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.
Highlights
Asexual vertebrates are rare and at risk of extinction due to their restricted adaptability through the loss of genetic recombination
One type of asexual reproduction found in vertebrates is gynogenesis, in which offspring are formed parthenogenetically, yet egg development cannot be completed without sperm from a related bisexual species that degenerates without fusing with the egg n ucleus[3]
Integrating the dataset of nuclear loci obtained by target resequencing and transcriptomes, mitochondrial sequences, microsatellites and morphological measurements generated from geographically comprehensive specimens (Supplementary Fig. S1, Table S1), we address two main questions: (i) did gynogenetic triploid Carassius originate from hybridization? most asexual vertebrates are of hybrid o rigin[15], there are two hypothetical scenarios for the origin of the Japanese gynogenetic triploid Carassius—one is the hybrid origin implied by the different genetic characteristics between Japanese diploids and gynogenetic triploids (e.g., allozyme21; RAPD28), and the other is autotriploidization, i.e., the occurrence of triploid individuals from a single diploid p opulation[27,29]
Summary
Asexual vertebrates are rare and at risk of extinction due to their restricted adaptability through the loss of genetic recombination. Much attention has been focused on the C. auratus-complex exhibiting sexual and gynogenetic reproduction associated with ploidy polymorphism (sexual diploid, gynogenetic triploid, and rare tetraploid)[20,21] This gynogenetic triploid is one of the most widespread asexual vertebrates, which is distributed in and around Eurasia, including Taiwan and the Japanese islands, and uses sympatric sexual diploid Carassius fish as sperm donors[20,22]. Phylogenetic studies on mitochondrial DNA reported that sexual diploids and gynogenetic triploids shared various mitochondrial haplotypes over diverged clades in wide ranges of East Asian freshwaters[26,27] These results indicate underlying mechanisms that facilitate genetic diversity or multiple autotriploidization-like origins from sexual diploid populations despite the extreme rarity of asexual v ertebrates[3]
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