Morphological differences in tardigrade spermatozoa induce variation in gamete motility

Kenta Sugiura; Kogiku Shiba; Kazuo Inaba; Midori Matsumoto

doi:10.1186/s40850-022-00109-w

Morphological differences in tardigrade spermatozoa induce variation in gamete motility

BMC Zool. 2022 Jan 30;7(1):8. doi: 10.1186/s40850-022-00109-w.

Authors

Kenta Sugiura¹, Kogiku Shiba², Kazuo Inaba², Midori Matsumoto³

Affiliations

¹ Department of Biosciences and Informatics, Faculty of Science and Technology, Keio University, 3-14-1 Hiyoshi, Kohoku, Yokohama, Kanagawa, 223-8522, Japan.
² Shimoda Marine Research Center, University of Tsukuba, 5-10-1 Shimoda, Shizuoka, 415-0025, Japan.
³ Department of Biosciences and Informatics, Faculty of Science and Technology, Keio University, 3-14-1 Hiyoshi, Kohoku, Yokohama, Kanagawa, 223-8522, Japan. mmatsumo@bio.keio.ac.jp.

Abstract

Background: Fertilization is an event at the beginning of ontogeny. Successful fertilization depends on strategies for uniting female and male gametes that developed throughout evolutionary history. In some species of tardigrades, investigations of reproduction have revealed that released spermatozoa swim in the water to reach a female, after which the gametes are stored in her body. The morphology of the spermatozoa includes a coiled nucleus and a species-specific-length acrosome. Although the mating behaviour and morphology of tardigrades have been reported, the motility of male gametes remains unknown. Here, using a high-speed camera, we recorded the spermatozoon motilities of two tardigrades, Paramacrobiotus sp. and Macrobiotus shonaicus, which have longer and shorter spermatozoa, respectively.

Results: The movement of spermatozoa was faster in Paramacrobiotus sp. than in M. shonaicus, but the beat frequencies of the tails were equal, suggesting that the long tail improved acceleration. In both species, the head part consisting of a coiled nucleus and an acrosome did not swing, in contrast to the tail. The head part of Paramacrobiotus sp. spermatozoa swung harder during turning; in contrast, the tail of M. shonaicus moved more widely than the head. Finally, after mating, the spermatozoa that reached the female aggregated around the cloaca while waiting to enter her body in both tested species.

Conclusions: This study provides results for the first observations and analyses of individual spermatozoon motility in tardigrades. A comparison of the spermatozoon movements of the two tardigrades suggested that the motilities of the male gametes were affected by morphological differences, where the longer spermatozoa swam faster and the shorter ones showed more stable swimming. Swimming was mainly induced by tail movement, but the long head of Paramacrobiotus sp. spermatozoa might be especially important for turning. In addition, observations of mated female cloacae suggested that the head parts of the spermatozoa were required for aggregation around the cloaca of a mated female.

Keywords: Fertilization; Imaging; Macrobiotus shonaicus; Mating; Morphology; Motility; Paramacrobiotus sp; Reproduction; Spermatozoa; Tardigrade.