has played a crucial role in the evolution of the dart and its mucus.

Blindness and Therapy in Late Medieval French and Italian Poetry by Julie Singer

writing, or the connection between description, visual evidence, and painting. Here Schöch covers eighteenth-century theories of language in Condillac, Rousseau, and others, ultimately showing that painting is a model for descriptive writing. Passages of the type described in the second section represent only one aspect of descriptive writing in this period. An entire esthétique picturale begins to emerge at the narrative level in the novels of this period:“Cet enjeu concerne l’ensemble de l’écriture descriptive , passages descriptifs inclus, mais tout particulièrement la modalité de l’écriture descriptive que j’ai choisi de désigner comme le discours descriptif” (214). As this study demonstrates, we should not consider description or narration as abstract, transhistorical practices, but rather view them within specific historical frameworks. This typology of novels will certainly form a useful basis for comparison with other novels of the period, or with descriptive practices in other periods. Boston University Gillian B. Pierce Singer, Julie. Blindness and Therapy in Late Medieval French and Italian Poetry. Cambridge: Brewer, 2011. ISBN 978-1-84384-272-9. Pp. 238. $99. Situated at the junction of medieval studies and disability studies, Singer’s book combines literary analysis and cultural history to offer an insightful examination of the interaction between rhetoric and medicine in fourteenth- and fifteenth-century French and Italian poetry. Singer focuses on the role of eyesight and blindness in love at a time when lyric explored—and at times, challenged—medical concepts. After presenting her project, Singer turns to the overlap of medical and poetic discourses in the love-imprint. She discusses the evolving view of the eye, which became an active participant in creating love, and demonstrates that the eyes served as a site of sex difference, with love darts or rays emanating from women’s eyes and being received by men’s.Anti-medical discourse is at the heart of the second chapter.While emphasizing Italian lyric, Singer explains that Petrarch’s justification of rhetoricians’ borrowing of medical language prepares the way for later French poets to treat blindness. The rest of the volume examines four rhetorical strategies: irony, metaphor, metonymy, and synecdoche, each analyzed in a separate chapter. Singer places irony in the context of the humors and restoring balance through contraries. She defines medieval irony and outlines two main models before focusing on works by Petrarch and Jacques Bauchant. The use of medical metaphor, particularly in Machaut’s Remede de Fortune, reveals that verse may distract from pain and that form can offer a cure: Singer provides a fascinating investigation of the reflection of the narrator’s lovesickness in the fixedform poems, arguing that the lover can ultimately heal himself. Singer also considers metaphor in Christine de Pizan’s Avision Christine,Alain Chartier’s Livre de l’Espérance, and the work of Gilles le Muisit, a blind abbot. Form continues to play an important role in the chapter linking metonymy and prosthesis. Machaut’s Livre du Voir Dit takes 232 FRENCH REVIEW 87.4 Reviews 233 center stage, with Singer proposing that the lyric insertions compensate for lacks. She sees the use of ‘round’ fixed forms such as ballades, virelais, and rondeaux as supplementing the defective eye’s role in love. Ultimately, she concludes, the lyric prostheses fail because they stand out from the surrounding text instead of concealing their difference. Singer devotes her final chapter to synecdoche, concentrating on images of blindfold Fortune in French poetry. Studying works by Machaut, Charles d’Orléans, Villon, Martin Le Franc, and Pierre Michault, she uncovers the therapeutic potential of blindness itself. Singer’s work is a model of the interdisciplinarity that she sees in her texts,which intermingle poetic and medical language.There are rare inconsistencies (Michault’s title is given as both“Dance”and“Danse” aux aveugles), and occasionally, Singer provides more background information than necessary for her arguments whereas at other times—particularly for authors besides Petrarch and Machaut—I wished for greater detail. Moreover, the volume could explore further the issue of how ‘real’ the effects of rhetorical remedies are. Those minor quibbles notwithstanding, Singer’s innovative approach raises important questions about lyric’s power, inviting us to view blindness...

A syringe-like love dart injects male accessory gland products in a tropical hermaphrodite.

Sexual conflict shapes the evolution of many behaviours and processes involved in reproduction. Nearly all evidence supporting this comes from species where the sexes are separated. However, a substantial proportion of animals and most plants are hermaphroditic, and theoretical work predicts that sexual conflict plays an important role even when the sexes are joined within one individual. This seems to have resulted in bizarre mating systems, sophisticated sperm packaging and complex reproductive morphologies. By far the best-known example of such a strategy in hermaphrodites is the shooting of so-called love-darts in land snails. All known love darts carry a gland product on their outside and enter this into the partner’s hemolymph by stabbing. Here, we show that species of the snail genus Everettia possess a syringe-like dart that serves as a real injection needle. Their dart is round in cross-section, contains numerous channels, and has perforations along its side. Histology and electron microscopy show that these holes connect to the channels inside the dart and run all the way up to the elaborate mucus glands that are attached to the dart sac. This is the first report on a love dart that is used as a syringe to directly inject the gland product into the partner’s hemolymph. Although the exact use and function of this dart remains to be demonstrated, this clearly adds to the complexity of the evolution of reproductive strategies in hermaphrodites in general. Moreover, the perforations on the outside of the love dart resemble features of other injection devices, thus uncovering common design and repeated evolution of such features in animals.

Evolution of female sperm-storage organs in the carrefour of stylommatophoran gastropods

The presence of specialized female sperm-storage organs has been recognized as an important factor influencing postcopulatory sexual selection via sperm competition and cryptic female choice in internally fertilizing species. We morphologically examined the complexity of sperm-storage organs in the carrefour (spermatheca and fertilization pouch) in 47 species of stylommatophoran gastropods. We used partial 28S rDNA sequences to construct a molecular phylogeny, and applied maximum likelihood (ML) and Bayesian methods to investigate the history of spermatheca diversification and to test different hypotheses of sperm-storage organ evolution. The phylogenetic reconstruction supported several gains and losses of spermathecae. Moreover, a complex spermatheca was associated with the occurrence of love darts or other kinds of auxiliary copulatory organs, the presence of a long penial flagellum, and cross-fertilization as the predominant mating system. However, our results also suggest associations of carrefour complexity with body size, reproductive strategy (semelparity versus iteroparity), reproductive mode (oviparity versus ovoviviparity), and habitat type. Carrefour length in 17 snail species possessing a spermatheca was positively correlated with sperm length. Our results indicate that postcopulatory sexual selection as well as life history and habitat specificity may have influenced the evolution of female sperm-storage organs in hermaphroditic gastropods.

A review of mating behavior in slugs of the genus Deroceras (Pulmonata: Agriolimacidae)*

The genus Deroceras Rafinesque, 1820 (the largest genus of terrestrial slugs) shows a high diversity of penis morphologies and mating behaviors. The function of most of the appending external and internal penial structures, some of them truly bizarre, is largely unknown. This paper reviews mating behavior and reproduction, based on data on 16 species from the literature and from unpublished observations. I analyze patterns common to all Deroceras species and differences among species. The general mating pattern consists of a long courtship with mutual stroking with a sarcobelum, a sudden penis eversion, and external sperm exchange (copulation). I distinguish also precourtship and withdrawal phases. Sperm exchange is usually very quick but, in a few species, occupies a considerable proportion of the total mating duration. Mutual sperm exchange is the rule. Species differences involve the durations of certain mating phases, presence and nature of initial trail following, nature and intensity of stroking (including the degree of contact with the sarcobelum), aggressiveness of courtship behavior, and the timing of the penial gland eversion. I hypothesize that the radiation of mating behaviors and associated structures has been driven by an arms race resulting from conflicting interests of mating partners over sperm donation and use. This could also have increased the rate of speciation in Deroceras. There are indications of the presence of sperm competition and conflicting interests between mating partners: individuals mate repeatedly, can store and digest sperm, and simultaneously use sperm from different mating partners for fertilization. Some details of mating behavior also indicate conflict. The timing of the penial gland eversion after sperm exchange suggests a manipulation akin to the role of love darts in helicid snails. Finally, some recommendations for studying mating behavior in Deroceras are given.

Use of the dart apparatus by the hermaphroditic land snail Polymita muscarum (Lea, 1834)

AbstractMany species of pulmonate land snails are equipped with one or more so-called "love darts". Even though the number and shape of these calcareous darts vary considerably between species, dart use has only been investigated in very few species. Here, we redescribe the mating behaviour of Polymita muscarum because previous reports did not include the use of the dart apparatus. Mating in this hermaphroditic land snail can be divided into three stages: courtship, copulation and post-copulatory activity. During courtship, full eversion of the genital atrium is reached, thus exposing the sensitive zone, genital lobes and dart apparatus. We observed that P. muscarum pushes the everted dart apparatus repeatedly onto different parts of the partner's body and does not lose its dart after stabbing. Dissected specimens had a single, slender dart with a round base, a broad corona and a circular cross-section. We propose that the morphology of P. muscarum 's dart is consistent with the idea of simple darts needing to be stabbed more often in order to increase the transfer of mucus, which contains a biologically active substance (i.e. allohormone) that enhances the chances of paternity. Besides adding to the growing diversity in the use of love darts in land snails, these findings contribute to the understanding of the evolution of this peculiar reproductive act.

Hermaphroditism: What's not to like?

Hermaphroditism is rare and phylogenically in decline among animal species. The evolutionary basis for this development is not well understood. This paper focusses on self-incompatible simultaneous hermaphroditism in animals. It proposes that such hermaphroditism is not stable in sufficiently heterogeneous populations, suggesting a possible reason for why hermaphroditism is rare among evolved animal species. The argument turns on the Bateman principle, namely that male reproductive success (RS) is limited by partner availability, while female RS is not. We show that: low-quality individuals do better if female; secondary sexual differentiation may be important for understanding the existence of males; and that hermaphroditic mating is reciprocal. Reciprocity may be key to understanding promiscuity and attendant phenomena such as cryptic female choice, sperm competition and love darts—common features of hermaphroditic mating. We also argue that hermaphrodites are especially vulnerable to male violence, suggesting a reason for the rarity of trioecy. Finally, we propose that external fertilization, and the scope for streaking, may be one reason fish are the only simultaneously hermaphroditic vertebrates.

Tales of two snails: sexual selection and sexual conflict in Lymnaea stagnalis and Helix aspersa

Sexual selection and sexual conflict have been shown to play key roles in the evolution of species with separate sexes. Experimental evidence is accumulating that this is also true for simultaneous hermaphrodites. For example, many species of land snails forcefully stab their mating partners with love darts. In the brown garden snail (Helix aspersa, now called Cantareus asperses), this dart increases sperm storage and paternity, probably via the transfer of an allohormone that inhibits sperm digestion. A recent interspecies comparison of dart-possessing land snails revealed coevolution between darts and spermatophore-receiving organs that is consistent with counteradaptation against an allohormonal manipulation. The great pond snail (Lymnaea stagnalis) seems to use a seminal product to manipulate its partner and mates in the male role when enough seminal fluid is available in the prostate gland. Receipt of semen not only initiates egg laying in virgin animals, but also feminizes the mating partner later in life. These increases in the female function have been shown to go at the expense of growth and seminal fluid production of the sperm recipient. Although in Helix, and probably also Lymnaea, the sperm donor benefits from the induced changes through increased fertilization success, the sperm recipient may experience injury, imposed reallocation of resources, and altered sperm storage. These findings support the existence of sexual conflict in simultaneously hermaphroditic snails, and its importance for the evolution of mating behaviors and reproductive morphologies is discussed.

The darting game in snails and slugs

Love darts are hard 'needles' that many snails and slugs use to pierce their partner during mating. In a few species, darts have been shown to play a role in sperm competition. Two new papers, by Davison et al., and Koene and Schulenburg, might further pique researchers' interest, because they show how the full potential of darts can be tapped for studies of sexual selection in hermaphrodites.

Everything you always wanted to know about sexes.

Everything you always wanted to know about sexes.

A CRYSTALLOGRAPHIC STUDY OF THE LOVE DART (GYPSOBELUM) OF THE LAND SNAIL HELIX POMATIA (L.)

Love darts are formed in land snails and injected into the partner's body during the mating process. Darts of Helix pomatia (L.) were studied with synchrotron X-ray powder diffraction, X-ray absorption spectroscopy (Ca K-edge EXAFS), and scanning electron microscopy. The polycrystalline dart consists almost exclusively of non-orientated aragonite crystals (calcium carbonate) with isotropic domain sizes of c. 40-80 nm with a variation in size along the dart. The hollow central channel inside the dart is covered with elongated, μm-sized crystals, possibly single crystals. Very small amounts of an unknown crystalline phase were found.