Horizontal Gene Transfer in Evolution


The concept of horizontal or lateral gene transfer (the non‐genealogical transmission of genetic material between organisms) was introduced in 1990s to explain the observed incongruence in phylogenetic reconstructions using different genes. Today, horizontal gene transfer is accepted as an important force modulating evolution of Bacteria, Archaea and unicellular eukaryotes, and evidence is rising for their role in the evolution of pluricellular eukaryotes (fungi, plants and animals). The realisation that horizontal gene transfer plays an important role in evolution of both, prokaryotes and eukaryotes, put in question the metaphor of the tree of life and the traditional view of evolution as a slow process. A more pluralistic approach to evolution is emerging that encompasses different evolutionary mechanisms operating at different levels of complexity.

Key Concepts

  • Horizontal gene transfer is the non‐genealogical transmission of genetic material between different organisms.
  • Horizontal gene transfer has become a part of evolutionary thinking over the past 25 years.
  • Horizontal gene transfer plays an important role in prokaryotic evolution.
  • Horizontal gene transfer also modulates evolution of unicellular eukaryotes.
  • Increasing evidence support the role of horizontal gene transfer in evolution of pluricellular eukaryotes.
  • Horizontal gene transfer challenges the tree of life metaphor.
  • Horizontal gene transfer challenges the traditional view of evolution as a slow process.
  • A pluralistic approach to evolution is needed.

Keywords: horizontal gene transfer; evolutionary mechanisms; reticulated evolution; tree of life

Figure 1. New metaphors of evolution taking into consideration the role of horizontal gene transfer. (a) The web of life (Reproduced with permission from Doolittle WF () © The American Association for the Advancement of Science). (b) The ring of life. (Reproduced with permission from Rivera and Lakel () Nature Publishing Group)


Bapteste E , O′Malley MA , Beiko RG , et al. (2009) Prokaryotic evolution and the tree of life are two different things. Biology Direct 4: 34. DOI: 10.1186/1745-6150-4-34.

Bapteste E , Susko E , Leigh J , et al. (2008) Alternative methods for concatenation of core genes indicate a lack of resolution in deep nodes of the prokaryotic phylogeny. Molecular Biology and Evolution 25: 83–91. DOI: 10.1093/mlbev/msm229.

Bapteste E , van Iersel L , Janke A , et al. (2013) Networks: expanding evolutionary thinking. Trends in Genetics 29: 439–441. DOI: 10.1016/j.tig.2013.05.007.

Boto L (2014) Horizontal gene transfer in the acquisition of novel traits by metazoans. Proceedings of the Royal Society B 281: 20132450. DOI: 10.1098/rspb.2013.2450.

Boussau B , Guéguen L and Gouy M (2008) Accounting for horizontal gene transfers explains conflicting hypotheses regarding the position of aquificales in the phylogeny of Bacteria. BMC Evolutionary Biology 8: 272. DOI: 10.1186/1471-2148-8-272.

Caro‐Quintero A and Konstantinidis KT (2015) Inter‐phylum HGT has shaped the metabolism of many mesophilic and anaerobic bacteria. The ISME Journal 9: 958–967. DOI: 10.1038/ismej.2014.193.

Chan CX , Beiko RG , Darling AE and Ragan MA (2009) Lateral transfer of genes and gene fragments in prokaryotes. Genome Biology and Evolution 2009: 429–438. DOI: 10.1093/gbe/evp044.

Cohen O and Pupko T (2010) Inference and characterization of horizontally transferred gene families using stochastic mapping. Molecular Biology and Evolution 27: 703–713. DOI: 10.1093/molbev/msp240.

Cohen O , Gophna U and Pupko T (2011) The complexity hypothesis revisited: Connectivity rather than function constitutes a barrier to horizontal gene transfer. Molecular Biology and Evolution 28: 1481–1489. DOI: 10.1093/molbev/msq333.

Crisp A , Boschetti C , Pery M , et al. (2015) Expression of multiple horizontally acquired genes is a hallmark of both vertebrate and invertebrate genomes. Genome Biology 16: 50. DOI: 10.1186/s13059-015-0607-3.

Dagan T , Artzy‐Randrup Y and Martin W (2008) Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution. Proceedings of the National Academy of Sciences of the United States of America 105: 10039–10044. DOI: 10.1073/pnas.0800679105.

Doolittle WF (1999) Phylogenetic classification and the universal tree. Science 284: 2124–2128. DOI: 10.1126/science.284.5423.2124.

Doolittle WF and Bapteste E (2007) Pattern pluralism and the tree of life hypothesis. Proceedings of the National Academy of Sciences of the United States of America 104: 2043–2049. DOI: 10.1073/pnas.0610699104.

Flot JF , Hespeels B , Li X , et al. (40 co‐authors) (2013) Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. Nature 500: 453–457. DOI: 10.1038/nature12326.

Galtier N and Daubin V (2008) Dealing with incongruence in phylogenetic analyses. Philosophical Transactions of the Royal Society B 363: 4023–4029. DOI: 10.1098/rstb.2008.0144.

Gao C , Ren X , Mason AS , et al. (2014) Horizontal gene transfer in plants. Functional Integrative Genomics 14: 23–29. DOI: 10.1007/s10142-013-0345-0.

Gladieux P , Ropars J , Badouin H , et al. (2014) Fungal evolutionary genomics provides insight into the mechanisms of adaptive divergence in eukaryotes. Molecular Ecology 23: 753–773. DOI: 10.1111/mec.12631.

Gladyshev EA , Meselson M and Arkhipova IR (2008) Massive horizontal gene transfer in bdelloid rotifers. Science 320: 1210–1213. DOI: 10.1126/science.1156407.

Gogarten JP and Townsend JP (2005) Horizontal gene transfer, genome innovation and evolution. Nature Reviews Microbiology 3: 679–687. DOI: 10.1038/nrmicro1204.

Goldenfeld N and Woese C (2007) Biology's next revolution. Nature 445: 369. DOI: 10.1038/445369a.

Gophna U , Charlebois RL and Doolittle WF (2004) Have archaeal genes contributed to bacterial virulence? Trends in Microbiology 12: 213–219. DOI: 10.1016/j.tim.2004.03.002.

Gribaldo S and Brochier C (2009) Phylogeny of prokaryotes: does it exist and why should be care? Research in Microbiology 160: 513–521. DOI: 10.1016/j.resmic.2009.07.006.

Guljamow A , Jenke‐Kodama H , Saumweber H , et al. (2007) Horizontal gene transfer of two cytoskeletal elements from a eukaryote to a cyanobacterium. Current Biology 17: R757–R759. DOI: 10.1016/j.cub.2007.06.063.

Hilario E and Gogarten JP (1993) Horizontal gene transfer of ATPase genes – the tree of life becomes a net of life. BioSystems 31: 111–119. DOI: 10.1016/0303-2647(93)90038-E.

Huang J and Gogarten JP (2006) Ancient horizontal gene transfer can benefit phylogenetic reconstruction. Trends in Genetics 22: 361–366. DOI: 10.1016/j.tig.2006.05.004.

Jain R , Rivera MC and Lake JA (1999) Horizontal gene transfer among genomes: the complexity hypothesis. Proceedings of the National Academy of Sciences of the United States of America 96: 3801–3806.

Kanhere A and Vingron M (2009) Horizontal gene transfer in prokaryotes show differential preferences for metabolic and translational genes. BMC Evolutionary Biology 9: 9. DOI: 10.1186/1471-2148-9-9.

Keeling PJ and Palmer JD (2008) Horizontal gene transfer in eukaryotic evolution. Nature Reviews Genetics 9: 605–618. DOI: 10.1038/nrg2386.

Koonin EV , Makarova AS and Aravind L (2001) Horizontal gene transfer in prokaryotes. Quantification and classification. Annual Review of Microbiology 55: 709–742.

Koonin EV and Wolf YI (2009a) Is evolution Darwinian or/and Lamarckian? Biology Direct 4: 42. DOI: 10.1186/1745-6150-4-42.

Lapierre P and Gogarten JP (2009) Estimating the size of the bacterial pan‐genome. Trends in Genetics 25: 107–110. DOI: 10.1016/j.tig.2008.12.004.

Lercher MJ and Pál C (2008) Integration of horizontally transferred genes into regulatory interaction networks takes many million years. Molecular Biology and Evolution 25: 559–567. DOI: 10.1093/molbev/msm283.

Lovell HC , Mansfield JW , Godfrey SAC , et al. (2009) Bacterial evolution by genomic island occurs via DNA transformation in planta. Current Biology 19: 1586–1590. DOI: 10.1016/j.cub.2009.08.018.

Marri PR and Golding GB (2008) Gene amelioration demonstrated: the journey of nascent genes in bacteria. Genome 51: 164–168. DOI: 10.1139/G07-105.

Nakamura Y , Itoh T , Matsuda H and Gojobori T (2004) Biased biological functions of horizontally transferred genes in prokaryotic genomes. Nature Genetics 36: 760–766. DOI: 10.1038/ng1381.

Nelson‐Satho S , Sousa FL , Roettger M , et al. (2015) Origins of major archaeal clades correspond to gene acquisitions from bacteria. Nature 517: 77–80. DOI: 10.1038/nature13805.

Oliver KR and Greene WK (2009) Transposable elements: powerful facilitators of evolution. Bioessays 31: 703–714. DOI: 10.1002/bies.200800219.

Puigbo P , Wolf YI and Koonin EV (2010) The tree and net components of prokaryote evolution. Genome Biology and Evolution 2: 745–756. DOI: 10.1093/gbe/evq062.

Ragan MA (2001) Detection of lateral gene transfer among microbial genomes. Current Opinion in Genetics and Development 11: 620–626. DOI: 10.1016/S0959-437X(00)00244-6.

Rannala B and Yang Z (2008) Phylogenetic inference using whole genomes. Annual Review of Genomics and Human Genetics 9: 217–231. DOI: 10.1146/annurev.genom.9.081307.164407.

Rest JS and Mindell DP (2003) Retroids in archaea: phylogeny and lateral origin. Molecular Biology and Evolution 20: 1134–1142. DOI: 10.1093/molbev/msg135.

Rivera MC and Lake JA (2004) The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431: 152–155. DOI: 10.1038/nature02848.

Schwartz JA , Curtis NE and Pierce SK (2014) Fish labelling reveals a horizontally transferred algal (Vaucheria litorea) nuclear gene on a sea slug (Elysia chlorotica) chromosome. The Biological Bulletin 277: 300–312.

Sorek R , Zhu Y , Creevey CJ , et al. (2007) Genome‐wide experimental determination of barriers to horizontal gene transfer. Science 318: 1449–1452. DOI: 10.1126/science.1147112.

Syvanen M (1985) Cross‐species gene transfer: implications for a new theory of evolution. Journal of Theoretical Biology 112: 333–343.

Tettelin H , Masignani V , Cieslewicz MJ , et al. (2005) Genome analysis of multiple pathogenic isolates of Streptococus agalactiae: implications for the microbial “pan‐genome”. Proceedings of the National Academy of Sciences of the United States of America 102: 13950–13955. DOI: 10.1073/pnas.0506758102.

Wagner A and De la Chaux N (2008) Distant horizontal gene transfer is rare for multiple families of prokaryotic insertion sequences. Molecular Genetics and Genomics 280: 397–408. DOI: 10.1007/s00438-008-0373-y.

Woese CR , Kandler O and Wheelis M (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proceedings of the National Academy of Sciences United States of America 87: 4576–4579.

Zhaxybayeva O , Gogarten JP , Charlebois RL , Doolittle WF and Papke RT (2006) Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events. Genome Research 16: 1099–1108. DOI: 10.1101/gr.5322306.

Zhaxybayeva O , Swithers KS , Lapierre P , et al. (2009) On the chimeric nature, thermophilic origin, and phylogenetic placement of the Thermotogales. Proceedings of the National Academy of Sciences of the United States of America 106: 5865–5870. DOI: 10.1073/pnas0901260106.

Further Reading

Andersson JO (2009) Gene transfer and diversification of microbial eukaryotes. Annual Review of Microbiology 63: 177–193. DOI: 10.1146/annurev.micro.091208.073203.

Bock R (2010) The give‐and‐take of DNA: horizontal gene transfer in plants. Trends in Plant Science 15: 11–22. DOI: 10.1016/j.tplants.2009.10.001.

Baltrus DA (2013) Exploring the costs of horizontal gene transfer. Trends in Ecology & Evolution 28: 489–495. DOI: 10.1016/j.tree.2013.04.002.

Boto L (2010) Horizontal gene transfer in evolution: facts and challenges. Proceedings of the Royal Society B 277: 819–827. DOI: 10.1098/rspb.2009.1679.

Boto L (2015) Evolutionary change and phylogenetic relationships in light of horizontal gene transfer. Journal of Biosciences 40: 465–472. DOI: 10.1007/s12038-015-9514-8.

Koonin EV and Wolf YI (2009b) The fundamental units, processes and patterns of evolution, and the Tree of Life conundrum. Biology Direct 4: 33. DOI: 10.1186/1745-6150-4-33.

Kuo C‐H and Ochman H (2009) The fate of new bacterial genes. FEMS Microbiological Reviews 33: 38–43. DOI: 10.1111/j.1574-6976.2008.00140.x.

Ragan MA and Beiko RG (2009) Lateral genetic transfer: open issues. Philosophical Transactions of the Royal Society B 364: 2241–2251. DOI: 10.1098/rstb.2009.0031.

Rocha EPC (2008) Evolutionary patterns in prokaryotic genomes. Current Opinion in Microbiology 11: 454–460. DOI: 10.1016/j.mib.2008.09.007.

Schoenknecht G , Weber APM and Lercher MJ (2014) Horizontal gene acquisitions by eukaryotes as drivers of adaptive evolution. Bioessays 36: 9–20. DOI: 10.1002/bies.201300095.

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Boto, Luis(Aug 2015) Horizontal Gene Transfer in Evolution. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0022835.pub2]