Progesterone initiates tendril formation in the oviducal gland during egg encapsulation in cloudy catshark (Scyliorhinus torazame)

Koya Shimoyama; Mai Kawano; Nobuhiro Ogawa; Kotaro Tokunaga; Wataru Takagi; Makito Kobayashi; Susumu Hyodo

doi:10.1186/s40851-023-00211-y

Progesterone initiates tendril formation in the oviducal gland during egg encapsulation in cloudy catshark (Scyliorhinus torazame)

Zoological Lett. 2023 May 30;9(1):13. doi: 10.1186/s40851-023-00211-y.

Authors

Koya Shimoyama¹, Mai Kawano², Nobuhiro Ogawa², Kotaro Tokunaga³, Wataru Takagi², Makito Kobayashi⁴, Susumu Hyodo²

Affiliations

¹ Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba, 277-8564, Japan. shimoyama@g.ecc.u-tokyo.ac.jp.
² Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba, 277-8564, Japan.
³ Ibaraki Prefectural Oarai Aquarium, Oarai, Ibaraki, 311-1301, Japan.
⁴ Department of Natural Sciences, International Christian University, Tokyo, 181-8585, Japan.

Abstract

The diverse reproductive strategies of elasmobranchs (sharks, rays, and skates) have attracted research attention, but the endocrine control of reproduction is still incompletely known in elasmobranchs. By long-term monitoring of the egg-laying cycle in cloudy catsharks (Scyliorhinus torazame), we recently demonstrated a transient increase in plasma progesterone (P4) levels just prior to the appearance of the capsulated eggs in the oviducts. In the present study, we examined the in vivo effects of P4 administration in mature female cloudy catsharks. Although no capsulated eggs were observed following the implantation of P4-containing silicone tubing, we did find dark swollen oviducts in the abdominal cavity, in which clumps of long and coiled tendrils were observed. The tendril is an extension of the egg capsule, and the formation of the egg capsule begins with the tendril before main capsule formation. During the period of P4 implantation, the tendrils elongated, and their diameters were significantly increased on day 2 of treatment. Tendril formation was also confirmed on the day of endogenous P4 surge. Tendrils were not formed in catsharks implanted with estradiol-17β or testosterone. Histological analysis of the oviducal gland revealed that P4 implantation induced the secretion of tendril materials from the secretory tubules in the baffle zone, while the tendril materials were stored in the cytoplasm of the secretory cells under low P4 condition. Morphometrically, the area of secreted luminal materials in the secretory tubules was highly correlated to the diameter of tendrils. Our results suggest that the P4 surge during the egg-laying cycle serves as a trigger for egg capsule formation in the oviducal gland of cloudy catshark, but the hormonal signals were incomplete as the main capsule was not formed. Further studies are required to identify the hormones required for ovulation and formation of the main egg capsule.

Keywords: Catshark; Collagen secretion; Egg-capsule formation; Egg-laying cycle; Elasmobranchs; Progesterone; Sex steroid.

Grants and funding

JSPS KAKENHI 19K22414/Japan Society for the Promotion of Science