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

Author:
  • Vladimir A. Lukhtanov
  • Vlad Dinca
  • Magne Friberg
  • Jindra Síchová
  • Martin Olofsson
  • Roger Vila
  • Frantisek Marec
  • Christer Wiklund
Publishing year: 2018
Language: English
Pages: 9610-9619
Publication/Series: Proceedings of the National Academy of Sciences of the United States of America
Volume: 115
Issue: 41
Document type: Journal article
Publisher: National Acad Sciences

Abstract english

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.

Keywords

  • Evolutionary Biology
  • Chromosomal evolution
  • Chromosomal rearrangement
  • Hybridization
  • Inverted meiosis
  • Speciation

Other

Published
  • ISSN: 0027-8424
Magne Friberg
E-mail: magne [dot] friberg [at] biol [dot] lu [dot] se

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Biodiversity

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Evolutionary Ecology of Plant–Insect Interactions

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Main supervisor

Hampus Petrén

Assistant supervisor

Isidora Longarevic

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Karin Gross