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Homology in the Age of Developmental Genomics

  • Günter P. Wagner

Abstract

The homology concept was introduced into pre-Darwinian evolutionary biology by Richard Owen as referring to “the same organ in different animals regardless of form and function”. Since then, it has played not only a fundamental role as an organizing idea in comparative anatomy but also an important role in preparing the way for evolutionary biology. Homology is the primary evidence for phylogenetic relationships among organisms, and whenever we project experimental results from a model organism onto humans, we assume homology among the mechanisms in humans and the model organism. Homology was fully integrated into the Darwinian tradition through Lankester’s redefinition as an organ in two species that is derived from the same organ in the most recent common ancestor of the two species. Nevertheless, the homology concept remains controversial primarily because it seems to escape a simple rigorous definition. Homology shares this attribute with other fundamental concepts like that of species or gene. In addition, homology is hard to pin down mechanistically. Apparently, homology is among the concepts biologists have a hard time living with but certainly can’t live without. This situation often leads to considerable frustration among biologists, and some have suggested abandoning the concept altogether and may even result in proposals to abandon the concept altogether, a move that is hardly feasible.

Keywords

Body Part Character State Gene Regulatory Network Transcription Factor Gene Character Modality 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

I thank Professor Andreas Wanninger for the invitation to participate in this important project as well as for comments and corrections to a previous version of this paper. I am also grateful to Jake Musser for suggestions and edits of the manuscript. Finally, I thank all current and former members of my lab for intellectual companionship during the long time these ideas were developed.

References

  1. Amundson R (2005) The changing role of the embryo in evolutionary thought: roots of Evo-Devo. Cambridge University Press, Cambridge, xii, 280ppGoogle Scholar
  2. Arendt D (2008) The evolution of cell types in animals: emerging principles from molecular studies. Nat Rev Genet 9:868–882PubMedCrossRefGoogle Scholar
  3. Brawand D, Soumillon M, Necsulea A, Julien P, Csardi G, Harrigan P et al (2011) The evolution of gene expression levels in mammalian organs. Nature 478:343–348PubMedCrossRefGoogle Scholar
  4. Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ (2013) Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat Methods 10:1213–1218PubMedCentralPubMedCrossRefGoogle Scholar
  5. Carroll SB (2008) Evo-Devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134:25–34PubMedCrossRefGoogle Scholar
  6. Czerny T, Halder G, Kloter U, Souabni A, Gehring WJ, Busslinger M (1999) Twin of eyeless, a second Pax-6 gene of Drosophila, acts upstream of eyeless in the control of eye development. Mol Cell 3:297–307PubMedCrossRefGoogle Scholar
  7. Damen WG (2007) Evolutionary conservation and divergence of the segmentation process in arthropods. Dev Dyn 236:1379–1391PubMedCrossRefGoogle Scholar
  8. Davidson E (2001) Genomic regulatory systems. Academic, San Diego, xii, 261Google Scholar
  9. de Beer GR (1971) Homology, an unsolved problem. Oxford University Press, London, 16ppGoogle Scholar
  10. Deutsch J (2005) Hox and wings. Bioessays 27:673–675PubMedCrossRefGoogle Scholar
  11. Dobzhansky T (1937) Genetics of the evolutionary process. Columbia University Press, New York, xiii, 505Google Scholar
  12. Donoghue MJ (1989) Phylogenies and the analysis of evolutionary sequences, with examples from seed plants. Evolution 43:1137–1156CrossRefGoogle Scholar
  13. Donoghue MJ (1992) Homology. In: Keller EF, Lloyd EA (eds) Keywords in evolutionary biology. Harvard University Press, Cambridge, MA, pp 171–179Google Scholar
  14. Felsenstein J (2003) Inferring phylogenies. Sinauer, Sunderland, xx, 664Google Scholar
  15. Friedrich M (2006) Ancient mechanisms of visual sense organ development based on comparison of the gene networks controlling larval eye, ocellus, and compound eye specification in Drosophila. Arthropod Struct Dev 35:357–378PubMedCrossRefGoogle Scholar
  16. Geeta R (2003) Structure trees and species trees: what they say about morphological development and evolution. Evol Dev 5:609–621PubMedCrossRefGoogle Scholar
  17. Gegenbaur C (1876) Zur Morphologie der Gliedmassen der Wirbeltiere. Morphologisches Jahrb 2:396–420Google Scholar
  18. Ghiselin MT (2005) Homology as a relation of correspondence between parts of individuals. Theory Biosci 124:91–103PubMedCrossRefGoogle Scholar
  19. Graf T, Enver T (2009) Forcing cells to change lineages. Nature 462:587–594PubMedCrossRefGoogle Scholar
  20. Graur D, Li W-H (2000) Fundamentals of molecular evolution, 2nd edn. Sinauer Ass. Inc, Sunderland, xiv, 481Google Scholar
  21. Hall BK (2003) Descent with modification: the unity underlying homology and homoplasy as seen through an analysis of development and evolution. Biol Rev Camb Philos Soc 78:409–433PubMedCrossRefGoogle Scholar
  22. Hallgrimsson B, Jamniczky H, Young NM, Rolian C, Parsons TE, Boughner JC et al (2009) Deciphering the palimpsest: studying the relationship between morphological integration and phenotypic covariation. Evol Biol 36:355PubMedCentralPubMedCrossRefGoogle Scholar
  23. Hebenstreit D, Fang M, Gu M, Charoensawan V, van Oudenaarden A, Teichmann SA (2011) RNA sequencing reveals two major classes of gene expression levels in metazoan cells. Mol Syst Biol 7:497PubMedCentralPubMedCrossRefGoogle Scholar
  24. Hennig W (1966) Phylogenetic systematics. University of Illinois Press, Urbana, 263Google Scholar
  25. Hobert O (2011) Regulation of terminal differentiation programs in the nervous system. Annu Rev Cell Dev Biol 27:681–696PubMedCrossRefGoogle Scholar
  26. Kin K, Nnamani MC, Lynch VJ, Michaelides E, Wagner GP (2015) Cell type phylogenetics and the origin of endometrial stromal cells. Cell Reports 10:1398–1409Google Scholar
  27. Lankester RE (1870) On the use of the term homology in modern zoology, and the distinction between homogenetic and homoplastic agreement. Annu Mag Nat Hist 6:34–43CrossRefGoogle Scholar
  28. Lynch VJ, Tanzer A, Wang Y, Leung FC, Gellersen B, Emera D et al (2008) Adaptive changes in the transcription factor HoxA-11 are essential for the evolution of pregnancy in mammals. Proc Natl Acad Sci U S A 105:14928–14933PubMedCentralPubMedCrossRefGoogle Scholar
  29. Lynch VJ, May G, Wagner GP (2011) Regulatory evolution through divergence of a phosphoswitch in the transcription factor CEBPB. Nature 480:383–386PubMedCrossRefGoogle Scholar
  30. Maddison WP, Donoghue MJ, Maddison DR (1984) Outgroup analysis and parsimony. Syst Zool 33:83–103CrossRefGoogle Scholar
  31. Mayr E (1942) Systematics and the origin of species. Columbia University Press, New York, xiv, 334Google Scholar
  32. Mayr E (1982) The growth of biological thought. The Belknap Press, Cambridge, ix, 974Google Scholar
  33. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628PubMedCrossRefGoogle Scholar
  34. Müller GB (2010) Epigenetic innovation. In: Pigliucci M, Müller GB (eds) Evolution – the extended synthesis. MIT Press, Boston, pp 307–332CrossRefGoogle Scholar
  35. Müller GB, Newman SA (1999) Generation, integration, autonomy: three steps in the evolution of homology. In: Bock GR, Cardew G (eds) Homology. Wiley, New York, pp 65–79Google Scholar
  36. Müller GB, Wagner GP (1991) Novelty in evolution: restructuring the concept. Ann Rev Ecol Syst 22:229–256CrossRefGoogle Scholar
  37. Musser J, Wagner GP, Prum RO (2015) Nuclear β-catenin expression supports homology of feather, avian scutate scale, and alligator scale early development J Exp Zoo (Mol Dev Evol) [in press]Google Scholar
  38. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York, x, 512Google Scholar
  39. Neph S, Stergachis AB, Reynolds A, Sandstrom R, Borenstein E, Stamatoyannopoulos JA (2012a) Circuitry and dynamics of human transcription factor regulatory networks. Cell 150:1274–1286PubMedCentralPubMedCrossRefGoogle Scholar
  40. Neph S, Vierstra J, Stergachis AB, Reynolds AP, Haugen E, Vernot B et al (2012b) An expansive human regulatory lexicon encoded in transcription factor footprints. Nature 489:83–90PubMedCentralPubMedCrossRefGoogle Scholar
  41. Oakley TH (2003) The eye as a replicating and diverging, modular developmental unit. Trends Ecol Evol 18:623–627CrossRefGoogle Scholar
  42. Oakley TH, Plachetzki DC, Rivera AS (2007) Furcation, field-splitting, and the evolutionary origins of novelty in arthropod photoreceptors. Arthropod Struct Dev 36:386–400PubMedCrossRefGoogle Scholar
  43. Oliveri P, Tu Q, Davidson EH (2008) Global regulatory logic for specification of an embryonic cell lineage. Proc Natl Acad Sci U S A 105:5955–5962PubMedCentralPubMedCrossRefGoogle Scholar
  44. Owen R (1848) On the archetype and homologies of the vertebrate skeleton. Voorst, London, viii, 203Google Scholar
  45. Patterson C (1982) Morphological characters and homology. In: Joysey KA, Friday AE (eds) Problems of phylogenetic reconstruction. Academic, London, pp 21–74Google Scholar
  46. Pavlicev M, Widder S (2015) Wiring for independence: positive feedback motifs facilitate individuation of traits in development and evolution. J Exp Zool (Mol Dev Evol) 324B:104–113Google Scholar
  47. Raff R (1996) The shape of life. Chicago University Press, Chicago, xxiii, 520Google Scholar
  48. Ree RH, Donoghue MJ (1999) Inferring rates of change in flower symmetry in asterid angiosperms. Syst Biol 48:633–641CrossRefGoogle Scholar
  49. Remane A (1952) Die Grundlagen des natürlichen systems, der vergleichenden Anatomie und der Phylogenetik. Akademische Verlagsgesellschaft Geest & Portig, Leipzig, vi, 364Google Scholar
  50. Riedl R (1978) Order in living organisms: a systems analysis of evolution. Wiley, New York, xx, 313Google Scholar
  51. Rieppel OC (1988) Fundamentals of comparative biology. Birkhäuser, BaselGoogle Scholar
  52. Roth VL (1988) The biological basis of homology. In: Humphries CJ (ed) Ontogeny and systematics. Columbia University Press, New York, pp 1–26Google Scholar
  53. Simpson GG (1961) Principles of animal taxonomy. Columbia University Press, New York, 247ppGoogle Scholar
  54. Sommer RJ, Sternberg PW (1994) Changes of induction and competence during the evolution of vulva development in nematodes. Science 265:114–118PubMedCrossRefGoogle Scholar
  55. Spemann H (1915) Zur Geschichte und Kritik des Begriffs der Homologie. In: Chun C, Johannsen W (eds) Allgemeine Biologie, vol 3. Teubner, Leipzig, pp 63–86Google Scholar
  56. Tomoyasu Y, Wheeler SR, Denell RE (2005) Ultrabithorax is required for membranous wing identity in the beetle Tribolium castaneum. Nature 433:643–647PubMedCrossRefGoogle Scholar
  57. Wagner GP (1994) Homology and the mechanisms of development. In: Hall BK (ed) Homology: the hierarchical basis of comparative biology. Academic, San Diego, xiii, 478ppGoogle Scholar
  58. Wagner GP (2007) The developmental genetics of homology. Nat Rev Genet 8:473–479PubMedCrossRefGoogle Scholar
  59. Wagner GP (2014) Homology, genes and evolutionary Innovation. Princeton University Press, PrincetonCrossRefGoogle Scholar
  60. Wagner GP, Lynch VJ (2010) Evolutionary novelties. Curr Biol 20:R48–R52PubMedCrossRefGoogle Scholar
  61. Wagner GP, Misof BY (1993) How can a character be developmentally constrained despite variation in developmental pathways? J Evol Biol 6:449–455CrossRefGoogle Scholar
  62. Wagner GP, Kin K, Lynch VJ (2012) Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples. Theory Biosci 131:281–285PubMedCrossRefGoogle Scholar
  63. Wagner GP, Kin K, Lynch VJ (2013) A model based criterion for gene expression calls using RNA-seq data. Theory Biosci 132:159–164PubMedCrossRefGoogle Scholar
  64. Wake DB (2003) Homology and homoplasy. In: Hall BK, Olson WM (eds) Keywords and concepts in evolutionary developmental biology, vol 191–201. Harvard University Press, Cambridge, MAGoogle Scholar
  65. Wang Z, Young RL, Xue H, Wagner GP (2011) Transcriptomic analysis of avian digits reveals conserved and derived digit identities in birds. Nature 477:583–586PubMedCrossRefGoogle Scholar
  66. Weatherbee SD, Halder G, Kim J, Hudson A, Carroll S (1998) Ultrabithorax regulates genes at several levels of the wing-patterning hierarchy to shape the development of the Drosophila haltere. Genes Dev 12:1474–1482PubMedCentralPubMedCrossRefGoogle Scholar
  67. Weatherbee SD, Frederik Nijhout H, Grunert LW, Halder G, Galant R, Selegue J et al (1999) Ultrabithorax function in butterfly wings and the evolution of insect wing patterns. Curr Biol 9:109–115PubMedCrossRefGoogle Scholar
  68. Weiss KM (1990) Duplication with variation: metameric logic in evolution from genes to morphology. Yearb Phys Anthropol 33:1–23CrossRefGoogle Scholar
  69. Wilkins AS (2002) The evolution of developmental pathways. Sinauer Assoc, Sunderland, xvii, 603ppGoogle Scholar
  70. Wray GA, Abouheif E (1998) When is homology not homology? Curr Opin Genet Dev 8:675–680PubMedCrossRefGoogle Scholar
  71. Young RL, Caputo V, Giovannotti M, Kohlsdorf T, Vargas AO, May GE et al (2009) Evolution of digit identity in the three-toed skink Chalcides chalcides: a new case of digit identity frame shift. Evol Dev 11:647–658PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2015

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyYale Systems Biology InstituteNew HavenUSA
  2. 2.Department of Obstetrics, Gynecology and Reproductive SciencesYale UniversityNew HavenUSA

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