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.

Biodiversity Unit Department of Biology Lund University 22362 Lund Sweden

Department of Ecology and Genetics University of Oulu 90014 Oulu Finland

Department of Entomology St Petersburg State University 199034 St Petersburg Russia

Department of Karyosystematics Zoological Institute of Russian Academy of Sciences 199034 St Petersburg Russia;

Department of Zoology Stockholm University SE 106 91 Stockholm Sweden

Institut de Biologia Evolutiva Consejo Superior de Investigaciones Científicas and Universitat Pompeu Fabra 08003 Barcelona Spain

Laboratory of Molecular Cytogenetics Institute of Entomology Biology Centre of the Czech Academy of Sciences 370 05 České Budějovice Czech Republic

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