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Is the copulation of silver-washed fritillary inverted? Function of the female genital projection (Lepidoptera: Nymphalidae: Argynnini)

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Abstract

Females of the silver-washed fritillary butterfly, Argynnis paphia (Linnaeus), and its relatives are known to have a unique genital projection called the cornucopia. Previous observations showed that the cornucopia partly penetrates the male genitalia during copulation, but its detailed structures and functions are unknown to date. Our observations using light microscopy, confocal laser scanning microscopy, scanning electron microscopy, and microcomputed tomography suggested that penetration by the female cornucopia occurs passively, and it is hooked and pulled by the male towards the male genitalia using sharp teeth on the uncus. This hooking and pulling causes wounds on the dorsal region of the cornucopia. Artificial amputation of a cornucopia confirmed that it is indispensable for spermatophore transfer from males and functions to break off the male phallic spines (cornuti). The broken spines may be used by females to help the digestion of spermatophores in the female’s corpus bursae. Females with larger body sizes had more broken spines in the corpus bursae, indicating that secure holding of a large female during copulation is challenging for males.

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Data availability

The statistical data generated or analyzed during this study are included in the online supplementary files. Scanned µCT images (zip file) are available from Figshare at 10.6084/m9.figshare.21992420.

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Acknowledgments

We thank Toyohei Saigusa and Takashi Adachi‑Yamada for valuable advice about rearing and collection of the butterflies, and Akihisa Takeuchi and Masayuki Uesugi for their support at SPring-8. The research at SPring-8 was approved through project number 2022A1201 to KY. We also thank Thomas J. Simonsen and an anonymous reviewer for their constructive comments. This study was partly supported by JSPS grant numbers 15H04409 and 19H03278 to KY and 15K07133 to YK. This study was conducted to fulfill the master's degree of TM, who thanks Shin-ichi Akimoto and Masahiro Ohara for their continuous guidance.

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YK and KY conceived the project. TM designed the experiments, collected specimens, analyzed morphology, and performed experiments. KY performed µCT analysis. YK performed SEM imaging and statistical analyses. All authors wrote and approved the final manuscript.

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Correspondence to Kazunori Yoshizawa.

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Matoba, T., Kamimura, Y. & Yoshizawa, K. Is the copulation of silver-washed fritillary inverted? Function of the female genital projection (Lepidoptera: Nymphalidae: Argynnini). Org Divers Evol 23, 871–879 (2023). https://doi.org/10.1007/s13127-023-00621-y

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