Abstract

Autopolyploids are traditionally used to demonstrate multivalent pairing and unstable inheritance. However, the autotetraploid fish (4nRR) (RRRR, 4n = 200) derived from the distant hybridization of Carassius auratus red var. (RCC) (RR, 2n = 100) (♀) × Megalobrama amblycephala (BSB) (BB, 2n = 48) (♂) exhibits chromosome number (or ploidy) stability over consecutive generations (F1–F10). Comparative analysis based on somatic and gametic chromosomal loci [centromeric, 5S rDNA, and Ag-NORs (silver-stained nucleolar organizer regions)] revealed that a substantial loss of chromosomal loci during genome doubling increases the divergence between homologous chromosomes and that diploid-like chromosome pairing was restored during meiosis in the first generation of 4nRR lineages. In addition, a comparative analysis of genomes and transcriptomes from 4nRR (F1) and its diploid progenitor (RCC) exhibited significant genomic structure and gene expression changes. From these data, we suggest that genomes and genes diverge and that expression patterns change in the first generations following autotetraploidization, which are processes that might contribute to the stable inheritance and successful establishment of autotetraploid lineages.

Highlights

  • Polyploidy has played an important role in the evolutionary history of vertebrates and other eukaryotes (Masterson 1994; Comai 2005; Mallet 2007; Otto 2007; Rieseberg and Willis 2007; Wood et al 2009)

  • All the fish were cultured in ponds at the Protection Station of Polyploid Fish, Hunan Normal University, and fed with artificial feed

  • To understand the genomic changes that occur during genome doubling, autodiploid gynogenetic progeny (2nG) (RR, 2n = 100) was produced by artificial gynogenesis from autodiploid 4nRB eggs (RR, 2n = 100) that were activated with UV-treated sterilized BSB sperm without treatment for chromosome doubling (Fig. 1)

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Summary

Introduction

Polyploidy has played an important role in the evolutionary history of vertebrates and other eukaryotes (Masterson 1994; Comai 2005; Mallet 2007; Otto 2007; Rieseberg and Willis 2007; Wood et al 2009). Because an additional set (or sets) of chromosomes may originate from the same or different species, polyploids have been classified into two major categories: autopolyploids and allopolyploids The original version of this article was revised due to a retrospective Open Access order. Multivalent pairing can cause meiotic irregularities and result in reduced fertility compared with the diploid progenitors (Parisod 2010). Autopolyploids were believed to suffer from several evolutionary disadvantages compared with allopolyploids and were considered rare evolutionary dead-ends (Otto 2007; Soltis and Soltis 2010). Accumulating evidence indicates that the actual appearance of autotetraploid species might be significantly underestimated and that autopolyploidy might contribute more to evolution and species diversification than traditionally thought (Barker et al 2016)

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