Histological evidence that diploid hybrids of Cobitis taenia and C. elongatoides (Teleostei, Cobitidae) develop into fertile females and sterile males

Juchno, Dorota; Boroń, Alicja

doi:10.1007/s10750-018-3530-2

Cited by 10 publications

(15 citation statements)

References 31 publications

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“…Hybrid sterility and asexuality evolves in a sex specific manner: Mechanistically, reproductive incapacity of hybrid males is reflected by defective development of hybrid testes as evidenced by histological examination of diploid ET ( [23], this study) and triploid ETT hybrid males (this study). The…”

Section: Resultsmentioning

confidence: 85%

“…Reproductive experiments and histological observations showed that C. elongatoides-taenia hybrid females (both diploid and triploid, naturally occurring as well as artificial F1 strains) are fertile and reproduce clonally by spermdependent parthenogenesis, known as gynogenesis (i.e. they produce unreduced eggs but require sperm to activate cellular division; [9,[20][21][22][23]. Occasional fusion of sperm with hybrid egg pronuclei results in triploid progeny with EET or ETT genomic constitution.…”

Section: Introductionmentioning

confidence: 99%

“…Occasional fusion of sperm with hybrid egg pronuclei results in triploid progeny with EET or ETT genomic constitution. In contrast to their clonal sisters, the male hybrids have drastically reduced reproductive capabilities and appear incapable either of fertilizing the normal haploid eggs or of triggering the development of the clonal eggs [21,23,24]. Any interspecific gene flow is thus prevented by clonality (females) or sterility (males) of contemporary hybrids.…”

Section: Introductionmentioning

confidence: 99%

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Parthenogenesis as a solution to hybrid sterility: the mechanistic basis of meiotic distortions in clonal and sterile hybrids

Dedukh

Majtánová

Marta

et al. 2019

Preprint

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Formation of species generally occurs in a continuum from potentially intermixing populations to independent entities isolated from other species by pre-and postzygotic barriers. Especially the establishment of hybrid sterility (HS) is a hallmark of speciation, which usually emerges at different rates between hybrid sexes. However, although HS is frequently observed, the underlying molecular mechanisms remain poorly understood. Here we report that speciation proceeds through a previously unnoticed stage at which gene flow is completely interrupted on side of both hybrid's sexes, although only male hybrids are sterile, while female fertility is rescued due to a particular gametogenetic deviation leading to the formation of clonal gametes. Specifically, analysis of gametogenetic pathways in hybrids between fish species Cobitis elongatoides and C. taenia revealed that male HS resulted from extensive asynapses and crossover reduction among elongatoides-taenia chromosomal pairs followed by apoptosis. By contrast, hybrid females exhibited premeiotic genome endoreplication which ensured proper formation of bivalents between identical chromosomal copies. This deviation ultimately restored fertility in females but since it simultaneously leads to the production of unreduced clonal gametes, it restricts interspecific gene flow thereby directly contributing to speciation. In conclusion, our data demonstrate that the emergence of asexuality may remedy HS in a sex-specific manner and is intermingled with the speciation process. Although gametogenetic mechanisms employed by asexual animals and plants have rarely been scrutinized, available evidence suggests that premeiotic endoreplication is relatively widespread. This suggests that observed link between HS and clonality may have general validity in taxa able of asexual reproduction. Author's summarySpecies are fundamental evolutionary units that presumably evolve in a continuum from potentially intermixing populations to independent entities isolated from other species by pre-and postzygotic barriers. Especially the establishment of hybrid sterility (HS) is a hallmark of speciation, which usually emerges at different rates between hybrid sexes. However, although HS is frequently observed, the underlying molecular mechanisms remain poorly understood. Here we report the existence of a previously unnoticed stage of speciation at which gene flow is completely interrupted, although only male hybrids are sterile, while female fertility is rescued due to a particular gametogenetic deviation leading to formation of clonal gametes. Specifically, HS resulted from extensive asynapses in male gonads, but in females the hybridization provoked premeiotic endoreplication which rescued chromosome pairing and fertility. Simultaneously, this meiotic deviation caused clonal transmission of maternal genome, thereby effectively restricting the interspeficic gene flow. Our results emphasize that emergence of clonality is a type of hybrid incompatibility that is intermingled with the formation of b...

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Section: Resultsmentioning

confidence: 85%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Parthenogenesis as a solution to hybrid sterility: the mechanistic basis of meiotic distortions in clonal and sterile hybrids

Dedukh

Majtánová

Marta

et al. 2019

Preprint

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“…Reproductive experiments and histological observations have shown that C. elongatoides × C. taenia hybrid females (ET, 49 chromosomes) reproduce clonally through sperm-dependent gynogenesis, producing only female hybrid progeny ( i.e. , they produce unreduced eggs but require sperm to activate cellular division; summarized in Figure 1A ; Janko et al 2007a , 2018 ; Choleva et al 2012 ; Juchno et al 2017 ; Juchno and Boroń 2018 ). The occasional fusion of sperm with hybrid egg pronuclei results in triploid progeny of both sexes with EET (74 chromosomes) or ETT (73 chromosomes) genomic constitutions, but only females are able to clonally propagate ( Figure 1A ).…”

mentioning

confidence: 99%

“…The occasional fusion of sperm with hybrid egg pronuclei results in triploid progeny of both sexes with EET (74 chromosomes) or ETT (73 chromosomes) genomic constitutions, but only females are able to clonally propagate ( Figure 1A ). In contrast to their clonal sisters, the diploid (ET) and triploid (EET and ETT) male hybrids have drastically reduced reproductive capabilities, and appear to be incapable of either fertilizing normal haploid eggs or triggering the development of clonal eggs ( Figure 1A ) ( Vasil’ev et al 2003 ; Choleva et al 2012 ; Juchno and Boroń 2018 ).…”

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confidence: 99%

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

et al. 2020

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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.

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

2021

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Hybrid sterility is an inevitable phenomenon in the speciation process to avoid indiscriminate increases in species, but it is not always unconditional. We used computer assisted sperm analysis (CASA) to analyze sperm motility of Cobitis hankugensis, Iksookimia longicorpa, and their unisexual natural hybrids. In parental species, the sperm concentrations of C. hankugensis and I. longicorpa were 11.6 ± 4.8 × 10 9 and 16.5 ± 6.8 × 10 9 , respectively. For sperm motility, the total motility was higher in the parental species (C. hankugensis, 91.3%; I. longicorpa, 87.5%) than other hybrids. After 1 min, the motility duration was reduced to 14% in C. hankugensis and 3.3% in I. longicorpa. This result could indicate that the duration of sperm motility of C. hankugensis is longer than that of

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Histological evidence that diploid hybrids of Cobitis taenia and C. elongatoides (Teleostei, Cobitidae) develop into fertile females and sterile males

Cited by 10 publications

References 31 publications

Parthenogenesis as a solution to hybrid sterility: the mechanistic basis of meiotic distortions in clonal and sterile hybrids

Parthenogenesis as a solution to hybrid sterility: the mechanistic basis of meiotic distortions in clonal and sterile hybrids

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

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

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