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Frequent origins of traumatic insemination involve convergent shifts in sperm and genital morphology

View ORCID ProfileJeremias N. Brand, Luke J. Harmon, Lukas Schärer
doi: https://doi.org/10.1101/2021.02.16.431427
Jeremias N. Brand
1University of Basel, Department of Environmental Sciences, Zoological Institute, Vesalgasse 1, 4051 Basel, Switzerland
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  • ORCID record for Jeremias N. Brand
  • For correspondence: jeremias.br@gmail.com
Luke J. Harmon
2Department of Biological Sciences, University of Idaho, Moscow, USA
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Lukas Schärer
1University of Basel, Department of Environmental Sciences, Zoological Institute, Vesalgasse 1, 4051 Basel, Switzerland
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Abstract

Traumatic insemination is a mating behaviour during which the (sperm) donor uses a traumatic intromittent organ to inject an ejaculate through the epidermis of the (sperm) recipient, thereby frequently circumventing the female genitalia. Traumatic insemination occurs widely across animals, but the frequency of its evolution, the intermediate stages via which it originates, and the morphological changes that such shifts involve remain poorly understood. Based on observations in 145 species of the free-living flatworm genus Macrostomum, we identify at least nine independent evolutionary origins of traumatic insemination from reciprocal copulation, but no clear indication of reversals. These origins involve convergent shifts in multivariate morphospace of male and female reproductive traits, suggesting that traumatic insemination has a canalising effect on morphology. Signatures of male-female coevolution across the genus indicate that sexual selection and sexual conflict drive the evolution of traumatic insemination, because it allows donors to bypass postcopulatory control mechanisms of recipients.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • To reduce manuscript complexity, we have separated the phylogenetic and taxonomic work from the comparative analysis. The phylogenetics will also be available as a preprint: bioRxiv:2021/437366 As a result of this change authors who have contributed to the molecular biology and bioinformatics work, but not to the comparative analysis presented in this manuscript, have been removed. All removed authors are coauthors of the phylogenetics manuscript.

  • Abbreviations

    HI
    Hypodermic insemination
    PC
    principal component
    pPCA
    phylogenetically corrected principal component analysis
  • Copyright 
    The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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    Posted March 28, 2021.
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    Frequent origins of traumatic insemination involve convergent shifts in sperm and genital morphology
    Jeremias N. Brand, Luke J. Harmon, Lukas Schärer
    bioRxiv 2021.02.16.431427; doi: https://doi.org/10.1101/2021.02.16.431427
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    Frequent origins of traumatic insemination involve convergent shifts in sperm and genital morphology
    Jeremias N. Brand, Luke J. Harmon, Lukas Schärer
    bioRxiv 2021.02.16.431427; doi: https://doi.org/10.1101/2021.02.16.431427

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