Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles

Abstract

According to the chromalveolate hypothesis (Cavalier-Smith T. 1999. Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol 46:347-366), the four eukaryotic groups with chlorophyll c-containing plastids originate from a single photosynthetic ancestor, which acquired its plastids by secondary endosymbiosis with a red alga. So far, molecular phylogenies have failed to either support or disprove this view. Here, we devise a phylogenomic falsification of the chromalveolate hypothesis that estimates signal strength across the three genomic compartments: If the four chlorophyll c-containing lineages indeed derive from a single photosynthetic ancestor, then similar amounts of plastid, mitochondrial, and nuclear sequences should allow to recover their monophyly. Our results refute this prediction, with statistical support levels too different to be explained by evolutionary rate variation, phylogenetic artifacts, or endosymbiotic gene transfer. Therefore, we reject the chromalveolate hypothesis as falsified in favor of more complex evolutionary scenarios involving multiple higher order eukaryote-eukaryote endosymbioses.