University of Oulu

Vladimir A. Lukhtanov, Vlad Dincă, Magne Friberg, Jindra Šíchová, Martin Olofsson, Roger Vila, František Marec, Christer Wiklund, Versatility of multivalent orientation, inverted meiosis, and rescued fitness in holocentric chromosomal hybrids. Proceedings of the National Academy of Sciences Oct 2018, 115 (41) E9610-E9619; DOI: 10.1073/pnas.1802610115

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

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Author: Lukhtanov, Vladimir A.1,2; Dincă, Vlad3,4; Friberg, Magne5;
Organizations: 1Department of Karyosystematics, Zoological Institute of Russian Academy of Sciences, 199034 St. Petersburg, Russia
2Department of Entomology, St. Petersburg State University, 199034 St. Petersburg, Russia
3Department of Ecology and Genetics, University of Oulu, 90014 Oulu, Finland
4Institut de Biologia Evolutiva, Consejo Superior de Investigaciones Científicas and Universitat Pompeu Fabra, 08003 Barcelona, Spain
5Biodiversity Unit, Department of Biology, Lund University, 22362 Lund, Sweden
6Laboratory of Molecular Cytogenetics, Institute of Entomology, Biology Centre of the Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic
7Department of Zoology, Stockholm University, SE-106 91 Stockholm, Sweden
Format: article
Version: published version
Access: open
Online Access: PDF Full Text (PDF, 1.6 MB)
Persistent link: http://urn.fi/urn:nbn:fi-fe2019062622101
Language: English
Published: National Academy of Sciences of the United States of America, 2018
Publish Date: 2019-06-26
Description:

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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Series: Proceedings of the National Academy of Sciences of the United States of America
ISSN: 0027-8424
ISSN-E: 1091-6490
ISSN-L: 0027-8424
Volume: 115
Issue: 41
Pages: E9610 - E9619
DOI: 10.1073/pnas.1802610115
OADOI: https://oadoi.org/10.1073/pnas.1802610115
Type of Publication: A1 Journal article – refereed
Field of Science: 1181 Ecology, evolutionary biology
1184 Genetics, developmental biology, physiology
Subjects:
Funding: V.A.L. was supported by Grant N 14-14-00541 from the Russian Science Foundation to the Zoological Institute of the Russian Academy of Sciences. V.D. was supported by the Wenner-Gren Foundation Sweden and by a Marie Curie International Outgoing Fellowship within the 7th European Community Framework Programme (Project 625997). M.F. was supported by a Junior Research Grant from the Swedish Research Council. R.V. was supported by Agencia Estatal de Investigación and Fondo Europeo de Desarrollo Regional (Project CGL2016-76322-P) and by Agència de Gestió d’Ajuts Universitaris i de Recerca (Project 2014-SGR-1532). J.Š. and F.M. acknowledge support from Grants 14–22765S and 17-13713S of the Czech Science Foundation.
Copyright information: © The Authors, 2018. Freely available online through the PNAS open access option.