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Review
. 2014 Aug 1;6(8):a016139.
doi: 10.1101/cshperspect.a016139.

On the age of eukaryotes: evaluating evidence from fossils and molecular clocks

Laura Eme  1 , Susan C Sharpe  1 , Matthew W Brown  1 , Andrew J Roger  1
Affiliations
Review

On the age of eukaryotes: evaluating evidence from fossils and molecular clocks

Laura Eme et al. Cold Spring Harb Perspect Biol. .

Abstract

Our understanding of the phylogenetic relationships among eukaryotic lineages has improved dramatically over the few past decades thanks to the development of sophisticated phylogenetic methods and models of evolution, in combination with the increasing availability of sequence data for a variety of eukaryotic lineages. Concurrently, efforts have been made to infer the age of major evolutionary events along the tree of eukaryotes using fossil-calibrated molecular clock-based methods. Here, we review the progress and pitfalls in estimating the age of the last eukaryotic common ancestor (LECA) and major lineages. After reviewing previous attempts to date deep eukaryote divergences, we present the results of a Bayesian relaxed-molecular clock analysis of a large dataset (159 proteins, 85 taxa) using 19 fossil calibrations. We show that for major eukaryote groups estimated dates of divergence, as well as their credible intervals, are heavily influenced by the relaxed molecular clock models and methods used, and by the nature and treatment of fossil calibrations. Whereas the estimated age of LECA varied widely, ranging from 1007 (943-1102) Ma to 1898 (1655-2094) Ma, all analyses suggested that the eukaryotic supergroups subsequently diverged rapidly (i.e., within 300 Ma of LECA). The extreme variability of these and previously published analyses preclude definitive conclusions regarding the age of major eukaryote clades at this time. As more reliable fossil data on eukaryotes from the Proterozoic become available and improvements are made in relaxed molecular clock modeling, we may be able to date the age of extant eukaryotes more precisely.

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Figures

Figure 1.
Figure 1.
Maximum likelihood phylogenetic tree of eukaryotes based on a phylogenomic dataset. Additional taxa were added to the original 159-gene Brown et al. (2013) dataset to maximize available fossil calibrations (total of 85 taxa, 43,099 sites). Black dots represent nodes on which fossil calibration constraints were imposed; yellow stars indicate the various positions of the root of the eukaryote tree considered; pink dots indicate the origin of major eukaryotic groups discussed here. A maximum likelihood (ML) phylogenetic tree was obtained from 60 heuristic searches using RAxML version 7.2.6 (Stamatakis 2006) under the Le and Gascuel (LG) + Γ +F amino acid substitution model (Le and Gascuel 2008). Numbers at nodes indicate bootstrap support (BS) for splits estimated from 500 bootstrap replicates. Most splits received maximum support and only BS < 100% is reported. Tree is shown rooted at the base of Amorphea, although roots at the base of either Obazoa or Excavates were also explored. Bayesian inference was also conducted using PhyloBayes 3.2 (Lartillot et al. 2009) by running four chains under either the CAT-GTR, CAT-Poisson, or the catfix C60-Poisson models of evolution, all combined with a gamma rates model. Bayesian calculations were not completed because of lack of convergence between chains, although the postburn-in consensus phylogeny from all runs was identical to the ML tree except for an unresolved multifurcation at the base of Excavata. Relaxed molecular clock (RMC) analyses were conducted with Phylobayes using the ML tree as a fixed topology. For all analyses, a birth–death tree prior was applied. Two chains were run until diagnostic statistics indicated convergence or estimated dates on nodes of interest for the two chains were <5% different. Fossil calibrations were taken from Parfrey et al. (2011) with the following modifications: four calibrations (Gonyaulacales, Spirotrichs, Foraminifera, Euglenids) were removed because of insufficient gene coverage within the clade of interest; the “Ciliate” calibration based on the tetrahymenol biomarker was removed (see text); as insufficient gene data was available from the haptophyte Isochrysis galbana, the upper bound on the coccolithophorid calibration was adjusted to an uninformative maximum (3000 Ma); the oldest cestode fossil (tapeworm) (Dentzien-Dias et al. 2013) was added as a calibration for Platyhelminths. The minimum age (250 Ma) was taken from the youngest possible age of the fossil and the upper boundary was set equal to the next-oldest calibrated node (Bilateria).
Figure 2.
Figure 2.
Impact of the root position and calibration constraints on estimated divergence times. Estimated age (in Myr) of LECA and major eukaryotic groups when the root was placed at the base of Amorphea (squares), Obazoa (diamonds), and Excavata (circles), using hard- (filled shapes) and soft- (open shapes) bounds constraints. Error bars represent 95% credible intervals. All estimations were performed using the C60 substitution model and the uncorrelated γ distribution of rates (UGam) clock model.
Figure 3.
Figure 3.
Impact of the molecular clock models and calibration constraints on estimated divergence times. Estimated age (in Myr) of LECA and major eukaryotic groups using the UGam (squares), LogN (diamonds), and CIR (circles) clock models, applying hard- (filled shapes) and soft- (open shapes) bounds constraints. Error bars represent 95% credible intervals. All analyses are based on the Amorphea root, using the C60 substitution model.
Figure 4.
Figure 4.
Impact of the substitution and molecular clock models on estimated divergence times. Estimated age (in Myr) of LECA and major eukaryotic groups using the UGam (squares), LogN (diamonds), and CIR (circles) clock models. Substitution model was either C60 (filled shapes) or LG (open shapes). Error bars represent 95% credible intervals. All estimations were calculated with the Amorphea root, using soft bounds calibration constraints.
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