The Evolution of Chromosome Numbers: Mechanistic Models and Experimental Approaches

Abstract

Chromosome numbers have been widely used to describe the most fundamental genomic attribute of an organism or a lineage. While providing strong phylogenetic signal, chromosome numbers vary remarkably among eukaryotes at all levels of taxonomic resolution. Changes in chromosome numbers regularly serve as indication of major genomic events, most notably polyploidy and dysploidy. Here, we review recent advancements in our ability to make inferences regarding historical events that led to alterations in the number of chromosomes of a lineage. We first describe the mechanistic processes underlying changes in chromosome numbers, focusing on structural chromosomal rearrangements. Then, we focus on experimental procedures, encompassing comparative cytogenomics and genomics approaches, and on computational methodologies that are based on explicit models of chromosome-number evolution. Together, these tools offer valuable predictions regarding historical events that have changed chromosome numbers and genome structures, as well as their phylogenetic and temporal placements.

Three recent sex chromosome-to-autosome fusions in aDrosophila virilisstrain with high satellite content

“…Chromosome rearrangements such as Robertsonian translocations are rare occurrences, but are commonly the cause of karyotype evolution between species (Mayrose and Lysak 2021). In humans, rearrangements resulting from breaks near the centromere are associated with miscarriages and in the case of somatic rearrangements, cancer (Barra and Fachinetti 2018).…”

“…This may be due to intrinsic instability of satellite DNA arrays caused by replication stress of polymerases progressing through highly repetitive sequences, or the formation of unstable DNA topology (Barra and Fachinetti 2018). Robertsonian translocations, one of the most common rearrangements in medical genetics and evolution, occur when there are breaks near the centromere of acrocentric chromosomes and when they are repaired they are fused to each other (Mayrose and Lysak 2021). Robertsonian translocations are associated with multiple miscarriages in humans and aneuploidy disorders like Patau and Down syndromes (Braekeleer and Dao 1990), with increased rates of aneuploidy driven by increased nondisjunction of Robertsonian or fused chromosomes (Schulz et al .…”

Diploidy within a Haploid Genus of Entomopathogenic Fungi

“…Whole-genome sequencing of an extensive collection of 794 natural (wild) isolates of Saccharomyces cerevisiae found alternative ploidy levels within 13% of the otherwise predominately diploid yeast ( Peter et al 2018 ). The same study found chromosomal copy number variation (CCNV or aneuploidy) in 19% of the isolates (193 of the 1,011), reiterating the importance of variation in chromosome numbers for organismal evolution ( Mayrose and Lysak 2020 ). Although at least some fungi readily undergo endoreplication, such levels of genome plasticity are not without constraints.…”

A New Case of Diploidy Within a Haploid Genus of Entomopathogenic Fungi

“…Whole-genome sequencing of an extensive collection of 794 natural (wild) isolates of Saccharomyces cerevisiae found alternative ploidy levels within 13%, of the otherwise predominately diploid yeast (Peter et al, 2018). The same study found chromosomal copy number variation (CCNV or aneuploidy) in 19% of the isolates (193 of the 1,011), reiterating the importance of variation in chromosome numbers for organismal evolution (Mayrose and Lysak, 2020). Although at least some fungi readily undergo endoreplication such levels of genome plasticity is not without constraints.…”