Interploidy gene flow involving the sexual-asexual cycle facilitates the diversification of gynogenetic triploid Carassius fish

Abstract

Asexual vertebrates are rare and at risk of extinction due to their restricted adaptability through the loss of genetic recombination. We explore the mechanisms behind the generation and maintenance of genetic diversity in triploid asexual (gynogenetic) Carassius auratus fish, which is widespread in East Asian fresh waters and exhibits one of the most extensive distribution among asexual vertebrates despite its dependence on host sperm. Our analyses of genetic composition using dozens of genetic markers and genome-wide transcriptome sequencing uncover admixed genetic composition of Japanese asexual triploid Carassius consisting of both the diverged Japanese and Eurasian alleles, suggesting the involvement of Eurasian lineages in its origin. However, coexisting sexual diploid relatives and asexual triploids in Japan show regional genetic similarity in both mitochondrial and nuclear markers. These results are attributed to a unique unidirectional gene flow from diploids to sympatric triploids, with the involvement of occasional sexual reproduction. Additionally, the asexual triploid shows a weaker population structure than the sexual diploid, and multiple triploid lineages coexist in most Japanese rivers. The generated diversity via repeated interploidy gene flow as well as an increased establishment of immigrants is assumed to offset the cost of asexual reproduction and might contribute to the successful broad distribution of this asexual vertebrate.

Changes in Ploidy Drive Reproduction Transition and Genomic Diversity in a Polyploid Fish Complex

“…Unisexual and sexual reproduction transition, which facilitates an increase in genetic diversity, has already been proposed in the polyploid Carassius species complex ( Lu et al 2021 ; Mishina et al 2021 ), and the complicated ecological and evolutionary impacts via the influence on the gene pool, diversification rate, and spatial distribution have also been suggested in some sexual and unisexual polyploid complexes ( Janko et al 2021 ). In this study, we provide comprehensive evidence that changes in ploidy, including from amphitriploid to amphitetraploid, then from amphitetraploid to novel amphitriploid, drive transition from unisexual to sexual reproduction and from sexual to unisexual reproduction, thereby leading to genomic and clonal diversity in the polyploid Carassius species complex.…”

“…Occasionally, a few individuals with higher ploidy, arising from accidental incorporation of a sperm nucleus from a sexual donor into a gynogenetic egg, were discovered in natural or reared populations of the Carassius complex ( Takai and Ojima 1983 ; Gui et al 1993 ; Li et al 2016b ; Lu et al 2018 ), and some of these males were found to produce diploid sperm ( Dong et al 2013 ; Lu et al 2021 ; Yamaguchi et al 2021 ). Although it has been assumed that these males contribute to the diversification of gynogenetic Carassius ( Lu et al 2021 ; Mishina et al 2021 ), the detailed biological process and the underlying mechanisms remain unknown.…”

Origin of scarlet gynogenetic triploid Carassius fish: Implications for conservation of the sexual–gynogenetic complex

“…auratus -complex populations in Hokkaido are believed to be derived from Honshu Island [ 29 ], it is still unclear whether they are indigenous or not. Recent extensive phylogeographic study, however, reported that the genetic characteristics of Hokkaido populations are close to those of northern Honshu (Tohoku region), but with distinct private mitochondrial haplotype groups, suggesting previous northward colonization of this species complex across Tsugaru Strait [ 11 ].…”

“…In addition, we compared the nuclear genetic characteristics of Hibuna with those of previously reported wild C . auratus -complex specimens [ 11 ] collected on Hokkaido, in Tohoku, and in the Yellow River of mainland China ( Fig 1A ).…”

“…auratus -complex [ 11 ]. This interploidy gene flow is probably derived from the recurring offspring of gynogenetic triploids that may result from mating between sexual female diploids and tetraploid males, which are produced by rare fertilization of triploid eggs with the sperm of a diploid male [ 11 , 24 , 25 ]. However, crossing experiments to confirm this interploidy gene flow have not yet been reported.…”