Estimating the timing of early eukaryotic diversification with multigene molecular clocks

Abstract

Although macroscopic plants, animals, and fungi are the most familiar eukaryotes, the bulk of eukaryotic diversity is microbial. Elucidating the timing of diversification among the more than 70 lineages is key to understanding the evolution of eukaryotes. Here, we use taxon-rich multigene data combined with diverse fossils and a relaxed molecular clock framework to estimate the timing of the last common ancestor of extant eukaryotes and the divergence of major clades. Overall, these analyses suggest that the last common ancestor lived between 1866 and 1679 Ma, consistent with the earliest microfossils interpreted with confidence as eukaryotic. During this interval, the Earth's surface differed markedly from today; for example, the oceans were incompletely ventilated, with ferruginous and, after about 1800 Ma, sulfidic water masses commonly lying beneath moderately oxygenated surface waters. Our time estimates also indicate that the major clades of eukaryotes diverged before 1000 Ma, with most or all probably diverging before 1200 Ma. Fossils, however, suggest that diversity within major extant clades expanded later, beginning about 800 Ma, when the oceans began their transition to a more modern chemical state. In combination, paleontological and molecular approaches indicate that long stems preceded diversification in the major eukaryotic lineages.

Fig. 1.

Summary of mean divergence dates for the most recent common ancestor of major clades of extant eukaryotes. Letters are at the mean divergence time and denote analyses, as detailed in Table S1. Error bars represent 95% HPD for BEAST analyses (a–h) and the 95% confidence interval for PhyloBayes (analysis i–p). (A) Estimated age of the root of extant eukaryotes across analyses. Root position: Opis, root constrained to Opisthokonta; Uni, root constrained to “Unikonta”; Estim, root estimated by BEAST. Calibration: All, all Phanerozoic and Proterozoic CCs; Phan, Phanerozic CCs only; 720, All CCs with the minimum age of red algae set to 720 Ma. d = 91 taxa. (B) Estimated ages of major clades from BEAST analyses.

Fig. 2.

Time-calibrated tree of extant eukaryotes using All calibration points, 109 taxa, and root constrained to Opisthokonta. Nodes are at mean divergence times and gray bars represent 95% HPD of node age. (Upper) Geological time scale; (Lower) Absolute time scale in Ma. Thick vertical bars demarcate eras and thin vertical lines denote periods, with dates derived from the 2009 International Stratigraphic Chart. Node calibrated with Phanerozoic fossils (•); node calibrated with Proterozoic fossils (◯). Estimated ages of calibrated nodes differ from calibration constraints (Table 1) because they have been modified by relaxed clock analysis of sequence data.