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Do holocentric chromosomes represent an evolutionary advantage? A study of paired analyses of diversification rates of lineages with holocentric chromosomes and their monocentric closest relatives

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Abstract

Despite most of the cytogenetic research is focused on monocentric chromosomes, chromosomes with kinetochoric activity localized in a single centromere, several studies have been centered on holocentric chromosomes which have diffuse kinetochoric activity along the chromosomes. The eukaryotic organisms that present this type of chromosomes have been relatively understudied despite they constitute rather diversified species lineages. On the one hand, holocentric chromosomes may present intrinsic benefits (chromosome mutations such as fissions and fusions are potentially neutral in holocentrics). On the other hand, they present restrictions to the spatial separation of the functions of recombination and segregation during meiotic divisions (functions that may interfere), separation that is found in monocentric chromosomes. In this study, we compare the diversification rates of all known holocentric lineages in animals and plants with their most related monocentric lineages in order to elucidate whether holocentric chromosomes constitute an evolutionary advantage in terms of diversification and species richness. The results showed that null hypothesis of equal mean diversification rates cannot be rejected, leading us to surmise that shifts in diversification rates between holocentric and monocentric lineages might be due to other factors, such as the idiosyncrasy of each lineage or the interplay of evolutionary selections with the benefits of having either monocentric or holocentric chromosomes.

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Abbreviations

CenH3:

Centromere-specific histone H3 variant

%GC:

Percentage of guanine-cytosine content in the DNA

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Acknowledgements

The authors thank the two anonymous reviewers for their helpful comments that helped to improve the previous version of this manuscript and R. Fernández (Harvard University, Cambridge, Massachusetts), G. Giribet (Harvard University, Cambridge, Massachusetts), and J. Rodríguez (Auburn University, Auburn, Alabama) for their help in providing information about the node ages of some lineages. This research was supported by the Spanish Ministry of Economy and Competitiveness (project CGL2016-77401-P).

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The authors declare that they have no conflict of interest.

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Correspondence to José Ignacio Márquez-Corro.

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Responsible Editor: Tatsuo Fukagawa

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Márquez-Corro, J.I., Escudero, M. & Luceño, M. Do holocentric chromosomes represent an evolutionary advantage? A study of paired analyses of diversification rates of lineages with holocentric chromosomes and their monocentric closest relatives. Chromosome Res 26, 139–152 (2018). https://doi.org/10.1007/s10577-017-9566-8

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  • DOI: https://doi.org/10.1007/s10577-017-9566-8

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