Research Frontiers 2018 Research Frontiers 2018 Life Science 34 The discovery of a female penis in the Brazilian cave insect genus Neotrogla (order Psocodea, family Prionoglarididae, tribe Sensitibillini) received considerable attention by the scientific community and the public (Fig. 1) [1]. Similar female penis is also known from the African cave insect genus Afrotrogla (also a member of Sensitibillini) [2]. During copulation, the females of Neotrogla (and probably Afrotrogla ) receive nutritious semen from the males using the female penis, and the semen forms a capsule within the femaleʼs sperm storage organ (spermatheca) (Fig. 1(d)). The female Neotrogla consume the contents of this seminal capsule not only for fertilization but also as nutrition. In the majority of animals, males are more active for mating (conventional sex-role). In contrast, to compete for this nutritious semen, the female Neotrogla evolved a more active role during mating than males (sex- role reversal), which is considered to be the major evolutionary pressure (reversed sexual selection) facilitating the evolution of female penis. Although there are other more examples of sex- role reversed animals, the genera Neotrogla and Afrotrogla are the only ones known to date in which a female penis has evolved [3]. Due to the systematic position of these two genera (Fig. 3), an independent origin of the female penis has to be assumed (since the genus Sensitibilla , the sister group of Afrotrogla , lacks female penis) [2]. Therefore, in addition to the reversed sexual selection caused by sex-role reversal, there must be at least an additional key factor which facilitated the evolution of a female penis. In search of such a potential factor, we focused on a specialized structure (spermathecal plate) located at the entrance of the spermatheca. In order to examine the detailed structure of this minute spermathecal plate, we used synchrotron μ CT (SR- μ CT) imaging, as well as light microscopes and confocal scanning laser microscopy. High resolution SR- μ CT was carried out at SPring-8 BL47XU using a beam energy of 8 keV in absorption-contrast mode. The tomography system consists of a full field X-ray microscope with Fresnel zone plate optics. The field of view and the effective pixel size are 0.11 mm × 0.11 mm and 0.0826 μ m × 0.0826 μ m, respectively. As a result, we identified the existence of a tiny switching valve (about 0.3 mm wide) at the entrance of the spermatheca (Fig. 2) [4]. The valve system is composed of an inlet duct, a closure element, actuator muscles to incline the closure element, resilin patches (a rubber-like protein) supporting the closure element, and two plates forming two insemination slots. This valve system serves to direct the seminal flow provided from the male into one of two slots Hidden morphological novelty enabling the evolution of female penis in the sex-role reversed cave insects Fig. 1. (a) Neotrogla brasiliensis photographs in a cave in Brazil. (b) Female penis of N. curvata. (c) Male and female terminal abdomens of N. curvata in copula. (d) Light microscopy photograph of the spermatheca, including the switching valve system and seminal capsules. (a) (b) (d) (c) Research Frontiers 2018 Research Frontiers 2018 35 of insemination (Fig. 2(b)). The existence of similar spermathecal plate is also confirmed in Afrotrogla and Sensitibilla (i.e., all genera of Sensitibillini), although its detailed structure and function have not been examined. This represents the first discovery of a functional biological switching valve in the animal kingdom. The females of close relatives of Sensitibillini can only receive one seminal capsule at a time. In contrast, by using the switching valve, the females of Sensitibillini can hold two seminal capsules at a time (Fig. 1(d) and Fig. 2(b)). Therefore, the switching valve makes it possible for female Sensitibillini to receive more nutrition from the males, rendering the female-female competition for the nutritious semen more intense in comparison to other sex-role reversed animals. In addition, independent origins of the female penis, which is an extremely rare evolutionary event, were identified in Sensitibillini, even though this is a small group of cave insects containing three genera and eleven named species, only (Fig. 3) [2]. It is very likely that the evolution of this switching valve was a prerequisite for the reversal of the genital organs in Sensitibillini. Many mechanical solutions engineered by humans do not exist in nature. The switching valve discovered in Neotrogla is constructed in a fundamentally different manner than engineered switching valves (Fig. 2) such as those in the oil and gas industry or for changing the water flows in the shower. This micrometer-sized structure could inspire alternative valve technologies on a micrometer/nanometer scale. References [1] K. Yoshizawa et al. : Curr. Biol. 24 (2014) 1006. [2] K. Yoshizawa et al. : Biol. Lett. 14 (2018) 20180533. [3] Y. Kamimura and K. Yoshizawa: Sex Role Reversal in Encyclopedia of Animal Cognition and Behavior (Springer, 2007). [4] K. Yoshizawa, Y. Kamimura, C. Lienhard, R.L. Ferreira and A. Blanke: eLife 7 (2018) e39563. Kazunori Yoshizawa a, * and Alexander Blanke b a Systematic Entomology, School of Agriculture, Hokkaido University b Institute for Zoology, University of Cologne *Email: psocid@res.agr.hokudai.ac.jp F i g . 2 . M o r p h o l o g y o f t h e s p e r m a t h e c a a n d spermathecal plate of Neotrogla . (a) 3D segmentation of the spermathecal plate with no seminal capsule. Abbreviations. CE: closure element; Sc1 and 2: body sclerite 1 and 2. (b) 3D segmentation of the spermathecal plate with two seminal capsules and showing seminal flow. (c) Muscle attachment to CE. (d) Detail of CE. Fig. 3. Phylogeny of Psocodea and assumed history of character evolution related to the origin of female penis. (a) (b) (d) (c) suborder PSOCOMORPHA suborder TROCTOMORPHA other TROGIOMORPHA Afrotrogla Sensitibilla Neotrogla Speleketor Prionoglaridinae Sensitibillini order PSOCODEA • switching valve • donation of nutritious semen? female penis female penis suborder TROGIOMORPHA
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