Parthenogenesis as a Solution to Hybrid Sterility: The Mechanistic Basis of Meiotic Distortions in Clonal and Sterile Hybrids

Abstract

Hybrid sterility is a hallmark of speciation, but the underlying molecular mechanisms remain poorly understood. Here, we report that speciation may regularly proceed through a stage at which gene flow is completely interrupted, but hybrid sterility occurs only in male hybrids whereas female hybrids reproduce asexually. We analysed gametogenic pathways in hybrids between the fish species Cobitiselongatoides and C. taenia and revealed that male hybrids were sterile owing to extensive asynapsis and crossover reduction among heterospecific chromosomal pairs in their gametes, which was subsequently followed by apoptosis. We found that polyploidization allowed pairing between homologous chromosomes and therefore partially rescued the bivalent formation and crossover rates in triploid hybrid males. However, it was not sufficient to overcome sterility. In contrast, both diploid and triploid hybrid females exhibited premeiotic genome endoreplication, thereby ensuring proper bivalent formation between identical chromosomal copies. This endoreplication ultimately restored female fertility but it simultaneously resulted in the obligate production of clonal gametes, preventing any interspecific gene flow. In conclusion, we demonstrate that the emergence of asexuality can remedy hybrid sterility in a sex-specific manner and contributes to the speciation process.

Uniparental Genome Elimination in Australian Carp Gudgeons

“…Previous studies have shown that the hybrid male’s sterility is caused by the inability to modify their gametogenesis in order to achieve clonality as females do. In this respect, males have problems with orthologous pairing in meiosis ( Kuroda et al 2019 ; Dedukh, Majtánová, et al 2020 ; Spangenberg et al 2017 ). Our analysis of gonadal microanatomy and flow cytometry did not indicate any aberration in male and female fertility, as both of them exhibited normal gonads with cells on various gametogenic stages.…”

Sex chromosomes in meiotic, hemiclonal, clonal and polyploid hybrid vertebrates: along the ‘extended speciation continuum'

“…inverted meiosis in butterflies [ 180 ]). Likewise, clonal gametogenic pathways, as premeiotic endoreplication, may also enable hybrids to successfully pass meiotic checkpoints [ 66 ] and to transmit at least parts of their genomes, despite the problems they experience with postzygotic incompatibilities [ 35 ]. Processes involving some type of hybrid-origin clonality allow the existence of hybrid vertebrates in the ‘extended speciation continuum’.…”

“…like in gynogenesis (middle), be truly fertilized, leading to ploidy elevation of offspring (left), or sperm may in part replace one of the maternal genomes in the egg, followed by its partial elimination (right) [ 54 ]. Gynogenesis (upper and lower rows): formation of clonal gametes by an ameiotic process (example: Poecilia formosa , upper row [ 47 , 64 ]; example: Carassius langsdorfii , lower row [ 65 ]) or endoreplication (example: diploid Cobitis elongatoides-taenia , upper row [ 66 , 67 ]; example: triploid Cobitis 1elongatoides-2taenia , lower row [ 66 – 68 ]) of genomes in germ cells followed by meiosis without effects of recombination. Diploid gametes (upper row) or triploid gametes (lower row) are fertilized without karyogamy, followed by sperm genome elimination.…”

Sperm motility analysis of Cobitis hankugensis, Iksookimia longicorpa (Teleostei, Cypriniformes, Cobitidae) and their unisexual natural hybrids

“…Moreover, their fertility was differed by sexes: females are fertile but males are sterile (Pandian, 2010). Recently, Dedukh et al (2020) described this underlying mechanism in a study using C. taenia hybrids as follows:…”