The phylogenetic origins and evolutionary history of holocentric chromosomes

Abstract

In eukaryotes, we can recognize two kinds of chromosomes, based on the location of the kinetochores. The majority of eukaryotes have monocentric chromosomes, in which kinetochoric activity is concentrated in a single locus. In several unrelated eukaryotic lineages, chromosomes are holocentric, having diffuse centromeric / kinetochoric activity along the length of the chromosome. Whether holocentric chromosomes are derived or ancestral is still under debate. This study uses the phylogenetic tree from Time Tree of Life project, comprising more than 50,000 sampled species, to reconstruct the evolution of holocentry. Asymmetrical two-state Markov (Mk2) models were compared with BiSSE models to assess sensitivity of our conclusions to possible effects of holocentry on lineage diversification rates. Our analyses based on Mk2 and BiSSE models inferred that the rate of transition from holocentric to monocentric chromosomes is two orders of magnitude higher than the reverse direction. The ancestral state of all eukaryotes is ambiguous depending on the model, inferred to be either monocentric (Mk2) or holocentric (BiSSE). Whatever the direction, the multiple transitions and high diversity of centromere organization across the tree of life are what we would expect if there are selective advantages to both chromosome types. Understanding those selective advantages is key to understanding how genetic information is organized and transmitted from one generation to the next, and why these major evolutionary transitions in centromere organization have occurred in the first place.