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Journal of Molecular Evolution

, Volume 83, Issue 5–6, pp 184–192 | Cite as

Molecular Phylogenetics and the Perennial Problem of Homology

  • S. Andrew Inkpen
  • W. Ford Doolittle
Review

Abstract

The concept of homology has a long history, during much of which the issue has been how to reconcile similarity and common descent when these are not coextensive. Although thinking molecular phylogeneticists have learned not to say “percent homology,” the problems are deeper than that and unresolved.

Keywords

Homology Molecular phylogenetics Philosophy of biology 

Reference

  1. Amundson R (2005) The changing role of the embryo in evolutionary thought: roots of evo-devo. Cambridge University, CambridgeCrossRefGoogle Scholar
  2. Beatty J (2006) Chance variation: Darwin on orchids. Phil Sci 73:629–641CrossRefGoogle Scholar
  3. Belon P (1551) L’histoire naturelle de estranges poissons marins. Renaud Chaudiere, ParisGoogle Scholar
  4. Boyden A (1947) Homology and analogy. A critical review of the meanings and implications of these concepts in biology. Am Midl Nat 37:648–669CrossRefGoogle Scholar
  5. Brigandt I (2003) Homology in comparative, molecular, and evolutionary developmental biology: the radiation of a concept. J Exp Zool 299B:9–17CrossRefGoogle Scholar
  6. Brigandt I (2006) Homology and heterochrony: the evolutionary embryologist Gavin Rylands de Beer (1899-1972). J Exp Zool 306B:317–328CrossRefGoogle Scholar
  7. Bryson V, Vogel HJ (1965) Evolving genes and proteins. Academic Press, New YorkGoogle Scholar
  8. Crick F (1970) Central dogma of molecular biology. Nature 227:561–563CrossRefPubMedGoogle Scholar
  9. Darnell JE, Doolittle WF (1986) Speculations on the early course of evolution. Proc Natl Acad Sci USA 83:1271–1275CrossRefPubMedPubMedCentralGoogle Scholar
  10. Darwin C (1859) On the origin of species by means of natural selection, or the preservation of the favoured races in the struggle for life. John Murray, LondonCrossRefGoogle Scholar
  11. Davis JC, Petrov DA (2004) Preferential duplication of conserved proteins in eukaryotic genomes. PLoS Biol 2(3):0318–0326CrossRefGoogle Scholar
  12. de Beer GR (1971) Homology, an unsolved problem. Oxford University Press, GlasgowGoogle Scholar
  13. Di Gregorio M (1995) A wolf in sheep’s clothing: Carl Gegenbaur, Ernst Haeckel, the vertebral theory of the skull, and the survival of Richard Owen. J Hist Biol 28:247–280CrossRefGoogle Scholar
  14. Dokholyan NV, Shakhnovich EI (2001) Understanding hierarchical protein structure from first principles. J Mol Biol 312:289–307CrossRefPubMedGoogle Scholar
  15. Donoghue MJ (1992) Homology. In: Fox Keller E, Lloyd EA (eds) Keywords in evolutionary biology. Harvard University Press, CambridgeGoogle Scholar
  16. Donoghue MJ, Sanderson MJ (1994) Complexity and homology in plants. In: Hall B (ed) Homology: the hierarchical basis of comparative biology. Academic Press, San Diego, pp 393–421CrossRefGoogle Scholar
  17. Doolittle RF (1994) Convergent evolution—the need to be explicit. Trends Biochem Sci 19:15–18CrossRefPubMedGoogle Scholar
  18. Doolittle RF (1995) The multiplicity of domains in proteins. Annu Rev Biochem 64:287–314CrossRefPubMedGoogle Scholar
  19. Fitch WM (1970) Distinguishing homologous from analogous proteins. Syst Biol 19(2):99–113Google Scholar
  20. Fitch WM (2000) Homology a personal view on some of the problems. Trends Genet 16:227–231CrossRefPubMedGoogle Scholar
  21. Fitch WN, Margoliash E (1967) Construction of phylogenetic trees. Science 155(3760):279–284CrossRefPubMedGoogle Scholar
  22. Gabaldon T, Koonin EV (2013) Functional and evolutionary implications of gene orthology. Nat Rev Genet 14:360–366CrossRefPubMedGoogle Scholar
  23. Gegenbaur K (1878) Grundriß der vergleichenden anatomie. Engelmann, LeipzigCrossRefGoogle Scholar
  24. Gould SJ (1985) A clock of evolution. Nat Hist 4:12–25Google Scholar
  25. Graham LA, Hobbs RS, Fletcher GL, Davies PL (2013) Helical antifreeze proteins have independently evolved in fishes on four occasions. PLoS ONE 8(12):e81285CrossRefPubMedPubMedCentralGoogle Scholar
  26. Gray GS, Fitch WM (1983) Evolution of antibiotic resistance genes: the DNA sequence of a kanamycin resistance gene from Staphylococcus aureus. Mol Biol Evol 1(11):57–66PubMedGoogle Scholar
  27. Haas O, Simpson GG (1946) Analysis of some phylogenetic terms, with attempts at redefinition. Proc Am Philos Soc 90:319–349PubMedGoogle Scholar
  28. Haeckel E (1866) Generelle morphologie der organismen. Reimer, BerlinCrossRefGoogle Scholar
  29. Haggerty LS, Jachiet P-A, Hanage WP, Fitzpatrick DA, Lopez P, O’Connell MJ, Pisani D, Wilkinson M, Bapteste E, McInerney JO (2013) A pluralistic account of homology: adapting the models to the data. Mol Biol Evol 31(3):501–506CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hall BK (1994) Homology: the hierarchical basis of comparative biology. Academic Press, San DiegoGoogle Scholar
  31. Hennig W (1966) Phylogenetic systematics. University of Illinois Press, UrbanaGoogle Scholar
  32. Hertwig O (1906) Handbuch der vergleichenden und experimentellen entwicklungslehre der wirbeltiere. Fisher, JenaGoogle Scholar
  33. Herzoni H, Koppstein D, Schwartz MG, Avrulin A, Bartel DP, Ulitisky I (2015) Principles of long noncoding RNA evolution derived from direct comparison of transcriptomes in 17 species. Cell Rep 11(7):1110–1122CrossRefGoogle Scholar
  34. Hillis DM (1994) Homology in molecular biology. In: Hall BK (ed) Homology: the hierachical basis of comparative biology. Academic Press, NYGoogle Scholar
  35. Hubbs C (1944) Concepts of homology and analogy. Am Nat 78:289–307CrossRefGoogle Scholar
  36. Irwin DM (2015) Genomic organization and evolution of ruminant lysozyme c genes. Zool Res 36(1):1–17PubMedPubMedCentralGoogle Scholar
  37. Kleisner K (2007) The formation of the theory of homology in biological sciences. Acta Biotheor 55:317–340CrossRefPubMedGoogle Scholar
  38. Koonin EN, Martin W (2005) On the origin of genomes and cells within organic departments. Trends Genet 21(12):647–654CrossRefPubMedGoogle Scholar
  39. Lankester R (1870) On the use of the term homology in modern zoology, and the distinction between homogenetic and homoplastic agreements. Ann Mag Nat Hist 6:34–43CrossRefGoogle Scholar
  40. Laubichler M (2000) Homology in development and the development of the homology concept. Am Zool 40:777–788Google Scholar
  41. Mackin KA, Ror RA, Theobald DL (2013) An empirical test of convergent evolution in rhodopsins. Mol Biol Evol 31:85–95CrossRefPubMedPubMedCentralGoogle Scholar
  42. Mindell DP (1991) Similarity and congruence as criteria for molecular homology. Mol Biol Evol 8(6):897–900Google Scholar
  43. Mindell DP, Meyer A (2001) Homology evolving. Trends Ecol Evol 16(8):434–440CrossRefGoogle Scholar
  44. Ohno S (1970) Evolution by gene duplication. Springer, New YorkCrossRefGoogle Scholar
  45. Orengo CA, Thornton JM (2005) Protein families and their evolution—a structural perspective. Annu Rev Biochem 74:867–900CrossRefPubMedGoogle Scholar
  46. Owen R (1843) Lectures on the comparative anatomy and physiology of the invertebrate animals, delivered at the royal college of surgeons in 1843. Longman, Brown, Green, and Longmans, LondonGoogle Scholar
  47. Owen R (1848) On the archetype and homologies of the vertebrate skeleton. John van Voorst, LondonCrossRefGoogle Scholar
  48. Owen R (1849) On the nature of limbs. Voorst, LondonCrossRefGoogle Scholar
  49. Panchen AL (1994) Richard Owen and the concept of homology. In: Hall B (ed) Homology. Academic Press, New York, pp 22–57Google Scholar
  50. Panchen AL (1999) Homology—history of a concept. In: Bock GR, Cardew G (eds) Homology. Wiley, West Sussex, pp 5–18Google Scholar
  51. Patterson C (1982) Morphological characters and homology. In: Joysey KA, Friday AE (eds) Problems of phylogenetic reconstruction. Academic Press, New York, pp 21–74Google Scholar
  52. Patterson C (1987) Molecules and morphology in evolution: conflict or compromise. Cambridge University Press, CambridgeGoogle Scholar
  53. Patterson C (1988) Homology in classical and molecular biology. Mol Biol Evol 5(6):603–625PubMedGoogle Scholar
  54. Pearson WR, Sierk ML (2005) The limits of protein sequence comparison? Curr Opin Struct Biol 15:254–260CrossRefPubMedPubMedCentralGoogle Scholar
  55. Petsko GA (2001) Homologuephobia Genome Biol 2(2); comment1002.1–comment1002.2Google Scholar
  56. Poole AM, Jeffares DC, Penny D (1998) The path from the RNA world. J Mol Evol 46(1):1–17CrossRefPubMedGoogle Scholar
  57. Reeck GR, De Haën C, Teller DC, Doolittle RF, Fitch WM, Dickerson RE, Chambon P, McLachlan AD, Margoliash E, Jukes TH, Zuckerkandl E (1987) Homology in proteins and nucleic acids: a terminology muddle and a way out of it. Cell 50:667CrossRefPubMedGoogle Scholar
  58. Remane A (1952) Die grundlagen des natürlichen systems, der vergleichenden anatomie und der phylogenetik. Akademische Verlagsgesellschaft, LeipzigGoogle Scholar
  59. Richards RJ (1992) The meaning of evolution: the morphological construction and ideological reconstruction of Darwin’s theory. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  60. Roth VL (1984) On homology. Biol J Linn Soc 22:13–29CrossRefGoogle Scholar
  61. Shafee TMA, Lay FT, Hulett MD, Anderson MA (2016) The defensins consist of two independent, convergent protein superfamilies. Mol Biol Evol . doi: 10.1093/molbev/msw106 PubMedGoogle Scholar
  62. Spemann H (1915) Zur geschichte und kritik des begriffs der homologie. In: Chun C, Johannsen W (eds) Die kulturen der gegenwart. Teubner, Leipzig, pp 63–86Google Scholar
  63. Storz JF (2016) Causes of molecular convergence and parallelism in protein evolution. Nat Rev Genet 17:239–250CrossRefPubMedGoogle Scholar
  64. Tait J (1928) Homology, analogy and plasis. Q Rev Biol 3:151–173CrossRefGoogle Scholar
  65. Treangen TJ, Rocha EPC (2011) Horizontal transfer, not duplication, drives the expansion of protein families in prokaryotes. PLoS Genet 7(1):e1001284CrossRefPubMedPubMedCentralGoogle Scholar
  66. Wagner GP (1989a) The biological homology concept. Annu Rev Ecol Syst 20:51–69CrossRefGoogle Scholar
  67. Wagner GP (1989b) The origin of morphological characters and the biological basis of homology. Evolution 43:1157–1171CrossRefGoogle Scholar
  68. Wagner GP (2014) Homology, genes and evolutionary innovation. Princeton University Press, PrincetonCrossRefGoogle Scholar
  69. Wake D (1994) Comparative terminology. Science 265:268–269CrossRefPubMedGoogle Scholar
  70. Wake D (1999) Homoplasy, homology and the problem of ‘sameness’ in biology. In: Bock GR, Cardew G (eds) Homology. Wiley, West Sussex, pp 24–32Google Scholar
  71. Williams GC (1966) Adaptation and natural selection. Princeton University Press, PrincetonGoogle Scholar
  72. Wray GA (1999) Evolutionary dissociations between homologous genes and homologous structures. Homology: Novartis Foundation Symposium 222. Wiley, Chichester, pp 189–206Google Scholar
  73. Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 97–166CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Department of Biochemistry and Molecular BiologyDalhousie UniversityHalifaxCanada
  2. 2.Department of PhilosophyDalhousie UniversityHalifaxCanada

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