A formal test of the theory of universal common ancestry

Abstract

Universal common ancestry (UCA) is a central pillar of modern evolutionary theory1. As first suggested by Darwin2, the theory of UCA posits that all extant terrestrial organisms share a common genetic heritage, each being the genealogical descendant of a single species from the distant past3,4,5,6. The classic evidence for UCA, although massive, is largely restricted to ‘local’ common ancestry—for example, of specific phyla rather than the entirety of life—and has yet to fully integrate the recent advances from modern phylogenetics and probability theory. Although UCA is widely assumed, it has rarely been subjected to formal quantitative testing7,8,9,10, and this has led to critical commentary emphasizing the intrinsic technical difficulties in empirically evaluating a theory of such broad scope1,5,8,9,11,12,13,14,15. Furthermore, several researchers have proposed that early life was characterized by rampant horizontal gene transfer, leading some to question the monophyly of life11,14,15. Here I provide the first, to my knowledge, formal, fundamental test of UCA, without assuming that sequence similarity implies genetic kinship. I test UCA by applying model selection theory5,16,17 to molecular phylogenies, focusing on a set of ubiquitously conserved proteins that are proposed to be orthologous. Among a wide range of biological models involving the independent ancestry of major taxonomic groups, the model selection tests are found to overwhelmingly support UCA irrespective of the presence of horizontal gene transfer and symbiotic fusion events. These results provide powerful statistical evidence corroborating the monophyly of all known life.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Selected class I evolutionary hypotheses, excluding HGT.
Figure 2: Selected class II evolutionary hypotheses, including HGT.

References

  1. 1

    Sober, E. Evidence and Evolution Ch. 4 (Cambridge University Press, 2008)

  2. 2

    Darwin, C. On the Origin of Species by Means of Natural Selection, or, The Preservation of Favoured Races in the Struggle for Life Ch. 14 (J. Murray, 1859)

  3. 3

    Raup, D. M. & Valentine, J. W. Multiple origins of life. Proc. Natl Acad. Sci. USA 80, 2981–2984 (1983)

  4. 4

    Crick, F. H. C. The origin of the genetic code. J. Mol. Biol. 38, 367–379 (1968)

  5. 5

    Sober, E. & Steel, M. Testing the hypothesis of common ancestry. J. Theor. Biol. 218, 395–408 (2002)

  6. 6

    Dobzhansky, T. Nothing in biology makes sense except in the light of evolution. Am. Biol. Teach. 35, 125–129 (1973)

  7. 7

    Hinegardner, R. T. & Engelberg, J. Rationale for a universal genetic code. Science 142, 1083–1085 (1963)

  8. 8

    Penny, D., Hendy, M. D. & Poole, A. M. Testing fundamental evolutionary hypotheses. J. Theor. Biol. 223, 377–385 (2003)

  9. 9

    Penny, D., Foulds, L. R. & Hendy, M. D. Testing the theory of evolution by comparing phylogenetic trees constructed from five different protein sequences. Nature 297, 197–200 (1982)

  10. 10

    Zuckerkandl, E. & Pauling, L. in Evolving Genes and Proteins (eds Bryson, V. & Vogel, H. J.) 97–166 (Academic Press, 1965)

  11. 11

    Doolittle, W. F. The nature of the universal ancestor and the evolution of the proteome. Curr. Opin. Struct. Biol. 10, 355–358 (2000)

  12. 12

    How true is the theory of evolution? Nature 290 (Editorial). 75–76 (1981)

  13. 13

    Popper, K. R. Unended Quest: An Intellectual Autobiography revised edn (Fontana, 1976)

  14. 14

    Syvanen, M. On the occurrence of horizontal gene transfer among an arbitrarily chosen group of 26 genes. J. Mol. Evol. 54, 258–266 (2002)

  15. 15

    Woese, C. R. On the evolution of cells. Proc. Natl Acad. Sci. USA 99, 8742–8747 (2002)

  16. 16

    Burnham, K. P. & Anderson, D. R. Model Selection and Inference: A Practical Information-Theoretic Approach (Springer, 1998)

  17. 17

    Kass, R. E. & Raftery, A. E. Bayes factors. J. Am. Stat. Assoc. 90, 773–795 (1995)

  18. 18

    Futuyma, D. J. Evolutionary Biology 3rd edn (Sinauer Associates, 1998)

  19. 19

    Murzin, A. G. How far divergent evolution goes in proteins. Curr. Opin. Struct. Biol. 8, 380–387 (1998)

  20. 20

    Karlin, S. & Altschul, S. Methods for assessing the statistical significance of molecular sequence features by using general scoring schemes. Proc. Natl Acad. Sci. USA 87, 2264–2268 (1990)

  21. 21

    Harlow, L. L., Mulaik, S. A. & Steiger, J. H. What If There Were No Significance Tests? (Multivariate Applications) (Lawrence Erlbaum, 1997)

  22. 22

    Reeck, G. et al. “Homology” in proteins and nucleic acids: a terminology muddle and a way out of it. Cell 50, 667 (1987)

  23. 23

    Mindell, D. & Meyer, A. Homology evolving. Trends Ecol. Evol. 16, 434–440 (2001)

  24. 24

    Crick, F. H. C. in Progress in Nucleic Acid Research (eds Davidson, J. N. & Cohn, W. E.) 163–217 (Academic Press, 1963)

  25. 25

    Doolittle, W. F. The practice of classification and the theory of evolution, and what the demise of Charles Darwin's tree of life hypothesis means for both of them. Phil. Trans. R. Soc. Lond. B 364, 2221–2228 (2009)

  26. 26

    Huxley, J. S. Evolution: The Modern Synthesis 2nd edn 397–399 (G. Allen & Unwin, 1943)

  27. 27

    Brown, J. R., Douady, C. J., Italia, M. J., Marshall, W. E. & Stanhope, M. J. Universal trees based on large combined protein sequence data sets. Nature Genet. 28, 281–285 (2001)

  28. 28

    Woese, C. & Fox, G. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl Acad. Sci. USA 74, 5088–5090 (1977)

  29. 29

    Poole, A. & Penny, D. Evaluating hypotheses for the origin of eukaryotes. Bioessays 29, 74–84 (2007)

  30. 30

    Chothia, C., Gough, J., Vogel, C. & Teichmann, S. A. Evolution of the protein repertoire. Science 300, 1701–1703 (2003)

  31. 31

    Do, C. B., Mahabhashyam, M. S., Brudno, M. & Batzoglou, S. ProbCons: probabilistic consistency-based multiple sequence alignment. Genome Res. 15, 330–340 (2005)

  32. 32

    Abascal, F., Zardoya, R. & Posada, D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104–2105 (2005)

  33. 33

    Guindon, S. & Gascuel, O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696–704 (2003)

  34. 34

    Altekar, G. Parallel metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 20, 407–415 (2004)

  35. 35

    Huson, D. & Bryant, D. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23, 254–267 (2006)

  36. 36

    Vuong, Q. H. Likelihood ratio tests for model selection and non-nested hypotheses. Econometrica 57, 307–333 (1989)

Download references

Acknowledgements

I thank J. Felsenstein, P. Garrity, N. Matzke, C. Miller, C. Theobald and J. Wilkins for critical commentary.

Author information

Correspondence to Douglas L. Theobald.

Ethics declarations

Competing interests

The author declares no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Tables S1-S12, Supplementary Equations and Discussion 2.1-2.3, Supplementary Figures S1-S2 with legends, Supplementary Methods and Results 3.1-3.4, Supplementary Notes 4.1-4.3 and References. (PDF 352 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Theobald, D. A formal test of the theory of universal common ancestry. Nature 465, 219–222 (2010). https://doi.org/10.1038/nature09014

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.