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

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.

Holocentric chromosomes

“…The availability of genomics data could therefore allow to dissect at a genome-level the origin of holocentrism in order to better understand if the same genes (or different) have been coopted to favour the shift from mono-to holocentrism. Lastly, a more detailed study of the holocentric chromosomes evolution could be useful to understand which costs and advantages acted as main drivers in the evolution of the chromosome structure in order to better understand the multiple shifts from mono-to holocentrism (and vice versa) that occurred during both plant and animal evolution, even within recent lineages [63].…”

Analysis of the small chromosomal Prionium serratum (Cyperid) demonstrates the importance of reliable methods to differentiate between mono- and holocentricity

“…The studies on artificial chromosomal rearrangements in various holocentric species showed that chromosome fragments retaining centromere activity are transmitted during mitosis and meiosis (Jankowska et al 2015 ). Comparisons of diversification rates between monocentric and holocentric sister clades in animals and plants did not detect an increase in diversification in holocentric species (Marquez-Corro et al 2018 ). Nevertheless, these analyses depend on the correct identification of the centromere type in a large number of lineages.…”

Epigenetics as an Evolutionary Tool for Centromere Flexibility

“…Furthermore, centromeric proteins and the kinetochore complex can change also in response to fluctuations in kinetochore protein levels (reviewed in [122]). Some organisms, such as Caenorhabditis elegans, have diffuse centromeres (holocentromeres) of unclear evolutionary advantage [123]. Despite the differences in DNA sequences, proteins composition and centromere size, all of these diverse centromere structures promote efficient chromosome segregation, balancing genome stability and adaptability, and ensuring faithful genome inheritance at each cellular generation.…”