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.

Centre for Applied Water Science Institute for Applied Ecology University of Canberra ACT Australia

Centre for Conservation Ecology and Genetics Institute for Applied Ecology University of Canberra ACT Australia

Department of Biology and Ecology Faculty of Science University of Ostrava Ostrava Czech Republic

Evolutionary Biology Unit South Australian Museum North Terrace Adelaide SA Australia

Laboratory of Fish Genetics Institute of Animal Physiology and Genetics Czech Academy of Sciences Liběchov Czech Republic

School of Biological Sciences The University of Adelaide SA Australia

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Gradual chromosomal lagging drive programmed genome elimination in hemiclonal fishes from the genus Hypseleotris

Inheritance patterns of male asexuality in hybrid males of a water frog Pelophylax esculentus

Meiotic deviations and endoreplication lead to diploid oocytes in female hybrids between bighead catfish (Clarias macrocephalus) and North African catfish (Clarias gariepinus)

A cyclical switch of gametogenic pathways in hybrids depends on the ploidy level

Cytogenetics of the Hybridogenetic Frog Pelophylax grafi and Its Parental Species Pelophylax perezi

Genomic evidence of paternal genome elimination in the globular springtail Allacma fusca

Genome elimination from the germline cells in diploid and triploid male water frogs Pelophylax esculentus