Diploid and aneuploid sperm in tetraploid ginbuna, Carassius auratus langsdorfii

Fumi Yamaguchi; Takafumi Fujimoto; Hiroko Suzuki; Hideki Tanaka; Masaru Murakami; Etsuro Yamaha; Katsutoshi Arai

doi:10.1016/j.theriogenology.2021.06.007

Diploid and aneuploid sperm in tetraploid ginbuna, Carassius auratus langsdorfii

Theriogenology. 2021 Sep 15:172:95-105. doi: 10.1016/j.theriogenology.2021.06.007. Epub 2021 Jun 8.

Authors

Fumi Yamaguchi¹, Takafumi Fujimoto², Hiroko Suzuki³, Hideki Tanaka³, Masaru Murakami⁴, Etsuro Yamaha⁵, Katsutoshi Arai⁶

Affiliations

¹ Faculty and Graduate School of Fisheries Sciences, Hokkaido University, Hakodate, Hokkaido, Japan. Electronic address: yamaguchi-fumi@hro.or.jp.
² Faculty and Graduate School of Fisheries Sciences, Hokkaido University, Hakodate, Hokkaido, Japan.
³ Gunma Prefectural Fisheries Experimental Station, Maebashi, Gunma, Japan.
⁴ School of Veterinary Medicine, Azabu University, Sagamihara, Kanagawa, Japan.
⁵ Nanae Fresh-Water Laboratory, Field Science Center for Northern Biosphere, Hokkaido University, Nanae, Hokkaido, Japan.
⁶ Faculty and Graduate School of Fisheries Sciences, Hokkaido University, Hakodate, Hokkaido, Japan; Institute for the Advancement of Higher Education, Hokkaido University, Sapporo, Hokkaido, Japan.

PMID: 34147877
DOI: 10.1016/j.theriogenology.2021.06.007

Abstract

Ginbuna (Carassius auratus langsdorfii (Teleostei: Cyprinidae)) occur in diploid, triploid, and tetraploid forms in wild populations. Diploid females reproduce bisexually, whereas polyploid (triploid and tetraploid) females reproduce gynogenetically with no contribution from sperm nuclei. However, tetraploid males produce diploid sperm. The mechanism responsible for the differences in egg and sperm ploidy has not been elucidated as tetraploid males are rare in wild populations. Here, we aimed to characterize the types of sperm and elucidate the mechanism of spermatogenesis in ginbuna. In the present study, we artificially produced tetraploid males by crossbreeding triploid ginbuna females with diploid goldfish (Carassius auratusauratus) males via accidental incorporation of sperm nuclei. We then examined spermatogenesis to reveal the process by which reduced diploid sperm are generated from tetraploid germ cells. DNA fingerprinting by random amplified polymorphic DNA (RAPD)-PCR indicated that the tetraploid progeny had a paternally derived genome. For the tetraploid male sperm, there were narrow (N-type) and broad (B-type) flow cytometrical histograms. The N-type were determined to be diploid with a low coefficient of variation (CV) by flow cytometry. The B-type were found to be aneuploid (hypodiploid to hexaploid) with a high CV. The head sizes of B-type sperm were variable, whereas those of the N-type sperm were uniform. Computer-assisted sperm analysis (CASA) revealed that both the haploid and diploid B-type sperm were weakly motile compared with the haploid sperm of goldfish and the diploid N-type sperm of tetraploid males. Bivalents and various multivalents were observed in the meiotic configurations of diploid spermatogenesis. In aneuploid spermatogenesis, most of the chromosomes were unpaired univalents and there were very few bivalents. Our findings provide empirical evidence for two different types of spermatogenesis in tetraploid C. a. langsdorfii males. Meiotic synapses might explain the observed differences in the ploidy status of the two sperm types.

Keywords: Aneuploidy; Computer-assisted sperm analysis; Meiosis; Polyploidy; Spermatogenesis; Unisexual species.

MeSH terms

Aneuploidy
Animals
Diploidy*
Female
Goldfish / genetics
Haploidy
Male
Polyploidy
Random Amplified Polymorphic DNA Technique / veterinary
Spermatozoa
Tetraploidy*
Triploidy