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. 2018 May;2(5):904-909.
doi: 10.1038/s41559-018-0525-3. Epub 2018 Apr 2.

Gene transfers can date the tree of life

Affiliations

Gene transfers can date the tree of life

Adrián A Davín et al. Nat Ecol Evol. 2018 May.

Abstract

Biodiversity has always been predominantly microbial, and the scarcity of fossils from bacteria, archaea and microbial eukaryotes has prevented a comprehensive dating of the tree of life. Here, we show that patterns of lateral gene transfer deduced from an analysis of modern genomes encode a novel and abundant source of information about the temporal coexistence of lineages throughout the history of life. We use state-of-the-art species tree-aware phylogenetic methods to reconstruct the history of thousands of gene families and demonstrate that dates implied by gene transfers are consistent with estimates from relaxed molecular clocks in Bacteria, Archaea and Eukarya. We present the order of speciations according to lateral gene transfer data calibrated to geological time for three datasets comprising 40 genomes for Cyanobacteria, 60 genomes for Archaea and 60 genomes for Fungi. An inspection of discrepancies between transfers and clocks and a comparison with mammalian fossils show that gene transfer in microbes is potentially as informative for dating the tree of life as the geological record in macroorganisms.

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Conflict of interest statement

Competing Interests

The authors declare no competing interests.

Figures

Figure 1
Figure 1. Gene transfers, like fossils, carry information on the timing of species divergence
a) The geological record provides the only source of information concerning absolute time: the age of the oldest fossil representative of a clade provides direct evidence on its minimum age, but inferring maximum age constraints (e.g. dashed line for the red clade), and by extension the relative age of speciation nodes, must rely on indirect evidence on the absence of fossils in the geological record,–. b) Gene transfers, in contrast, do not carry information on absolute time, but they do define relative node age constraints by providing direct evidence for the relative age of speciation events: the gene transfer depicted by the black arrow implies that the diversification of the blue donor clade predates the diversification of the red clade (i.e. node D is necessarily older than node R). Note, however, that the depicted transfer is not informative about the relative age of nodes D’ and R. c) Sequence divergence (here measured in units of expected number of nucleotide substitutions along a strict molecular clock time tree, see supplementary materials) for 36 mammals is correlated (Pearson’s R2=0.664, p<10-2) with age estimates based on the fossil record (ages corresponding to the time of divergence in million years). d) A similar relationship can be seen for gene transfer based relative ages by plotting the sequence divergence (measured similar to part c) against the relative age of ancestral nodes for 40 cyanobacterial genomes (Spearman’s rank correlation rho=0.741, p<10-6) inferred by the MaxTiC (maximal time consistency) algorithm.
Figure 2
Figure 2. Agreement between transfer based relative ages and molecular clocks
a) Relative ages derived from 12 fossil calibrations from a phylogeny of 36 extant mammals were compared with node ages sampled from four different relaxed molecular clock models implemented in Phylobayes and with node ages derived from random chronograms, keeping the species phylogeny fixed. b-d) Relative ages derived from gene transfers using the MaxTiC algorithm were compared with estimates from the same 5 models as in a). For each model and each sampled chronogram we calculated the fraction of relative age constraints that are satisfied. Each violin plot shows the distribution of the fraction of relative age constraints satisfied by 5000 sampled chronograms; inside the violins, boxes correspond to the first and third quartiles of the distribution, a thick horizontal line to the median, and the whiskers extend to extrema no further than 1.5 times the interquartile range. The blue distribution corresponds to random chronograms drawn from the prior with the 95% confidence interval denoted by dashed lines, orange to the strict molecular clock, purple to the autocorrelated lognormal, green to the uncorrelated gamma and grey to the white-noise models.
Figure 3
Figure 3. Donor clades appear older than recipient clades in LGTs retained by MaxTiC.
For genuine LGTs, the donor lineage must be at least as old as the recipient. As one proxy to investigate whether this is the case for transfers retained by our MaxTiC algorithm, we calculated clade-to-tip distances (see supporting text for details) for the inferred donor and recipient clades for LGTs that were retained and discarded by MaxTiC. (a) In all three datasets, transfers retained by MaxTiC (in red) have the property that donor clades are further from the tips of the tree than recipient clades, but the opposite pattern is observed for conflicting transfers rejected by MaxTiC (green), consistent with the idea that MaxTiC identifies genuine LGTs.
Figure 4
Figure 4. The order of speciations according to LGT calibrated to geological time.
5000 chronograms with a speciation time order compatible with LGT-based constraints were sampled per data set and calibrated to geological time (a: Cyanobacteria, b: Archaea, c: Fungi, for details see Methods). The black line corresponds to the consensus chronogram. Red shading represents the spread of node orders within the sample: nodes are in bright red if there is little or no uncertainty on their order according to LGT, in a light red smear if there is high uncertainty on their order. Dates in units of millions of years ago are provided for clades discussed in the text, which are labeled and shaded. Confidence intervals indicate 95% HPD of the time calibrated time orders with the exception of nodes, indicated with an asterisk, that had unambiguous calibrated time orders for which the 95% HPD of the corresponding node from Figures S25-27 is given. Supplementary Figures S1, S2 and S3 provide the same consensus chronograms with species names at the tips.

Comment in

  • Fossil-free dating.
    Dos Reis M. Dos Reis M. Nat Ecol Evol. 2018 May;2(5):771-772. doi: 10.1038/s41559-018-0532-4. Nat Ecol Evol. 2018. PMID: 29610470 No abstract available.

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