Abstract
Species of the Brazilian cave barklouse genus Neotrogla (Psocodea: “Psocoptera”: Trogiomorpha: Prionoglarididae: Sensitibillini) are known to have a “female penis (gynosome)” that functions as an intromittent organ inserted into the membranous pouches in the simple male genital chamber during copulation to receive semen. However, the functions of other male and female genital structures and the copulatory processes of Neotrogla were completely unknown to date. Based on µCT observation of the male and female postabdomen and connected muscles both before and in copula, we clarified the functions of the male and female genital structures. In addition, based on the analyses of the established 3D models, we concluded that precise and rigid contact of multiple genital structures, and step-by-step releases of each holding mechanism achieved by the cooperation of both sexes are involved in the copulatory processes. The coevolution between the male and female genital structures in Neotrogla may provide a new example for the evolution of tolerance traits.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00114-023-01855-8/MediaObjects/114_2023_1855_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00114-023-01855-8/MediaObjects/114_2023_1855_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00114-023-01855-8/MediaObjects/114_2023_1855_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00114-023-01855-8/MediaObjects/114_2023_1855_Fig4_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00114-023-01855-8/MediaObjects/114_2023_1855_Fig5_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00114-023-01855-8/MediaObjects/114_2023_1855_Fig6_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00114-023-01855-8/MediaObjects/114_2023_1855_Fig7_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00114-023-01855-8/MediaObjects/114_2023_1855_Fig8_HTML.png)
Similar content being viewed by others
References
Arnqvist G, Rowe L (2002) Correlated evolution of male and female morphologles in water striders. Evolution 56:936–947. https://doi.org/10.1111/j.0014-3820.2002.tb01406.x
Cheng Z, Yoshizawa K (2019) Functional morphology of Trichadenotecnum male and female genitalia analyzed using μCT (Insecta: Psocodea: Psocomorpha). J Morph 280:555–567. https://doi.org/10.1002/jmor.20965
Cheng Z, Yoshizawa K (2022) Exploration of the homology among the muscles associated with the female genitalia of the three suborders of Psocodea (Insecta). Arthropod Str Dev 66:101141. https://doi.org/10.1016/j.asd.2022.101141
Cheng Z, Kamimura Y, Ferreira RL, Lienhard C, Yoshizawa K (2023) Acquisition of novel muscles enabled protruding and retracting mechanisms of female penis in sex-role reversed cave insects. Roy Soc Open Sci. 10:220471. https://doi.org/10.1098/rsos.220471
House CM, Simmons LW (2006) Offensive and defensive sperm competition roles in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae). Behav Ecol Sociobiol 60:131–136 (https://www.jstor.org/stable/25063796)
Kamimura Y (2012) Correlated evolutionary changes in Drosophila female genitalia reduce the possible infection risk caused by male copulatory wounding. Behav Ecol Sociobiol 66:1107–1114. https://doi.org/10.1007/s00265-012-1361-0
Kamimura Y, Mitsumoto H (2012) Lock-and-key structural isolation between sibling Drosophila species. Entomol Sci 15:197–201. https://doi.org/10.1111/j.1479-8298.2011.00490.x
Kamimura Y, Yoshizawa K, Lienhard C, Ferreira RL, Abe J (2021) Evolution of nuptial gifts and its coevolutionary dynamics with male-like persistence traits of females for multiple mating. BMC Ecol Evol 21:164. https://doi.org/10.1186/s12862-021-01901-x
Lange R, Reinhardt K, Michiels NK, Anthes N (2013) Functions, diversity, and evolution of traumatic mating. Biol Rev 88:585–601. https://doi.org/10.1111/brv.12018
Lewis S, South A (2012) The evolution of animal nuptial gifts. Adv Study Behav 44:53–97. https://doi.org/10.1016/B978-0-12-394288-3.00002-2
Lienhard C (2007) Description of a new African genus and a new tribe of Speleketorinae (Psocodea: ‘Psocoptera’: Prionoglarididae). Rev Suiss Zool 114:441–469. https://doi.org/10.5962/bhl.part.80399
Lienhard C, Carmo TOD, Ferreira RL (2010) A new genus of Sensitibillini from Brazilian caves (Psocodea: “Psocoptera”: Prionoglarididae). Rev Suiss Zool 117:611–635. https://doi.org/10.5962/bhl.part.117600
Lienhard C, Ferreira RL (2013) A new species of Neotrogla from Brazilian caves (Psocodea:’Psocoptera’: Prionoglarididae). Rev Suiss Zool 120:3–12
Masly JP, Kamimura Y (2014) Asymmetric mismatch in strain-specific genital morphology causes increased harm to Drosophila females. Evolution 68:2401–2411. https://doi.org/10.1111/evo.12436
Michels J, Gorb SN, Reinhardt K (2015) Reduction of female copulatory damage by resilin represents evidence for tolerance in sexual conflict. J Roy Soc Interface 12:20141107. https://doi.org/10.1098/rsif.2014.1107
Polak M, McEvey SF (2022) Refutation of traumatic insemination in the Drosophila bipectinata species complex. Biol Lett 18:20210625. https://doi.org/10.1098/rsbl.2021.0625
Simmons LW (2014) Sexual selection and genital evolution. Austral Entomol 53:1–17. https://doi.org/10.1111/aen.12053
Sota T, Kubota K (1998) Genital lock-and-key as a selective agent against hybridization. Evolution 52:1507–1513. https://doi.org/10.1111/j.1558-5646.1998.tb02033.x
Tanaka KM, Kamimura Y, Takahashi A (2018) Mechanical incompatibility caused by modifications of multiple male genital structures using genomic introgression in Drosophila. Evolution 72:2406–2418. https://doi.org/10.1111/evo.13592
Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man, 1871–1971. Aldine-Atherton, Chicago, pp 136–179
Uesugi K, Hoshino M, Takeuchi A, Suzuki Y, Yagi N (2012) Development of fast and high throughput tomography using CMOS image detector at SPring-8. Dev X-Ray Tomography VIII 8506:85060I. https://doi.org/10.1117/12.929575
Uesugi K, Hoshino M, Takeuchi A (2017) Introducing high efficiency image detector to X-ray imaging tomography. J Phys Conference Series 849:012051. https://doi.org/10.1088/1742-6596/849/1/012051
Yoshizawa K (2001) A systematic revision of Japanese Trichadenotecnum Enderlein (Psocodea:’Psocoptera’: Psocidae: Ptyctini), with redefinition and subdivision of the genus. Invertebr Syst 15:159–204. https://doi.org/10.1071/IT00013
Yoshizawa K (2005) Morphology of Psocomorpha (Psocodea:’ Psocoptera’). Insecta Matsumurana NS 62:1–44
Yoshizawa K, Ferreira RL, Kamimura Y, Lienhard C (2014) Female penis, male vagina, and their correlated evolution in a cave insect. Curr Biol 24:1006–1010. https://doi.org/10.1016/j.cub.2014.03.022
Yoshizawa K, Kamimura Y, Lienhard C, Ferreira RL, Blanke A (2018) A biological switching valve evoluved in the female of a sex-role reversed cave insect to receive multiple seminal packages. eLife 7:e39563. https://doi.org/10.7554/eLife.39563
Yoshizawa K, Ferreira RL, Yao I, Lienhard C, Kamimura Y (2018b) Independent origins of female penis and its coevolution with male vagina in cave insects (Psocodea: Prionoglarididae). Biol Lett 14:20180533. https://doi.org/10.1098/rsbl.2018.0533
Yoshizawa K, Ferreira RL, Lienhard C, Kamimura Y (2019) Why did a female penis evolve in a small group of cave insects? BioEssays 41:1900005. https://doi.org/10.1002/bies.201900005
Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, Gerig G (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31:1116–1128. https://doi.org/10.1016/j.neuroimage.2006.01.015
Acknowledgements
We thank Kentaro Uesugi for support with the µCT imaging. Research at Spring-8 was approved through project numbers 2016A1269 (leader: Ryuichiro Machida), 2017B1712 and 2018B1725 (Naoki Ogawa). This work was supported by Japan Society for the Promotion of Science, grant numbers 20J2088301 to ZC and 15H04409 and 19H03278 to KY. RLF thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq grant n. 308334/2018-3).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interests.
Additional information
Communicated by: Matthias Waltert
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Cheng, Z., Kamimura, Y., Ferreira, R.L. et al. Are males just passive? Coupling mechanism of the Brazilian cave insects with inverted genitalia. Sci Nat 110, 26 (2023). https://doi.org/10.1007/s00114-023-01855-8
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00114-023-01855-8