The evolution of chromosome numbers: mechanistic models and experimental approaches

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.

Model Adequacy Tests for Likelihood Models of Chromosome-Number Evolution

SummaryChromosome number is a central feature of eukaryote genomes. Deciphering patterns of chromosome-number change along a phylogeny is central to the inference of whole genome duplications and ancestral chromosome numbers. ChromEvol is a probabilistic inference tool that allows the evaluation of several models of chromosome-number evolution and their fit to the data. However, fitting a model does not necessarily mean that the model describes the empirical data adequately. This vulnerability may lead to incorrect conclusions when model assumptions are not met by real data.Here, we present a model adequacy test for likelihood models of chromosome-number evolution. The procedure allows to determine whether the model can generate data with similar characteristics as those found in the observed ones.We demonstrate that using inadequate models can lead to inflated errors in several inference tasks. Applying the developed method to 200 angiosperm genera, we find that in many of these, the best-fitted model provides poor fit to the data. The inadequacy rate increases in large clades or in those in which hybridizations are present.The developed model adequacy test can help researchers to identify phylogenies whose underlying evolutionary patterns deviate substantially from current modelling assumptions and should guide future methods developments.

Genome Size and Chromosome Number Evolution in Korean Iris L. Species (Iridaceae Juss.)

Chromosome numbers, karyotypes, and genome sizes of 14 Iris L. (Iridaceae Juss.) species in Korea and their closely related taxon, Sisyrinchium rosulatum, are presented and analyzed in a phylogenetic framework. To date, understanding the chromosomal evolution of Korean irises has been hampered by their high chromosome numbers. Here, we report analyses of chromosome numbers and karyotypes obtained via classic Feulgen staining and genome sizes measured using flow cytometry in Korean irises. More than a two-fold variation in chromosome numbers (2n = 22 to 2n = 50) and over a three-fold genome size variation (2.39 pg to 7.86 pg/1 C) suggest the putative polyploid and/or dysploid origin of some taxa. Our study demonstrates that the patterns of genome size variation and chromosome number changes in Korean irises do not correlate with the phylogenetic relationships and could have been affected by different evolutionary processes involving polyploidy or dysploidy. This study presents the first comprehensive chromosomal and genome size data for Korean Iris species. Further studies involving molecular cytogenetic and phylogenomic analyses are needed to interpret the mechanisms involved in the origin of chromosomal variation in the Iris.

Speciation through chromosomal fusion and fission in Lepidoptera

Changes in chromosome numbers may strongly affect reproductive barriers, because individuals heterozygous for distinct karyotypes are typically expected to be at least partially sterile or to show reduced recombination. Therefore, several classic speciation models are based on chromosomal changes. One import mechanism generating variation in chromosome numbers is fusion and fission of existing chromosomes, which is particularly likely in species with holocentric chromosomes, i.e. chromosomes that lack a single centromere. Holocentric chromosomes evolved repeatedly across the tree of life, including in Lepidoptera . Although changes in chromosome numbers are hypothesized to be an important driver of the spectacular diversification of Lepidoptera, comparative studies across the order are lacking. We performed the first comprehensive literature survey of karyotypes for Lepidoptera species since the 1970s and tested if, and how, chromosomal variation might affect speciation. Even though a meta-analysis of karyological differences between closely related taxa did not reveal an effect on the degree of reproductive isolation, phylogenetic diversification rate analyses across the 16 best-covered genera indicated a strong, positive association of rates of chromosome number evolution and speciation. These findings suggest a macroevolutionary impact of varying chromosome numbers in Lepidoptera and likely apply to other taxonomic groups, especially to those with holocentric chromosomes. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers’.

Reconstructing ancestral chromosome numbers and inflorescence features in Eleusininae (Poaceae: Chloridoideae: Cynodonteae)

The chromosome number in Poaceae has changed widely over 77 Myr of evolution and polyploidization. Chromosome number changes can suggest a high rate of diversification and evolutionary novelties, and such changes can contribute to speciation. Despite this, chromosome numbers alone do not allow the evolutionary history of a group to be traced. Combined phylogenetic and karyological analyses can clarify the evolutionary history of taxa and allow taxonomic relationships and hierarchical levels to be inferred. The subtribe Eleusininae is the largest of the subfamily Chloridoideae. This study aims to reconstruct their chromosome number evolution, for which ChromEvol 2.0 software was used. Haploid chromosome numbers of Eleusininae were retrieved from the literature, and a consensus phylogenetic tree of Eleusininae was reconstructed. It was possible to infer 41 events of chromosome rearrangements along the evolutionary history of Eleusininae, according to the probabilistic model used. Chromosome number evolution in Eleusininae was mainly influenced by polyploidy events. The ancestral basic chromosome number for Eleusininae was p = 6, but the most recent common ancestor showed p2 = 10. In addition, some derived basic chromosome numbers, such as x = 9, arose through dysploidy, whereas x = 20 was generated via polyploidy.