Abstract

Metazoans usually reproduce sexually, blending the unique identity of parental genomes for the next generation through functional crossing-over and recombination in meiosis. However, some metazoan lineages have evolved reproductive systems where offspring are either full (clonal) or partial (hemiclonal) genetic replicas. In the latter group, the process of uniparental genome elimination selectively eliminates either the maternal or paternal genome from germ cells, and only one parental genome is selected for transmission. Although fairly common in plants, hybridogenesis (i.e., clonal haploidization via chromosome elimination) remains a poorly understood process in animals. Here, we explore the proximal cytogenomic mechanisms of somatic and germ cell chromosomes in sexual and hybrid genotypes of Australian carp gudgeons (Hypseleotris) by tracing the fate of each set during mitosis (in somatic tissues) and meiosis (in gonads). Our comparative study of diploid hybrid and sexual individuals revealed visually functional gonads in male and female hybrid genotypes and generally high karyotype variability, although the number of chromosome arms remains constant. Our results delivered direct evidence for classic hybridogenesis as a reproductive mode in carp gudgeons. Two parental sets with integral structure in the hybrid soma (the F1 constitution) contrasted with uniparental chromosomal inheritance detected in gonads. The inheritance mode happens through premeiotic genome duplication of the parental genome to be transmitted, whereas the second parental genome is likely gradually eliminated already in juvenile individuals. The role of metacentric chromosomes in hybrid evolution is also discussed.

Highlights

  • The great majority of metazoan organisms reproduce through sex in a two-stage process, commencing with meiosis in each parent and culminating in the fusion of one ploidy-reduced, genetically shuffled gamete from each parent into a single zygote (Crow and Kimura 1965; Kondrashov 1988)

  • Five sexual species have been recognized in eastern Australia: two, Hypseleotris compressa and H. klunzingeri frequently co-occur with the sexual/unisexual complex, but there is no record of them being involved in any hybridization

  • Our results suggest that genome elimination has already occurred via micronuclei formation before meiosis commences in juvenile carp gudgeons

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Summary

Introduction

The great majority of metazoan organisms reproduce through sex in a two-stage process, commencing with meiosis in each parent and culminating in the fusion of one ploidy-reduced, genetically shuffled gamete from each parent into a single zygote (Crow and Kimura 1965; Kondrashov 1988). In sexual reproduction, both paternal and maternal genomes enter meiosis. The resulting haploid gametes contain a unique cocktail of recombinant chromosomal DNA from the mother and father In this way reproducing animals we call “sexual.” the meiotic molecular machinery is highly conserved ß The Author(s) 2021.

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