{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T06:06:16Z","timestamp":1790834776793,"version":"4.1.0"},"reference-count":40,"publisher":"The Company of Biologists","issue":"4","license":[{"start":{"date-parts":[[2022,2,15]],"date-time":"2022-02-15T00:00:00Z","timestamp":1644883200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/www.biologists.com\/user-licence-1-1\/"}],"funder":[{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"crossref","award":["15H03743"],"award-info":[{"award-number":["15H03743"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2022,2,15]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n               <jats:p>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.<\/jats:p>","DOI":"10.1242\/jeb.238782","type":"journal-article","created":{"date-parts":[[2022,2,3]],"date-time":"2022-02-03T10:21:10Z","timestamp":1643883670000},"source":"Crossref","is-referenced-by-count":5,"title":["Sexual inactivation induced by the mucus that covers land snail love darts: sexual selection and evolution of allohormones in hermaphrodites"],"prefix":"10.1242","volume":"225","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0108-2285","authenticated-orcid":false,"given":"Kaito","family":"Shibuya","sequence":"first","affiliation":[{"name":"Department of Environmental Life Sciences, Graduate School of Life Sciences, Tohoku University, Kawauchi 41, Aoba-ku, Sendai 980-0862, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Satoshi","family":"Chiba","sequence":"additional","affiliation":[{"name":"Department of Environmental Life Sciences, Graduate School of Life Sciences, Tohoku University, Kawauchi 41, Aoba-ku, Sendai 980-0862, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1091-2313","authenticated-orcid":false,"given":"Kazuki","family":"Kimura","sequence":"additional","affiliation":[{"name":"Department of Environmental Life Sciences, Graduate School of Life Sciences, Tohoku University, Kawauchi 41, Aoba-ku, Sendai 980-0862, Japan"},{"name":"Department of Biology, Kyungpook National University, 80 Daehak-ro, Buk-gu, Daegu 41566, South Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"237","published-online":{"date-parts":[[2022,2,18]]},"reference":[{"key":"2022021808155251000_JEB238782C1","doi-asserted-by":"publisher","first-page":"1446","DOI":"10.1139\/z88-211","article-title":"Courtship and copulation in the terrestrial snail Helix aspersa","volume":"66","author":"Adamo","year":"1988","journal-title":"Can. J. Zool."},{"key":"2022021808155251000_JEB238782C2","doi-asserted-by":"publisher","first-page":"80","DOI":"10.1002\/jez.1402550111","article-title":"The \u201clove dart\u201d of the snail Helix aspersa injects A pheromone that decreases courtship duration","volume":"255","author":"Adamo","year":"1990","journal-title":"J. Exp. Zool."},{"key":"2022021808155251000_JEB238782C3","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/0163-1047(91)80123-V","article-title":"The interactions of courtship, feeding, and locomotion in the behavioral hierarchy of the snail Helix aspersa","volume":"55","author":"Adamo","year":"1991","journal-title":"Behav. Neural Biol."},{"key":"2022021808155251000_JEB238782C4","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1146\/annurev-ento-120709-144823","article-title":"Insect seminal fluid proteins: Identification and function","volume":"56","author":"Avila","year":"2011","journal-title":"Annu. Rev. Entomol."},{"key":"2022021808155251000_JEB238782C5","doi-asserted-by":"publisher","first-page":"1767","DOI":"10.1139\/z00-113","article-title":"Incidence of dart shooting, sperm delivery, and sperm storage in natural populations of the simultaneously hermaphroditic land snail Arianta arbustorum","volume":"78","author":"Baminger","year":"2000","journal-title":"Can. J. Zool."},{"key":"2022021808155251000_JEB238782C6","doi-asserted-by":"publisher","first-page":"1477","DOI":"10.1016\/j.peptides.2003.10.023","article-title":"Functions and analysis of the seminal fluid proteins of male Drosophila melanogaster fruit flies","volume":"25","author":"Chapman","year":"2004","journal-title":"Peptides"},{"key":"2022021808155251000_JEB238782C7","doi-asserted-by":"publisher","first-page":"183","DOI":"10.4003\/0740-2783-23.1.183","article-title":"The function of dart shooting in helicid snails","volume":"23","author":"Chase","year":"2007","journal-title":"Amer. Malacol. Bull."},{"key":"2022021808155251000_JEB238782C8","doi-asserted-by":"publisher","first-page":"1471","DOI":"10.1098\/rspb.2006.3474","article-title":"The snail's love-dart delivers mucus to increase paternity","volume":"273","author":"Chase","year":"2006","journal-title":"Pro. Roy. Soc. B"},{"key":"2022021808155251000_JEB238782C9","doi-asserted-by":"publisher","first-page":"732","DOI":"10.1007\/s00265-005-0103-y","article-title":"Independence, not conflict, characterizes dart-shooting and sperm exchange in a hermaphroditic snail","volume":"59","author":"Chase","year":"2006","journal-title":"Behav. Ecol. Sociobiol."},{"key":"2022021808155251000_JEB238782C10","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1016\/0092-8674(88)90192-4","article-title":"A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster","volume":"54","author":"Chen","year":"1988","journal-title":"Cell"},{"key":"2022021808155251000_JEB238782C11","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1016\/j.anbehav.2020.06.009","article-title":"Disentangling female postmating responses induced by semen transfer components in a simultaneous hermaphrodite","volume":"166","author":"Daupagne","year":"2020","journal-title":"Anim. Behav."},{"key":"2022021808155251000_JEB238782C12","doi-asserted-by":"publisher","first-page":"10025","DOI":"10.1073\/pnas.0901217106","article-title":"Postcopulatory sexual selection: Darwin's omission and its consequences","volume":"106","author":"Eberhard","year":"2009","journal-title":"Proc. Natl. Acad. Sci. U.S.A"},{"key":"2022021808155251000_JEB238782C13","doi-asserted-by":"publisher","first-page":"92","DOI":"10.1016\/0304-3940(90)90523-C","article-title":"\u03b2-Endorphin acts on the reproductive tract of female rats to suppress sexual receptivity","volume":"115","author":"Forsberg","year":"1990","journal-title":"Neurosci. Lett."},{"key":"2022021808155251000_JEB238782C14","doi-asserted-by":"publisher","first-page":"819","DOI":"10.1016\/0010-406X(66)90438-5","article-title":"The internal chloride concentration of H and D cells in the snail brain","volume":"19","author":"Kerkut","year":"1966","journal-title":"Comp. Biochem. Physiol."},{"key":"2022021808155251000_JEB238782C15","first-page":"59","article-title":"Interference effect of the alien land snail Macrochlamys sp. on the native land snail Bekkochlamys perfragilis","volume":"17","author":"Kimura","year":"2015","journal-title":"Res. Bull. Environ. Edu. Center, Miyagi Univ. Edu."},{"key":"2022021808155251000_JEB238782C16","doi-asserted-by":"publisher","first-page":"815","DOI":"10.1007\/s10682-009-9339-8","article-title":"Interspecific interference competition alters habitat use patterns in two species of land snails","volume":"24","author":"Kimura","year":"2010","journal-title":"Evol. Ecol."},{"key":"2022021808155251000_JEB238782C17","doi-asserted-by":"publisher","first-page":"806","DOI":"10.1111\/bij.12008","article-title":"Delayed spermatophore removal in the land snail Euhadra peliomphala","volume":"108","author":"Kimura","year":"2013","journal-title":"Biol. J. Linn. Soc."},{"key":"2022021808155251000_JEB238782C18","doi-asserted-by":"publisher","first-page":"264","DOI":"10.1186\/1471-2148-13-264","article-title":"Strategic ejaculation in simultaneously hermaphroditic land snails: more sperm into virgin mates","volume":"13","author":"Kimura","year":"2013","journal-title":"BMC Evol. Biol."},{"key":"2022021808155251000_JEB238782C19","doi-asserted-by":"publisher","first-page":"20143063","DOI":"10.1098\/rspb.2014.3063","article-title":"The direct cost of traumatic secretion transfer in hermaphroditic land snails: individuals stabbed with a love dart decrease lifetime fecundity","volume":"282","author":"Kimura","year":"2015","journal-title":"Pro. Roy. Soc. B"},{"key":"2022021808155251000_JEB238782C20","doi-asserted-by":"publisher","first-page":"631","DOI":"10.1016\/j.anbehav.2012.12.026","article-title":"The mucus of a land snail love-dart suppresses subsequent matings in darted individuals","volume":"85","author":"Kimura","year":"2013","journal-title":"Anim. Behav."},{"key":"2022021808155251000_JEB238782C21","doi-asserted-by":"publisher","first-page":"1150","DOI":"10.1242\/jeb.095935","article-title":"Common effect of the mucus transferred during mating in two dart-shooting snail species from different families","volume":"217","author":"Kimura","year":"2014","journal-title":"J. Exp. Biol."},{"key":"2022021808155251000_JEB238782C22","doi-asserted-by":"publisher","first-page":"284","DOI":"10.1080\/03949370.2015.1037359","article-title":"Effect of injection of love-dart mucus on physical vigour in land snails: can remating suppression be explained by physical damage","volume":"28","author":"Kimura","year":"2016","journal-title":"Ethol. Ecol. Evol."},{"key":"2022021808155251000_JEB238782C23","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1080\/07924259.2005.9652176","article-title":"Allohormones and sensory traps: a fundamental difference between hermaphrodites and gonochorists","volume":"48","author":"Koene","year":"2005","journal-title":"Invertebr. Reprod. Dev."},{"key":"2022021808155251000_JEB238782C24","doi-asserted-by":"publisher","first-page":"2313","DOI":"10.1242\/jeb.201.15.2313","article-title":"Changes in the reproductive system of the snail Helix aspersa caused by mucus from the love dart","volume":"201","author":"Koene","year":"1998","journal-title":"J. Exp. Biol."},{"key":"2022021808155251000_JEB238782C25","doi-asserted-by":"publisher","first-page":"773","DOI":"10.1093\/beheco\/12.6.773","article-title":"Dart shooting influences paternal reproductive success in the snail Helix aspersa (Pulmonata, Stylommatophora)","volume":"12","author":"Landolfa","year":"2001","journal-title":"Behav. Ecol."},{"key":"2022021808155251000_JEB238782C26","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1093\/mollus\/eyv046","article-title":"The love-darts of land snails: integrating physiology, morphology and behaviour","volume":"82","author":"Lodi","year":"2016","journal-title":"J. Molluscan Stud."},{"key":"2022021808155251000_JEB238782C27","first-page":"65","article-title":"Notes on the copulation and spawning of Euhadra quaesita","volume":"22","author":"Nagasawa","year":"1991","journal-title":"Chiribotan"},{"key":"2022021808155251000_JEB238782C28","first-page":"763","article-title":"The land snail genus Macrochlamys Gray, 1847 from Thailand, with descriptions of five new species (Pulmonata: Ariophantidae)","volume":"66","author":"Pholyotha","year":"2018","journal-title":"Raffles Bull. Zool."},{"key":"2022021808155251000_JEB238782C29","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1007\/s00265-006-0178-0","article-title":"Complexity of seminal fluid: a review","volume":"60","author":"Poiani","year":"2006","journal-title":"Behav. Ecol. Sociobiol."},{"key":"2022021808155251000_JEB238782C30","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1093\/mollus\/61.3.325","article-title":"Mating behaviour of Deroceras rodnae Grossu and Lupu, 1965 and D. praecox Wiktor, 1966 (Pulmonata: Agriolimacidae)","volume":"61","author":"Reise","year":"1995","journal-title":"J. Molluscan Stud."},{"key":"2022021808155251000_JEB238782C31","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1093\/mollus\/eyu089","article-title":"Mating behaviour, dart shape and spermatophore morphology of the Cuban tree snail Polymita picta (Born, 1780)","volume":"81","author":"Reyes-Tur","year":"2015","journal-title":"J. Molluscan Stud."},{"key":"2022021808155251000_JEB238782C32","doi-asserted-by":"publisher","first-page":"122","DOI":"10.1007\/s002650100345","article-title":"Dart receipt promotes sperm storage in the garden snail Helix aspersa","volume":"50","author":"Rogers","year":"2001","journal-title":"Behav. Ecol. Sociobiol."},{"key":"2022021808155251000_JEB238782C33","doi-asserted-by":"publisher","first-page":"581","DOI":"10.1016\/j.tree.2005.08.014","article-title":"The darting game in snails and slugs","volume":"20","author":"Schilthuizen","year":"2005","journal-title":"Trends Ecol. Evol."},{"key":"2022021808155251000_JEB238782C34","doi-asserted-by":"publisher","first-page":"380","DOI":"10.1093\/gbe\/evy242","article-title":"Insights into the evolution of shells and love darts of land snails revealed from their matrix proteins","volume":"11","author":"Shimizu","year":"2019","journal-title":"Genome Biol. Evol."},{"key":"2022021808155251000_JEB238782C35","doi-asserted-by":"publisher","first-page":"1173","DOI":"10.1093\/beheco\/arn090","article-title":"Dual function of seminal substances for mate guarding in a ground beetle","volume":"19","author":"Takami","year":"2008","journal-title":"Behav. Ecol."},{"key":"2022021808155251000_JEB238782C36","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1002\/jez.1402070103","article-title":"A sex pheromone secreting gland in the terrestrial snail, Euhadra peliomphala","volume":"207","author":"Takeda","year":"1979","journal-title":"J. Exp. Zool."},{"key":"2022021808155251000_JEB238782C37","first-page":"325","article-title":"Notes on a swelling on the head in land snails","volume":"42","author":"Taki","year":"1930","journal-title":"Zool. Mag."},{"key":"2022021808155251000_JEB238782C38","first-page":"159","article-title":"Notes on a warty growth on the head of some land snails","volume":"13","author":"Taki","year":"1935","journal-title":"J. Sci., Hiroshima Univ., Ser. B, Div."},{"key":"2022021808155251000_JEB238782C39","doi-asserted-by":"publisher","first-page":"973","DOI":"10.1093\/biolinnean\/blaa171","article-title":"Genetic variation in the Giant African Snail Lissachatina fulica (Bowdich, 1822) in its invasive ranges of Asia and West Africa","volume":"131","author":"Vijayan","year":"2020","journal-title":"Biol. J. Linn. Soc."},{"key":"2022021808155251000_JEB238782C40","doi-asserted-by":"crossref","DOI":"10.1007\/978-0-387-87458-6","volume-title":"Mixed Effects Models and Extensions in Ecology with R","author":"Zuur","year":"2009"}],"container-title":["Journal of Experimental Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.biologists.com\/jeb\/article-pdf\/doi\/10.1242\/jeb.238782\/2129081\/jeb238782.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/journals.biologists.com\/jeb\/article-pdf\/doi\/10.1242\/jeb.238782\/2131351\/jeb238782.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/journals.biologists.com\/jeb\/article-pdf\/doi\/10.1242\/jeb.238782\/2131351\/jeb238782.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,2,18]],"date-time":"2022-02-18T08:16:02Z","timestamp":1645172162000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/jeb\/article\/225\/4\/jeb238782\/274420\/Sexual-inactivation-induced-by-the-mucus-that"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,2,15]]},"references-count":40,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2022,2,15]]}},"URL":"https:\/\/doi.org\/10.1242\/jeb.238782","relation":{},"ISSN":["0022-0949","1477-9145"],"issn-type":[{"value":"0022-0949","type":"print"},{"value":"1477-9145","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,2,15]]},"article-number":"jeb238782"}}