Ontogeny of the complex sperm in the macrostomid flatworm <i>Macrostomum lignano</i> (Macrostomorpha, Rhabditophora)

Willems, Maxime; Leroux, Frédéric R.; Claeys, Myriam; Boone, M. A.; Mouton, Stijn; Artois, Tom; Borgonie, Gaëtan

doi:10.1002/jmor.10675

Cited by 18 publications

(33 citation statements)

References 17 publications

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“…The evolutionary origin of the sperm bristles currently is unclear (51). A study of sperm ultrastructure suggests a homology between the bristles in Macrostomum and lateral ledges in the sperm of Bradynectes sterreri (one of our outgroup species) and Psammomacrostomum turbanelloides (51) (a likely relative of our Gen. nov. 1, sp.…”

Section: Discussionmentioning

confidence: 96%

Mating behavior and the evolution of sperm design

Schärer

Littlewood

Waeschenbach

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

118

312

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Sperm are the most diverse of all animal cell types, and much of the diversity in sperm design is thought to reflect adaptations to the highly variable conditions under which sperm function and compete to achieve fertilization. Recent work has shown that these conditions often evolve rapidly as a consequence of multiple mating, suggesting a role for sexual selection and sexual conflict in the evolution of sperm design. However, very little of the striking diversity in sperm design is understood functionally, particularly in internally fertilizing organisms. We use phylogenetic comparative analyses covering 16 species of the hermaphroditic flatworm genus Macrostomum to show that a complex sperm design is associated with reciprocal mating and that this complexity is lost secondarily when hypodermic insemination-sperm injection through the epidermis-evolves. Specifically, the complex sperm design, which includes stiff lateral bristles, is likely a male persistence trait associated with sexual conflicts over the fate of received ejaculates and linked to female resistance traits, namely an intriguing postcopulatory sucking behavior and a thickened epithelium of the sperm-receiving organ. Our results suggest that the interactions between sperm donor, sperm, and sperm recipient can change drastically when hypodermic insemination evolves, involving convergent evolution of a needle-like copulatory organ, a simpler sperm design, and a simpler female genital morphology. Our study documents that a shift in the mating behavior may alter fundamentally the conditions under which sperm compete and thereby lead to a drastic change in sperm design.Platyhelminthes | sexually antagonistic coevolution | simultaneous hermaphrodite | sperm morphology | traumatic insemination P arker's (1-3) far-reaching extension of Darwin's (4) narrow focus on precopulatory mating interactions highlighted that sexual selection continues to operate after mating partners have agreed to mate and that considering postcopulatory sexual selection therefore is crucial to understand the evolution of many reproductive traits (5, 6). This insight has led to extensive research in evolutionary biology that focused on understanding the biology of sperm (7), the most diverse of all animal cell types (8,9). From this research emerged an apparent consensus that the diversity in sperm design-the strikingly variable ways of constructing a sperm-reflects the highly variable physiological and morphological environments in which sperm have to survive, function, and compete for fertilization (5,(10)(11)(12)(13)(14). Moreover, recent studies have documented clearly that these environments can evolve rapidly, probably because of coevolutionary interactions linked to multiple mating and the resulting sexual selection and sexual conflicts (15-21). However, the bewildering diversity in sperm design is poorly understood at the functional level, particularly in internally fertilizing organisms (9,12,22). A recent review on the evolution of sperm morphological diversity concluded...

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Section: Discussionmentioning

confidence: 96%

Mating behavior and the evolution of sperm design

Schärer

Littlewood

Waeschenbach

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

118

312

View full text Add to dashboard Cite

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“…2D), and ultrastructure reveals a corresponding differentiation of the intracellular structure (Fig. 5), which changes during spermiogenesis (Willems et al. , 2009).…”

Section: Morphology and Behaviour Of The Genitalia And Spermmentioning

confidence: 97%

Goings-on inside a worm: functional hypotheses derived from sexual conflict thinking

Vizoso¹,

Rieger²,

Schärer³

2010

Biological Journal of the Linnean Society

132

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Different interests between mating partners regarding the fate of their gametes can lead to sexual conflicts in many species. Although these conflicts can sometimes be dealt with pre-copulatorily (e.g. by choosing with which partners to mate), they often extend beyond copulation. Post-copulatory sexual conflicts are expected to be particularly strong in simultaneous hermaphrodites because an individual may have to accept sperm in order to obtain an opportunity to donate sperm, reducing the effectiveness of pre-copulatory conflict resolution. The present study investigates the post-copulatory interactions between male and female sexual traits of a highly promiscuous simultaneous hermaphrodite, the free-living flatworm Macrostomum lignano. Using light and electron microscopy, we show the different levels of complexity of the sperm and the genitalia, and derive hypotheses about how the different traits may represent evolutionary responses to such sexual conflicts.

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“…1; Vizoso et al 2010). The nucleus is located inside the shaft (Willems et al 2009). So far, the function of the feeler, the bristles, and the brush are not well understood.…”

Section: Communicated By T Moorementioning

confidence: 99%

Sperm competition affects sex allocation but not sperm morphology in a flatworm

Janicke

Schärer

2010

Behav Ecol Sociobiol

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Sperm competition has been shown to be an important evolutionary agent affecting the behaviour, physiology, and morphology of both males and females. One morphological trait that is particularly likely to be affected by sperm competition is sperm size because it is thought to influence the competitiveness of sperm by determining sperm longevity, motility, and/or their ability to displace competing sperm. Most comparative studies across taxa have found a positive relationship between the level of sperm competition and sperm length, but very few studies have tested for a phenotypically plastic adjustment of sperm morphology in response to sperm competition. In this study, we experimentally tested for an effect of sperm competition on phenotypic plasticity in sperm morphology in an obligately outcrossing simultaneous hermaphrodite, the free-living flatworm Macrostomum lignano, by either raising worms in monogamous pairs (no sperm competition) or in promiscuous groups (intense sperm competition). Worms in groups produced larger testes and smaller ovaries as predicted by sex allocation theory and as previously documented in this species. However, we found no evidence for an effect of group size on sperm morphology, measured as total sperm length, sperm body length, and the length of two different sperm appendages. We conclude that M. lignano may either be incapable of adjusting the sperm morphology in a phenotypically plastic way and/or that there might be no benefit of phenotypic plasticity in sperm traits in this species.

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Ontogeny of the complex sperm in the macrostomid flatworm Macrostomum lignano (Macrostomorpha, Rhabditophora)

Cited by 18 publications

References 17 publications

Mating behavior and the evolution of sperm design

Mating behavior and the evolution of sperm design

Goings-on inside a worm: functional hypotheses derived from sexual conflict thinking

Sperm competition affects sex allocation but not sperm morphology in a flatworm

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