Versatility of multivalent orientation, inverted meiosis, and rescued fitness in holocentric chromosomal hybrids

Vladimir A. Lukhtanov, Vlad Dinca, Magne Friberg, Jindra Síchová, Martin Olofsson, Roger Vila, Frantisek Marec, Christer Wiklund

Результат исследований: Научные публикации в периодических изданияхстатьянаучнаярецензирование

6 Цитирования (Scopus)

Выдержка

Chromosomal rearrangements (e.g., fusions/fissions) have the potential to drive speciation. However, their accumulation in a population is generally viewed as unlikely, because chromosomal heterozygosity should lead to meiotic problems and aneuploid gametes. Canonical meiosis involves segregation of homologous chromosomes in meiosis I and sister chromatid segregation during meiosis II. In organisms with holocentric chromosomes, which are characterized by kinetic activity distributed along almost the entire chromosome length, this order may be inverted depending on their metaphase I orientation. Here we analyzed the evolutionary role of this intrinsic versatility of holocentric chromosomes, which is not available to monocentric ones, by studying F1 to F4 hybrids between two chromosomal races of the Wood White butterfly (Leptidea sinapis), separated by at least 24 chromosomal fusions/fissions. We found that these chromosomal rearrangements resulted in multiple meiotic multivalents, and, contrary to the theoretical prediction, the hybrids displayed relatively high reproductive fitness (42% of that of the control lines) and regular behavior of meiotic chromosomes. In the hybrids, we also discovered inverted meiosis, in which the first and critical stage of chromosome number reduction was replaced by the less risky stage of sister chromatid separation. We hypothesize that the ability to invert the order of the main meiotic events facilitates proper chromosome segregation and hence rescues fertility and viability in chromosomal hybrids, potentially promoting dynamic karyotype evolution and chromosomal speciation.

Язык оригиналаанглийский
Страницы (с-по)E9610-E9619
ЖурналProceedings of the National Academy of Sciences of the United States of America
Том115
Номер выпуска41
DOI
СостояниеОпубликовано - 9 окт 2018

Отпечаток

Meiosis
Chromosomes
Chromosome Segregation
Chromatids
Siblings
Sinapis
Genetic Fitness
Butterflies
Aptitude
Aneuploidy
Metaphase
Karyotype
Germ Cells
Fertility
Population

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Lukhtanov, Vladimir A. ; Dinca, Vlad ; Friberg, Magne ; Síchová, Jindra ; Olofsson, Martin ; Vila, Roger ; Marec, Frantisek ; Wiklund, Christer. / Versatility of multivalent orientation, inverted meiosis, and rescued fitness in holocentric chromosomal hybrids. В: Proceedings of the National Academy of Sciences of the United States of America. 2018 ; Том 115, № 41. стр. E9610-E9619.
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abstract = "Chromosomal rearrangements (e.g., fusions/fissions) have the potential to drive speciation. However, their accumulation in a population is generally viewed as unlikely, because chromosomal heterozygosity should lead to meiotic problems and aneuploid gametes. Canonical meiosis involves segregation of homologous chromosomes in meiosis I and sister chromatid segregation during meiosis II. In organisms with holocentric chromosomes, which are characterized by kinetic activity distributed along almost the entire chromosome length, this order may be inverted depending on their metaphase I orientation. Here we analyzed the evolutionary role of this intrinsic versatility of holocentric chromosomes, which is not available to monocentric ones, by studying F1 to F4 hybrids between two chromosomal races of the Wood White butterfly (Leptidea sinapis), separated by at least 24 chromosomal fusions/fissions. We found that these chromosomal rearrangements resulted in multiple meiotic multivalents, and, contrary to the theoretical prediction, the hybrids displayed relatively high reproductive fitness (42{\%} of that of the control lines) and regular behavior of meiotic chromosomes. In the hybrids, we also discovered inverted meiosis, in which the first and critical stage of chromosome number reduction was replaced by the less risky stage of sister chromatid separation. We hypothesize that the ability to invert the order of the main meiotic events facilitates proper chromosome segregation and hence rescues fertility and viability in chromosomal hybrids, potentially promoting dynamic karyotype evolution and chromosomal speciation.",
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Versatility of multivalent orientation, inverted meiosis, and rescued fitness in holocentric chromosomal hybrids. / Lukhtanov, Vladimir A.; Dinca, Vlad; Friberg, Magne; Síchová, Jindra; Olofsson, Martin; Vila, Roger; Marec, Frantisek; Wiklund, Christer.

В: Proceedings of the National Academy of Sciences of the United States of America, Том 115, № 41, 09.10.2018, стр. E9610-E9619.

Результат исследований: Научные публикации в периодических изданияхстатьянаучнаярецензирование

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T1 - Versatility of multivalent orientation, inverted meiosis, and rescued fitness in holocentric chromosomal hybrids

AU - Lukhtanov, Vladimir A.

AU - Dinca, Vlad

AU - Friberg, Magne

AU - Síchová, Jindra

AU - Olofsson, Martin

AU - Vila, Roger

AU - Marec, Frantisek

AU - Wiklund, Christer

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N2 - Chromosomal rearrangements (e.g., fusions/fissions) have the potential to drive speciation. However, their accumulation in a population is generally viewed as unlikely, because chromosomal heterozygosity should lead to meiotic problems and aneuploid gametes. Canonical meiosis involves segregation of homologous chromosomes in meiosis I and sister chromatid segregation during meiosis II. In organisms with holocentric chromosomes, which are characterized by kinetic activity distributed along almost the entire chromosome length, this order may be inverted depending on their metaphase I orientation. Here we analyzed the evolutionary role of this intrinsic versatility of holocentric chromosomes, which is not available to monocentric ones, by studying F1 to F4 hybrids between two chromosomal races of the Wood White butterfly (Leptidea sinapis), separated by at least 24 chromosomal fusions/fissions. We found that these chromosomal rearrangements resulted in multiple meiotic multivalents, and, contrary to the theoretical prediction, the hybrids displayed relatively high reproductive fitness (42% of that of the control lines) and regular behavior of meiotic chromosomes. In the hybrids, we also discovered inverted meiosis, in which the first and critical stage of chromosome number reduction was replaced by the less risky stage of sister chromatid separation. We hypothesize that the ability to invert the order of the main meiotic events facilitates proper chromosome segregation and hence rescues fertility and viability in chromosomal hybrids, potentially promoting dynamic karyotype evolution and chromosomal speciation.

AB - Chromosomal rearrangements (e.g., fusions/fissions) have the potential to drive speciation. However, their accumulation in a population is generally viewed as unlikely, because chromosomal heterozygosity should lead to meiotic problems and aneuploid gametes. Canonical meiosis involves segregation of homologous chromosomes in meiosis I and sister chromatid segregation during meiosis II. In organisms with holocentric chromosomes, which are characterized by kinetic activity distributed along almost the entire chromosome length, this order may be inverted depending on their metaphase I orientation. Here we analyzed the evolutionary role of this intrinsic versatility of holocentric chromosomes, which is not available to monocentric ones, by studying F1 to F4 hybrids between two chromosomal races of the Wood White butterfly (Leptidea sinapis), separated by at least 24 chromosomal fusions/fissions. We found that these chromosomal rearrangements resulted in multiple meiotic multivalents, and, contrary to the theoretical prediction, the hybrids displayed relatively high reproductive fitness (42% of that of the control lines) and regular behavior of meiotic chromosomes. In the hybrids, we also discovered inverted meiosis, in which the first and critical stage of chromosome number reduction was replaced by the less risky stage of sister chromatid separation. We hypothesize that the ability to invert the order of the main meiotic events facilitates proper chromosome segregation and hence rescues fertility and viability in chromosomal hybrids, potentially promoting dynamic karyotype evolution and chromosomal speciation.

KW - Chromosomal evolution

KW - Chromosomal rearrangement

KW - Hybridization

KW - Inverted meiosis

KW - Speciation

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