Dataset Information

Mating behavior and the evolution of sperm design.

ABSTRACT: 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.

SUBMITTER: Scharer L

PROVIDER: S-EPMC3029721 | biostudies-literature | 2011 Jan

REPOSITORIES: biostudies-literature

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Mating behavior and the evolution of sperm design.

Schärer Lukas L Littlewood D Timothy J DT Waeschenbach Andrea A Yoshida Wataru W Vizoso Dita B DB

Proceedings of the National Academy of Sciences of the United States of America 20110110 4

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 ...[more]

PMID: 21220334

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Project description:Male reproductive biology can by characterized through competition over mates as well as mate choice. Multiple mating and male mate choice copying, especially in internally fertilizing species, set the stage for increased sperm competition, i.e., sperm of two or more males can compete for fertilization of the female's ova. In the internally fertilizing fish Poecilia mexicana, males respond to the presence of rivals with reduced expression of mating preferences (audience effect), thereby lowering the risk of by-standing rivals copying their mate choice. Also, males interact initially more with a non-preferred female when observed by a rival, which has been interpreted in previous studies as a strategy to mislead rivals, again reducing sperm competition risk (SCR). Nevertheless, species might differ consistently in their expression of aggressive and reproductive behaviors, possibly due to varying levels of SCR. In the current study, we present a unique data set comprising ten poeciliid species (in two cases including multiple populations) and ask whether species can be characterized through consistent differences in the expression of aggression, sexual activity and changes in mate choice under increased SCR. We found consistent species-specific differences in aggressive behavior, sexual activity as well as in the level of misleading behavior, while decreased preference expression under increased SCR was a general feature of all but one species examined. Furthermore, mean sexual activity correlated positively with the occurrence of potentially misleading behavior. An alternative explanation for audience effects would be that males attempt to avoid aggressive encounters, which would predict stronger audience effects in more aggressive species. We demonstrate a positive correlation between mean aggressiveness and sexual activity (suggesting a hormonal link as a mechanistic explanation), but did not detect a correlation between aggressiveness and audience effects. Suites of correlated behavioral tendencies are termed behavioral syndromes, and our present study provides correlational evidence for the evolutionary significance of SCR in shaping a behavioral syndrome at the species level across poeciliid taxa.

Project description:Mating plugs in animals are ubiquitous and are commonly interpreted to be products of mating strategies. In spiders, however, mating plugs may also take on functions beyond female remating prevention. Due to the vagaries of female genital (spermathecal) anatomy, most spiders face the problem of having to secure additional, non-anatomical, protection for transferred sperm. Here, we test the hypothesis that mating plugs, rather than (or in addition to) being adaptations for mating strategies, may serve as sperm protection mechanism. Based on a comparative study on 411 epigyna sampled from 36 families, 187 genera, 330 species of entelegyne spiders, our results confirm the necessity of a sperm protection mechanism. We divided the entelegyne spermathecae into four types: SEG, SED, SCG and SCD. We also studied detailed morphology of epigynal tracts in the spider Diphya wulingensis having the SEG type spermathecae, using 3D-reconstruction based on semi thin histological series section. In this species, we hypothesize that two distinct types of mating plug, the sperm plug and the secretion plug, serve different functions. Morphological details support this: sperm plugs are formed on a modified spermathecal wall by the spilled sperm, and function as a temporary protection mechanism to prevent sperm from leaking and desiccating, while secretion plugs function in postcopulation both as a permanent protection mechanism, and to prevent additional mating. Furthermore, with the modified spermathecal wall of S2 stalk, the problem of shunt of sperm input and output, and the possibility of female multiple mating have been resolved. Variation in spermathecal morphology also suggests that the problem of sperm protection might be resolved in different ways in spiders. Considering mating plugs of varying shapes and origins in the vast morphospace of spiders, we conclude that mating plugs might serve different purposes that relate both to mating strategies, as well as to sperm protection.

Dataset Information

Mating behavior and the evolution of sperm design.

Publications

Mating behavior and the evolution of sperm design.

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