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Material heterogeneity of male genitalia reduces genital damage in a bushcricket during sperm removal behaviour.

ABSTRACT: Sperm removal behaviour (SRB) is known in many animals, and male genital structures are often involved in the SRB, e.g. rubbing female genitalia vigorously. However, it remains unclear how those male genital structures function properly without severe genital damage during SRB. In the present study, we focused on the bushcricket Metaplastes ornatus and examined the biomechanics of male and female genital structures, involved in their SRB as a model case. During an initial phase of mating, males of this species thrust their subgenital plate with hook-like spurs and many microscopic spines into the female genital chamber. By moving the subgenital plate back-and-forth, males stimulate females, and this stimulation induces the ejection of sperm previously stored in females. We aimed to uncover the mechanics of the interaction between the subgenital plate and genital chamber during SRB. The genital morphology and its material composition were investigated using modern imaging and microscopy techniques. The obtained results showed a pronounced material heterogeneity in the subgenital plate and the genital chamber. The material heterogeneity was completely absent in that of a second bushcricket species, Poecilimon veluchianus, which does not exhibit SRB. Finite element simulations showed that the specific material heterogeneity can redistribute the stress in the subgenital plate of M. ornatus and, thereby, reduces stress concentration during SRB. This may explain why only a few examined males had a broken spur. We suggest that the observed structural features and material heterogeneity in M. ornatus are adaptations to their SRB.

SUBMITTER: Matsumura Y

PROVIDER: S-EPMC7688094 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundAsymmetric genitalia have repeatedly evolved in animals, yet the underlying causes for their evolution are mostly unknown. The fruit fly Drosophila pachea has asymmetric external genitalia and an asymmetric phallus with a right-sided phallotrema (opening for sperm release). The complex of female and male genitalia is asymmetrically twisted during copulation and males adopt a right-sided copulation posture on top of the female. We wished to investigate if asymmetric male genital morphology and a twisted gentitalia complex may be associated with differential allocation of sperm into female sperm storage organs.MethodsWe examined the internal complex of female and male reproductive organs by micro-computed tomography and synchrotron X-ray tomography before, during and after copulation. In addition, we monitored sperm aggregation states and timing of sperm transfer during copulation by premature interruption of copulation at different time-points.ResultsThe asymmetric phallus is located at the most caudal end of the female abdomen during copulation. The female reproductive tract, in particular the oviduct, re-arranges during copulation. It is narrow in virgin females and forms a broad vesicle at 20 min after the start of copulation. Sperm transfer into female sperm storage organs (spermathecae) was only in a minority of examined copulation trials (13/64). Also, we found that sperm was mainly transferred early, at 2-4 min after the start of copulation. We did not detect a particular pattern of sperm allocation in the left or right spermathecae. Sperm adopted a granular or filamentous aggregation state in the female uterus and spermathecae, respectively.DiscussionNo evidence for asymmetric sperm deposition was identified that could be associated with asymmetric genital morphology or twisted complexing of genitalia. Male genital asymmetry may potentially have evolved as a consequence of a complex internal alignment of reproductive organs during copulation in order to optimize low sperm transfer rates.

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Material heterogeneity of male genitalia reduces genital damage in a bushcricket during sperm removal behaviour.

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