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

Lukhtanov, Vladimir A. ; Dinca, Vlad ; Friberg, Magne LU ; Síchová, Jindra ; Olofsson, Martin ; Vila, Roger ; Marec, Frantisek and Wiklund, Christer (2018) In Proceedings of the National Academy of Sciences of the United States of America 115(41). p.9610-9619
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... (More)

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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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Chromosomal evolution, Chromosomal rearrangement, Hybridization, Inverted meiosis, Speciation
in
Proceedings of the National Academy of Sciences of the United States of America
volume
115
issue
41
pages
9610 - 9619
publisher
National Academy of Sciences
external identifiers
  • scopus:85054726525
  • pmid:30266792
ISSN
0027-8424
DOI
10.1073/pnas.1802610115
language
English
LU publication?
yes
id
a5547cc2-0eca-4807-ad22-aaaa294d8653
date added to LUP
2018-10-30 13:34:00
date last changed
2021-10-06 03:56:24
@article{a5547cc2-0eca-4807-ad22-aaaa294d8653,
  abstract     = {<p>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 F<sub>1</sub> to F<sub>4</sub> 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.</p>},
  author       = {Lukhtanov, Vladimir A. and Dinca, Vlad and Friberg, Magne and Síchová, Jindra and Olofsson, Martin and Vila, Roger and Marec, Frantisek and Wiklund, Christer},
  issn         = {0027-8424},
  language     = {eng},
  number       = {41},
  pages        = {9610--9619},
  publisher    = {National Academy of Sciences},
  series       = {Proceedings of the National Academy of Sciences of the United States of America},
  title        = {Versatility of multivalent orientation, inverted meiosis, and rescued fitness in holocentric chromosomal hybrids},
  url          = {http://dx.doi.org/10.1073/pnas.1802610115},
  doi          = {10.1073/pnas.1802610115},
  volume       = {115},
  year         = {2018},
}