Integrated genomic and fossil evidence illuminates life's early evolution and eukaryote origin - PubMed (original) (raw)

Integrated genomic and fossil evidence illuminates life's early evolution and eukaryote origin

Holly C Betts et al. Nat Ecol Evol. 2018 Oct.

Abstract

Establishing a unified timescale for the early evolution of Earth and life is challenging and mired in controversy because of the paucity of fossil evidence, the difficulty of interpreting it and dispute over the deepest branching relationships in the tree of life. Surprisingly, it remains perhaps the only episode in the history of life where literal interpretations of the fossil record hold sway, revised with every new discovery and reinterpretation. We derive a timescale of life, combining a reappraisal of the fossil material with new molecular clock analyses. We find the last universal common ancestor of cellular life to have predated the end of late heavy bombardment (>3.9 billion years ago (Ga)). The crown clades of the two primary divisions of life, Eubacteria and Archaebacteria, emerged much later (<3.4 Ga), relegating the oldest fossil evidence for life to their stem lineages. The Great Oxidation Event significantly predates the origin of modern Cyanobacteria, indicating that oxygenic photosynthesis evolved within the cyanobacterial stem lineage. Modern eukaryotes do not constitute a primary lineage of life and emerged late in Earth's history (<1.84 Ga), falsifying the hypothesis that the Great Oxidation Event facilitated their radiation. The symbiotic origin of mitochondria at 2.053-1.21 Ga reflects a late origin of the total-group Alphaproteobacteria to which the free living ancestor of mitochondria belonged.

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Conflict of interest statement

Competing interests

The authors declare no competing interests.

Figures

Figure 1

Figure 1

Posterior time estimates when using (a) a Uniform calibration density prior distribution, reflecting a lack of information about the divergence time relative to the fossil constraint, (b) a Cauchy 50% maximum calibration density prior distribution, reflecting a view that the divergence date should fall between the constraints, (c) a Cauchy 10% maximum calibration density prior distribution, reflecting a view that the fossil prior is a good approximation of the divergence date and (d) a Cauchy 90% maximum calibration density prior distribution, reflecting a view that the fossil prior is a poor approximation of the divergence date, all with an uncorrelated clock model. Then posterior age estimates when using (e) a Cauchy 50% maximum calibration density prior distribution with an autocorrelated clock model and finally, (f) a Cauchy 50% maximum calibration density prior distribution, with an uncorrelated clock model and a single partition scheme. All molecular clock analysis converged well. The coloured dots highlight specific nodes with their respective confidence intervals displayed as bars in light blue; orange (LUCA), red (crown Archaeabacteria), blue (crown Eubacteria), yellow (crown Eukaryota), pink (alphaproterobacteria) and dark blue (cyanobacteria). This figure illustrates how divergence times change as alternative approaches to modelling calibrations and the process of molecular revolution change. Divergence estimates from Figure 1f and their credibility intervals could be rejected based on an AIC test. The other results (Figure 1a-e) cannot be rejected.

Figure 2

Figure 2

Changes in divergence times (billions of years before present) that result from applying alternative strategies, (a) Cauchy 50% maximum calibration density prior distribution vs Uniform calibration density prior distribution, (b) Cauchy 50% maximum calibration density prior distribution vs Cauchy 10% maximum calibration density prior distribution, (c) Cauchy 50% maximum calibration density prior distribution vs Cauchy 90% maximum calibration density prior distribution, (d) Cauchy 50% maximum calibration density prior distribution uncorrelated clock model vs Cauchy 50% maximum calibration density prior distribution autocorrelated clock model, (e) Cauchy 50% maximum calibration density prior distribution in both cases, 29 partition scheme vs 1 partition scheme. The lower row displays the results of adding additional genes as infinite sites plots, (f) 5 gene dataset, (g) 10 gene dataset, (h) 15 gene dataset, (i) 20 gene dataset and (j) 29 gene dataset. In all cases blue dots denote the node dates.

Figure 3

Figure 3

A tree combining uncertainties from approaches using uncorrelated and autocorrelated clock models and different calibration density distributions showing tip labels for Eukaryota (grey), Archaeabacteria (red), and Eubacteria (blue). The purple bars denote the credible intervals for each node. Red dots highlight calibrated nodes and the corresponding black dot highlights the age of the minimum bound of its corresponding calibration. The phylogenetic relationships of the mitochondrion within Alphaproteobacteria are still debated,–, and it is unclear whether the free-living ancestor of the mitochondrion was a crown or a stem representative of this group. The pink and red bars above the crown eukaryote node denote the time period in which crown alphaproteobacteria and stem alphaproteobacteria respectively were also present, and therefore in such time that the mitochondrial endosymbiosis may have occurred. The green bar lower down denotes the time in which the plastid endosymbiosis may have occurred. Some important events in the Earth’s and life’s history are indicated along the base of the figure.

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