Abstract
BackgroundCentromeres are essential for accurate chromosome segregation, yet sequence conservation is low even among closely related species. Centromere drive predicts rapid turnover because some centromeric sequences may compete better than others during female meiosis. In addition to sequence composition, longer centromeres may have a transmission advantage.ResultsWe report the first observations of extremely long centromeres, covering on average 34 % of the chromosomes, in the red imported fire ant Solenopsis invicta. By comparison, cytological examination of Solenopsis geminata revealed typical small centromeric constrictions. Bioinformatics and molecular analyses identified CenSol, the major centromeric satellite DNA repeat. We found that CenSol sequences are very similar between the two species but the CenSol copy number in S. invicta is much greater than that in S. geminata. In addition, centromere expansion in S. invicta is not correlated with the duplication of CenH3. Comparative analyses revealed that several closely related fire ant species also possess long centromeres.ConclusionsOur results are consistent with a model of simple runaway centromere expansion due to centromere drive. We suggest expanded centromeres may be more prevalent in hymenopteran insects, which use haplodiploid sex determination, than previously considered.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0760-7) contains supplementary material, which is available to authorized users.
Highlights
Centromeres are essential for accurate chromosome segregation, yet sequence conservation is low even among closely related species
Our results are consistent with a model of simple runaway centromere expansion due to centromere drive for the evolution of long centromeres in fire ants
Centromeres are larger in S. invicta than S. geminata We used DAPI to stain metaphase chromosomes and found that, in contrast to typical monocentric chromosomes with a narrow constriction at the centromere, every S. invicta chromosome exhibited long primary constrictions (Fig. 1)
Summary
Centromeres are essential for accurate chromosome segregation, yet sequence conservation is low even among closely related species. In addition to sequence composition, longer centromeres may have a transmission advantage. Centromeres serve as the fundamental chromosome structure responsible for accurate chromosome segregation during eukaryotic cell division. Most eukaryotic chromosomes are monocentric, having microtubule attachment domains restricted to a small constriction zone. Holocentric chromosomes have microtubule binding domains along the entire length of the chromosome and have independently evolved many times [1,2,3]. Monocentric and holocentric chromosomes have been extensively studied, but less attention has been given to centromeres with intermediate structures. Centromeres with longer constrictions occur after Robertsonian fusions [4] as well as in atypical situations such as in hybrids and cancer cell lines [5, 6].
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