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.

多种同时雌雄同体的陆生蜗牛展现出一种显著的交配行为，即所谓的"恋矢（love dart）射击"。在交配过程中，这类陆生蜗牛会通过将恋矢刺入交配伴侣的身体，来传递特定的分泌物。已有研究证实，精子供体可从这种创伤性分泌物转移行为中获益——该分泌物会操控精子受体的生理机能，提升供体自身的受精成功率。然而，目前尚不清楚接受恋矢射击是否会对受体个体造成适应性代价。因此，性冲突与对抗性军备竞赛对陆生蜗牛创伤性分泌物转移行为演化的影响，至今仍存在学术争议。为探究这一影响，我们以亮巴蜗牛（Bradybaena pellucida）为实验对象，对比了接受过交配伴侣恋矢射击与未接受该行为的个体的终身繁殖力与寿命。实验结果显示，接收恋矢的蜗牛其终身繁殖力与寿命均出现显著下降。上述结果表明，这种代价高昂的交配行为——恋矢射击——会在精子供体与受体之间引发性冲突，而对抗性军备竞赛推动了与恋矢射击相关的形态与行为特征的多样化。本研究结果同时支持了"雌雄同体动物的性冲突会出现剧烈升级"的理论假说。