Chromosome number evolution and the diversification of ray-finned fishes

Abstract

Ray-finned fishes account for nearly half of all vertebrate species today and are arguably the most phenotypically diverse vertebrate clade in Earth’s history. Across this great species richness, they also exhibit many axes of trait diversity. One trait which varies widely is haploid chromosome number, ranging from 6 to 223, although most species have 23–25 chromosomes. Prior research has found that evolution of chromosome number can affect gene expression, meiosis, and gametic compatibility—mechanisms that may influence speciation. Therefore, this study is focused on the macroevolutionary impacts that chromosome number evolution may have on the evolution and diversification of Actinopterygii (ray-finned fishes). First, I tested three hypotheses to explain why an observed central tendency of ~24 haploid chromosomes is so prevalent across distantly related lineages. My findings emphasize that descending dysploidy—loss of individual chromosomes—is a fast and important mechanism in fish chromosome evolution. This process, which may be a component of rediploidization, contributes to the retention of ~24 chromosomes even in lineages that have undergone polyploidy. Descending dysploidy may also be advantageous by reducing the energetic cost of cell division, helping maintain genomic stability. My results further show that chromosome number evolution is a dynamic process shaped by both biotic and abiotic factors. Traits such as dispersal ability, climatic niche, salinity, water depth, fertilization mode, and parental care all interact in complex ways to influence chromosomal change, making it challenging to disentangle their individual effects. Finally, I examined how chromosome number evolution relates to speciation and diversification. Using state-dependent diversification models, I found that the cumulative number of polyploidy events—rather than polyploidy itself—modulates diversification rates. In some cases, polyploidy appears to accelerate diversification and in others, it slows it, offering a potential explanation for the conflicting conclusions of earlier studies which have long debated the impact of whole genome duplications on speciation and diversification. Still, these patterns raise fundamental evolutionary questions such as: if polyploidy can enhance diversification, why don’t we see species with infinite chromosome numbers? Furthermore, if descending dysploidy is such a prevalent process why stop at 24 chromosomes instead of reducing all the way down to one? My results suggest that the explanation may not be reduceable to a single dimension (i.e., chromosome number), but rather diversification outcomes depend on unobserved (i.e., not yet measured) traits, which modulate how lineages respond to chromosomal changes. Identifying these “hidden” factors could be key to understanding how genomic architecture and standing genetic variation shape evolutionary potential across macroevolutionary time and the actinopterygian tree of life.