Piercing the partner's skin influences sperm uptake in the earthworm Lumbricus terrestris

Koene, Joris M.; Pförtner, Tina; Michiels, Nico K.

doi:10.1007/s00265-005-0030-y

Cited by 55 publications

(29 citation statements)

References 28 publications

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“…The latter is consistent with the bizarre mating systems, sperm packaging, and reproductive morphologies found in hermaphrodites [4], [12]. Examples of this include hypodermic insemination in tropical flatworms [22], partner sedation in sea slugs [23], hypodermic injection of gland products in earthworms and sea slugs [18], [24] and highly complex sperm design in flatworms [25].…”

Section: Introductionsupporting

confidence: 58%

A Syringe-Like Love Dart Injects Male Accessory Gland Products in a Tropical Hermaphrodite

2013

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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.

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Section: Introductionsupporting

confidence: 58%

A Syringe-Like Love Dart Injects Male Accessory Gland Products in a Tropical Hermaphrodite

2013

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“…F) of stylommatophoran land snails (Davison et al ., ; Koene & Schulenburg, ), the copulatory setae in earthworms (Cuadrado & Martinez‐Ansemil, ; Koene et al ., ), the teeth of plethodontid salamanders involved in copulatory biting (Houck & Reagan, ; Rollmann, Houck & Feldhoff, ; Houck & Arnold, ), the sting of scorpions that display a ‘sexual sting’ ritual (Inceoglu et al ., ), and male fang use in a wolf spider (Johns et al ., ). Consistent with the paternity‐benefit hypothesis, mucus delivered with the snail's love dart has been shown to increase a successful shooter's fertilisation success (Chase & Blanchard, ), while setal gland products in earthworms increase the partner's refractory period and sperm uptake (Koene et al ., ), and secretions transferred during copulatory biting in salamanders increase current receptivity and shorten time to sperm transfer (Houck & Reagan, ; Rollmann et al ., ). In scorpions, it is speculated that the injection of a pre‐venom into the female's body tranquilises females and so reduces physical resistance to mating (discussed in Inceoglu et al ., ).…”

Section: Categorisation Of Traumatic Mating Strategiesmentioning

confidence: 99%

Functions, diversity, and evolution of traumatic mating

et al. 2013

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Copulation can involve the wounding of the mating partner by specialised devices. This type of mating, which we term traumatic mating, has been regarded as exceptional. Its prevalence, however, has not been compared across taxa, nor have its functions and putative evolutionary pathways. A categorisation has been lacking to date. We here show that traumatic mating is a widespread and diverse phenomenon that likely evolved via several pathways. Its putative functions include: (i) anchorage during mating; (ii) stimulation of short-term female reproductive investment; (iii) male paternity advantages; and (iv) enhanced fertilisation efficiency in transitions to internal fertilisation. Both natural and sexual selection have likely contributed to the parallel evolution of traumatic intromittent organs in phylogenetically distant taxa. These organs are sometimes remarkably similar in shape and often, but not always, inject sperm. The target sites of trauma infliction and the nature of secretions delivered alongside sperm are thus far poorly studied, but data on both are needed to elucidate the function of traumatic mating. The few existing studies that explicitly quantify fitness impacts of traumatic mating indicate that this strategy may often be costly to the party being wounded. However, a comprehensive approach to assess overall investments and returns for both sexes is a major target for future work. Finally, for the first time, we corroborate quantitatively the hypothesis that traumatic mating evolved relatively more often among hermaphroditic than among gonochoric taxa.

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“…For example, sexual conflict is thought to have resulted in the evolution of seemingly harmful matings involving traumatic insemination in separate‐sexed organisms such as bedbugs (Arnqvist & Rowe, ), strepsiptera insects (Peinert et al, ), and some cephalopods (Hoving et al, ), and in hermaphrodites such as sea slugs and polyclad flatworms (Anthes & Michiels, ; Michiels & Newman, ; Schmitt, Anthes, & Michiels, ); for a review see Reinhardt, Anthes, & Lange, ). Besides injection of sperm, hypodermic injection of accessory gland products alone can also be harmful, which is the case in land snails (Hasse, Marxen, Becker, Ehrenberg, & Epple, ; Koene, ; Schilthuizen, ) and earthworms (Koene, Pförtner, & Michiels, ; for a review see Zizzari, Smolders, & Koene, ).…”

Section: Introductionmentioning

confidence: 99%

The effect of mating on female reproduction across hermaphroditic freshwater snails

Swart

Starkloff

Ypenburg

et al. 2020

Invertebrate Biology

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Sexual conflicts often arise between mating partners because each sex tries to maximize its own reproductive success. One major male strategy to influence a partner's resource allocation is the transfer of accessory gland proteins. This has been shown to occur in simultaneous hermaphrodites as well as in organisms with separate sexes. Although accessory gland proteins affect the investment of resources in both male and female function, we here specifically focus on female investment. In the great pond snail, Lymnaea stagnalis, previous studies found that the accessory gland protein ovipostatin reduced female fecundity by suppressing egg laying in the partner in the short term (days). To investigate whether this reduction in egg laying is a commonly found effect of mating in freshwater snails, we compared egg output for evidence of suppression in isolated and paired snails of eight pulmonate species. Furthermore, we determined whether the suppression of egg laying caused a shift in resource allocation to the eggs. We found that in five of the eight species egg laying was suppressed, with fewer and lighter egg masses being laid when they had access to a mating partner. In mated pairs of L. stagnalis and Biomphalaria alexandrina, allocation of resources to the eggs was altered in opposite ways: individuals of L. stagnalis laid fewer but larger and heavier eggs; individuals of B. alexandrina laid smaller and lighter eggs, with no change in egg numbers. Such changes in the female function are most likely the result of combined effects of receiving accessory gland proteins, and the cost of mating in both male and female roles. Thus, effects of the maternal environment, including the receipt of accessory gland proteins, on offspring investment are not restricted to species with separate sexes.

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Piercing the partner's skin influences sperm uptake in the earthworm Lumbricus terrestris

Cited by 55 publications

References 28 publications

A Syringe-Like Love Dart Injects Male Accessory Gland Products in a Tropical Hermaphrodite

A Syringe-Like Love Dart Injects Male Accessory Gland Products in a Tropical Hermaphrodite

Functions, diversity, and evolution of traumatic mating

The effect of mating on female reproduction across hermaphroditic freshwater snails

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