Tempo and mode of recurrent polyploidization in the Carassius auratus species complex (Cypriniformes, Cyprinidae)

Abstract

Polyploidization is an evolutionarily rare but important mechanism in both plants and animals because it increases genetic diversity. Goldfish of the Carassius auratus species complex can be tetraploids, hexaploids and octaploids. Polyploidization events have occurred repeatedly in goldfish, yet the extent of this phenomenon and its phyletic history are poorly understood. We explore the origin, tempo and frequency of polyploidization in Chinese and Japanese goldfish using both mitochondrial (mtDNA) and nuclear DNA sequences from up to 1202 individuals including the outgroup taxon, Cyprinus carpio. Analyses of de novo nuclear gene data resolve two clusters of alleles and the pattern supports the prior hypothesis of an ancient allotetraploidization for Carassius. Alleles shared by tetraploid and hexaploid individuals indicate recent autoploidizations within the C. auratus complex. Sympatric tetraploids and hexaploids share mtDNA haplotypes and these frequently occur independently within six well-supported lineages and sublineages on a small spatial scale. Gene flow estimates (F st values) indicate that hexaploids differ only slightly from sympatric tetraploids, if at all. In contrast, allopatric populations of tetraploids and hexaploids differ from one another to a far greater extent. Gene flow between sampled localities appears to be limited. Coalescence-based time estimations for hexaploids reveal that the oldest lineage within any sampled locality is around one million years old, which is very young. Sympatric, recurrent autoploidization occurs in all sampled populations of the C. auratus complex. Goldfish experience polyploidization events more frequently than any other vertebrate.

Numerous mitochondrial DNA haplotypes reveal multiple independent polyploidy origins of hexaploids in Carassius species complex

“…A total of 3,105 individuals of the Carassius species complex were currently sampled from 34 locations through mainland China. And the other 1,054 sample data of Carassius species complex from 15 localities in East Asia were collected from previous reports (Luo et al., ; Takada et al., ). Details about all the samples, sampling sites, and references are given in Table .…”

“…Tetraploids with 100 chromosomes are diploidizated allotetraploids that reproduce by sexual reproduction (Luo, Stadler, He, & Meyer, ; Ohno, Muramoto, Christian, & Atkin, ), while hexaploids with about 150 chromosomes are able to reproduce by dual modes including unisexual gynogenesis and bisexual reproduction (Gui & Zhou, ; Gui & Zhu, ; Zhou, Wang, & Gui, ), and octaploids reproduce only via unisexual gynogenesis (Xiao et al., ; Zhu & Gui, ). Recently, an early allopolyploidy event leading to ancestral allotetraploids has been revealed, and a recurrent autopolyploidy from allotetraploids that results in allohexaploids has been elucidated in the Carassius species complex (Li, et al., ; Luo et al., ). Therefore, the wide geographic distribution, coexistence of different ploidy forms, and occurrence of repeated polyploidy events make the Carassius species complex an ideal system to investigate evolutionary trajectory and ecological adaption of polyploidy in vertebrates (Gao et al., ; Liu et al., ).…”

Autotriploid origin of Carassius auratus as revealed by chromosomal locus analysis

“…However, to our knowledge, to date, there was no direct genetic evidence for this. Although analyses of both mitochondrial and nuclear DNA sequences have revealed that recurrent autoploidization occurs in all sampled populations of the C. auratus complex (Luo et al, 2014), our most important finding was the direction of cytogenetic evidence for the autotriploid origin of C. auratus with 150 chromosomes. What was the possible origin of the autotriploid forms in the C. auratus complex?…”

“…Thus, it has been assumed that C. carpio and C. auratus have undergone a fourth round of genome duplication (Luo et al, 2007;Wang et al, 2012). In recent years, many studies have revealed that polyploid C. auratus have undergone several successive rounds of genome polyploidy and that they have experienced an additional, more recent genome duplication event (Gui and Zhou, 2010;Li et al, 2014;Luo et al, 2014). In the Dongting water system, the C. auratus complex is characterized by the coexistence of diploids (2nCC) and polyploids (3nCC and 4nCC), which are quite similar morphologically but differ markedly in their modes of reproduction (Koboyasi, 1971;Mezhzherin and Kokodiy, 2010;Yang et al, 1992).…”

“…Thus, C. auratus is also characterized by the coexistence of diploids and polyploids. In C. auratus complex populations (Jakovlić and Gui, 2011;Jiang et al, 2013;Luo et al, 2014), the diploids and the polyploids are quite similar morphologically, but differ markedly in their modes of reproduction. The diploid form reproduces sexually, whereas the polyploid form has dual reproduction modes, with both unisexual gynogenesis and sexual reproduction (Koboyasi, 1971;Mezhzherin and Kokodiy, 2010;Yang et al, 1992).…”