Macroevolutionary inference of complex modes of chromosomal speciation in a cosmopolitan plant lineage

Abstract

Summary The effects of single chromosome number change—dysploidy – mediating diversification remain poorly understood. Dysploidy modifies recombination rates, linkage, or reproductive isolation, especially for one‐fifth of all eukaryote lineages with holocentric chromosomes. Dysploidy effects on diversification have not been estimated because modeling chromosome numbers linked to diversification with heterogeneity along phylogenies is quantitatively challenging. We propose a new state‐dependent diversification model of chromosome evolution that links diversification rates to dysploidy rates considering heterogeneity and differentiates between anagenetic and cladogenetic changes. We apply this model to Carex (Cyperaceae), a cosmopolitan flowering plant clade with holocentric chromosomes. We recover two distinct modes of chromosomal evolution and speciation in Carex. In one diversification mode, dysploidy occurs frequently and drives faster diversification rates. In the other mode, dysploidy is rare, and diversification is driven by hidden, unmeasured factors. When we use a model that excludes hidden states, we mistakenly infer a strong, uniformly positive effect of dysploidy on diversification, showing that standard models may lead to confident but incorrect conclusions about diversification. This study demonstrates that dysploidy can have a significant role in speciation in a large plant clade despite the presence of other unmeasured factors that simultaneously affect diversification.