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The genomic landscape of evolutionary convergence in mammals, birds and reptiles

Nature Ecology & Evolution volume 1, Article number: 0041 (2017) Cite this article

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Abstract

Many lineage-defining (nodal) mutations possess high functionality. However, differentiating adaptive nodal mutations from those that are functionally compensated remains challenging. To address this challenge, we identified functional nodal mutations (fNMs) in ~3,400 nuclear DNA (nDNA) and 4 mitochondrial DNA (mtDNA) protein structures from 91 and 1,003 species, respectively, representing the entire mammalian, bird and reptile phylogeny. A screen for candidate compensatory mutations among co-occurring amino acid changes in close structural proximity revealed that such compensated fNMs encompass 37% and 27% of the mtDNA and nDNA datasets, respectively. Analysis of the remaining (non-compensated) mutations, which are enriched for adaptive mutations, showed that birds and mammals share most such recurrent fNMs (N = 51). Among the latter, we discovered mutations in thermoregulation-related genes. These represent the best candidates to explain the molecular basis of convergent body thermoregulation in birds and mammals. Our analysis reveals the landscape of possible mutational compensation and convergence in amniote phylogeny.

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Figure 1: Illustration demonstrating fNM potential compensation and possible adaptation in a protein-coding gene.
Figure 2: Prevalence assessment of potential compensation for fNMs in amniotes.
Figure 3: Analysis of shared non-compensated fRNMs between all possible tree branches.

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References

  1. Breen, M. S., Kemena, C., Vlasov, P. K., Notredame, C. & Kondrashov, F. A. Epistasis as the primary factor in molecular evolution. Nature 490, 535–538 (2012).

    Article  CAS  Google Scholar 

  2. Levin, L., Zhidkov, I., Gurman, Y., Hawlena, H. & Mishmar, D. Functional recurrent mutations in the human mitochondrial phylogeny — dual roles in evolution and disease. Genome Biol. Evol. 5, 876–890 (2013).

    Article  Google Scholar 

  3. Rosenberg, N. A. et al. Genome-wide association studies in diverse populations. Nat. Rev. Genet. 11, 356–366 (2010).

    Article  CAS  Google Scholar 

  4. Kern, A. D. & Kondrashov, F. A. Mechanisms and convergence of compensatory evolution in mammalian mitochondrial tRNAs. Nat. Genet. 36, 1207–1212 (2004).

    Article  CAS  Google Scholar 

  5. Schaner, P. et al. Episodic evolution of pyrin in primates: human mutations recapitulate ancestral amino acid states. Nat. Genet. 27, 318–321 (2001).

    Article  CAS  Google Scholar 

  6. Zhang, G. et al. Triangulation of the human, chimpanzee, and Neanderthal genome sequences identifies potentially compensated mutations. Hum. Mutat. 31, 1286–1293 (2010).

    Article  Google Scholar 

  7. Moreno-Loshuertos, R. et al. Evolution meets disease: penetrance and functional epistasis of mitochondrial tRNA mutations. PLoS Genet. 7, e1001379 (2011).

    Article  CAS  Google Scholar 

  8. Poon, A. & Chao, L. The rate of compensatory mutation in the DNA bacteriophage phiX174. Genetics 170, 989–999 (2005).

    Article  CAS  Google Scholar 

  9. Poon, A. F. & Chao, L. Functional origins of fitness effect-sizes of compensatory mutations in the DNA bacteriophage phiX174. Evolution 60, 2032–2043 (2006).

    CAS  Google Scholar 

  10. Tenaillon, O. et al. The molecular diversity of adaptive convergence. Science 335, 457–461 (2012).

    Article  CAS  Google Scholar 

  11. Kryazhimskiy, S., Rice, D. P., Jerison, E. R. & Desai, M. M. Microbial evolution. Global epistasis makes adaptation predictable despite sequence-level stochasticity. Science 344, 1519–1522 (2014).

    Article  CAS  Google Scholar 

  12. Mishmar, D. et al. Natural selection shaped regional mtDNA variation in humans. Proc. Natl Acad. Sci. USA 100, 171–176 (2003).

    Article  CAS  Google Scholar 

  13. Nachman, M. W., Brown, W. M., Stoneking, M. & Aquadro, C. F. Nonneutral mitochondrial DNA variation in humans and chimpanzees. Genetics 142, 953–963 (1996).

    CAS  Google Scholar 

  14. Parmakelis, A., Kotsakiozi, P. & Rand, D. Animal mitochondria, positive selection and cyto-nuclear coevolution: insights from pulmonates. PLoS ONE 8, e61970 (2013).

    Article  CAS  Google Scholar 

  15. Levin, L., Blumberg, A., Barshad, G. & Mishmar, D. Mito-nuclear co-evolution: the positive and negative sides of functional ancient mutations. Front. Genet. 5, 448 (2014).

    Article  Google Scholar 

  16. Sabeti, P. C. et al. Detecting recent positive selection in the human genome from haplotype structure. Nature 419, 832–837 (2002).

    Article  CAS  Google Scholar 

  17. Liu, X. et al. Detecting and characterizing genomic signatures of positive selection in global populations. Am. J. Hum. Genet. 92, 866–881 (2013).

    Article  CAS  Google Scholar 

  18. McCandlish, D. M., Rajon, E., Shah, P., Ding, Y. & Plotkin, J. B. The role of epistasis in protein evolution. Nature 497, E1–2; discussion E2–3 (2013).

    Article  Google Scholar 

  19. Baresic, A., Hopcroft, L. E., Rogers, H. H., Hurst, J. M. & Martin, A. C. Compensated pathogenic deviations: analysis of structural effects. J. Mol. Biol. 396, 19–30 (2010).

    Article  CAS  Google Scholar 

  20. Foote, A. D. et al. Convergent evolution of the genomes of marine mammals. Nat. Genet. 47, 272–275 (2015).

    Article  CAS  Google Scholar 

  21. Stern, D. L. The genetic causes of convergent evolution. Nat. Rev. Genet. 14, 751–764 (2013).

    Article  CAS  Google Scholar 

  22. Bernt, M. & Middendorf, M. A method for computing an inventory of metazoan mitochondrial gene order rearrangements. BMC Bioinformat. 12 Suppl. 9, S6 (2011).

    Article  Google Scholar 

  23. Ivankov, D. N., Finkelstein, A. V. & Kondrashov, F. A. A structural perspective of compensatory evolution. Curr. Opin. Struct. Biol. 26, 104–112 (2014).

    Article  CAS  Google Scholar 

  24. Osada, N. & Akashi, H. Mitochondrial-nuclear interactions and accelerated compensatory evolution: evidence from the primate cytochrome c oxidase complex. Mol. Biol. Evol. 29, 337–346 (2012).

    Article  CAS  Google Scholar 

  25. Filteau, M. et al. Evolutionary rescue by compensatory mutations is constrained by genomic and environmental backgrounds. Mol. Syst. Biol. 11, 832 (2015).

    Article  Google Scholar 

  26. Blount, Z. D., Borland, C. Z. & Lenski, R. E. Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli . Proc. Natl Acad. Sci. USA 105, 7899–7906 (2008).

    Article  CAS  Google Scholar 

  27. Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).

    Article  CAS  Google Scholar 

  28. Pei, J., Kim, B.-H. & Grishin, N. V. PROMALS3D: a tool for multiple protein sequence and structure alignments. Nucleic Acids Res. 36, 2295–2300 (2008).

    Article  CAS  Google Scholar 

  29. Nawrocki, E. P. & Eddy, S. R. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29, 2933–2935 (2013).

    Article  CAS  Google Scholar 

  30. Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).

    Article  CAS  Google Scholar 

  31. Meredith, R. W. et al. Impacts of the Cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334, 521–524 (2011).

    Article  CAS  Google Scholar 

  32. Morgan, C. C. et al. Heterogeneous models place the root of the placental mammal phylogeny. Mol. Biol. Evol. 30, 2145–2156 (2013).

    Article  CAS  Google Scholar 

  33. Hackett, S. J. et al. A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763–1768 (2008).

    Article  CAS  Google Scholar 

  34. Vidal, N. & Hedges, S. B. The phylogeny of squamate reptiles (lizards, snakes, and amphisbaenians) inferred from nine nuclear protein-coding genes. C. R. Biol. 328, 1000–1008 (2005).

    Article  CAS  Google Scholar 

  35. Glaser, F. et al. ConSurf: identification of functional regions in proteins by surface-mapping of phylogenetic information. Bioinformatics 19, 163–164 (2003).

    Article  CAS  Google Scholar 

  36. Grantham, R. Amino acid difference formula to help explain protein evolution. Science 185, 862–864 (1974).

    Article  CAS  Google Scholar 

  37. Kondrashov, A. S., Sunyaev, S. & Kondrashov, F. A. Dobzhansky–Muller incompatibilities in protein evolution. Proc. Natl Acad. Sci. USA 99, 14878–14883 (2002).

    Article  CAS  Google Scholar 

  38. Hanada, R. et al. Central control of fever and female body temperature by RANKL/RANK. Nature 462, 505–509 (2009).

    Article  CAS  Google Scholar 

  39. Zhang, Y. et al. Targeted deletion of thioesterase superfamily member 1 promotes energy expenditure and protects against obesity and insulin resistance. Proc. Natl Acad. Sci. USA 109, 5417–5422 (2012).

    Article  CAS  Google Scholar 

  40. Taylor-Burt, K. R., Monroy, J., Pace, C., Lindstedt, S. & Nishikawa, K. C. Shiver me titin! Elucidating titin’s role in shivering thermogenesis. J. Exp. Biol. 218, 694–702 (2015).

    Article  Google Scholar 

  41. Miinalainen, I. J. et al. Mitochondrial 2,4-dienoyl-CoA reductase deficiency in mice results in severe hypoglycemia with stress intolerance and unimpaired ketogenesis. PLoS Genet. 5, e1000543 (2009).

    Article  Google Scholar 

  42. Caterina, M. J. et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288, 306–313 (2000).

    Article  CAS  Google Scholar 

  43. Ramsey, K. M. et al. Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science 324, 651–654 (2009).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank R. Zarivach for critical discussions and the Negev Foundation for a Scholarship of Excellence awarded to L.L. This study was funded by research grants from the Israeli Science Foundation (610/12), Binational Science Foundation and a US Army Life Science division grant 67993LS awarded to D.M.

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Authors and Affiliations

  1. Department of Life Sciences, Building 40, Room 009, Ben Gurion University of the Negev, Beer-Sheva, Israel 8410501

    Liron Levin & Dan Mishmar

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  1. Liron Levin
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Correspondence to Dan Mishmar.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Figures 1–5; supplementary Tables 1–4 (PDF 1434 kb)

Supplementary Dataset 1

Nodal mutations identified in mtDNA tRNAs genes, mtDNA rRNAs genes and nodal mutations identified in mtDNA protein coding genes. (XLSX 3372 kb)

Supplementary Dataset 2

Nodal mutations identified in nDNA-encoded protein genes. (XLSX 16633 kb)

Supplementary Dataset 3

MATLAB scripts generated for the analysis presented in this Article. (ZIP 3831 kb)

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Levin, L., Mishmar, D. The genomic landscape of evolutionary convergence in mammals, birds and reptiles. Nat Ecol Evol 1, 0041 (2017). https://doi.org/10.1038/s41559-016-0041

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