Extremely Intron-Rich Genes in the Alveolate Ancestors Inferred with a Flexible Maximum-Likelihood Approach

Abstract

Chromalveolates are a large, diverse supergroup of unicellular eukaryotes that includes Apicomplexa, dinoflagellates, ciliates (three lineages that form the alveolate branch), heterokonts, haptophytes, and cryptomonads (three lineages comprising the chromist branch). All sequenced genomes of chromalveolates have relatively low intron density in protein-coding genes, and few intron positions are shared between chromalveolate lineages. In contrast, genes of different chromalveolates share many intron positions with orthologous genes from other eukaryotic supergroups, in particular, the intron-rich orthologs from animals and plants. Reconstruction of the history of intron gain and loss during the evolution of chromalveolates using a general and flexible maximum-likelihood approach indicates that genes of the ancestors of chromalveolates and, particularly, alveolates had unexpectedly high intron densities. It is estimated that the chromalveolate ancestor had, approximately, two-third of the human intron density, whereas the intron density in the genes of the alveolate ancestor is estimated to be slightly greater than the human intron density. Accordingly, it is inferred that the evolution of chromalveolates was dominated by intron loss. The conclusion that ancestral chromalveolate forms had high intron densities is unexpected because all extant unicellular eukaryotes have relatively few introns and are thought to be unable to maintain numerous introns due to intense purifying selection in their, typically, large populations. It is suggested that, at early stages of evolution, chromalveolates went through major population bottlenecks that were accompanied by intron invasion.