A time line of the environmental genetics of the haptophytes

Abstract

The use of genomic data and the rise of phylogenomics have radically changed our view of the eukaryotic tree of life at a high taxonomic level by identifying 4-6 supergroups. Yet, our understanding of the evolution of key innovations within each of these supergroups is limited because of poor species sampling relative to the massive diversity encompassed by each supergroup. Here we apply a multigene approach that incorporates a wide taxonomic diversity to infer the time line of the emergence of strategic evolutionary transitions in the haptophytes, a group of ecologically and biogeochemically significant marine protists that belong to the Chromalveolata supergroup. Four genes (SSU, LSU, tufA, and rbcL) were extensively analyzed under several Bayesian models to assess the robustness of the phylogeny, particularly with respect to 1) data partitioning; 2) the origin of the genes (host vs. endosymbiont); 3) across-site rate variation; and 4) across-lineage rate variation. We show with a relaxed clock analysis that the origin of haptophytes dates back to 824 million years ago (Ma) (95% highest probability density 1,031-637 Ma). Our dating results show that the ability to calcify evolved earlier than previously thought, between 329 and 291 Ma, in the Carboniferous period and that the transition from mixotrophy to autotrophy occurred during the same time period. Although these two transitions precede a habitat change of major diversities from coastal/neritic waters to the pelagic realm (291-243 Ma, around the Permian/Triassic boundary event), the emergence of calcification, full autotrophy, and oceanic lifestyle seem mutually independent.