Development Genes and Evolution

, Volume 213, Issue 3, pp 149–154 | Cite as

Patterns of gene expression: homology or homocracy?

  • Claus Nielsen
  • Pedro Martinez
Hypothesis Paper


Numerous papers over the years have stated that the original meaning of the term homology is historical and morphological and denotes organs/structures in two or more species derived from the same structure in their latest common ancestor. However, several more recent papers have extended the use of the term to cover organs/structures which are organised through the expression of homologous genes. This usage has created an ambiguity about the meaning of the term, and we propose to remove this by proposing a new term, homocracy, for organs/structures which are organised through the expression of identical patterning genes. We want to emphasise that the terms homologous and homocratic are not mutually exclusive. Many homologous structures are in all probability homocratic, whereas only a small number of homocratic structures are homologous.


Homology Homocracy Evolution Patterning Gene 


  1. Abouheif E, Akam M, Dickinson WJ, Holland PWH, Meyer A, Patel NH, Raff RA, Roth LV, Wray GA (1997) Homology and developmental genes. Trends Genet 13:432–433CrossRefPubMedGoogle Scholar
  2. Abzhanov A, Kaufman TC (2000) Homologs of Drosophila appendage genes in the patterning of arthropod limbs. Dev Biol 227:673–689CrossRefPubMedGoogle Scholar
  3. Ackerman H, Udalova I, Hull J, Kwiatkowski D (2002) Evolution of a polymorphic regulatory element in interferon-γ through transposition and mutation. Mol Biol Evol 19:884–890PubMedGoogle Scholar
  4. Akimenko MA, Ekker M, Wegner J, Lin W, Westerfield M (1994) Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J Neurosci 14:3475–3486PubMedGoogle Scholar
  5. Aspock G, Burglin TR (2001) The Caenorhabditis elegans distal-less ortholog ceh-43 is required for development of the anterior hypodermis. Dev Dyn 222:403–409CrossRefPubMedGoogle Scholar
  6. Beermann A, Jay DG, Beeman RW, Hulskamp M, Tautz D, Jurgens G (2001) The Short antennae gene of Tribolium is required for limb development and encodes the orthologue of the Drosophila Distal-less protein. Development 128:287–297PubMedGoogle Scholar
  7. Beldade P, Brakefield PM, Long AD (2002) Contribution of Distal-less to quantitative variation in butterfly eyespots. Nature 415:315–318CrossRefPubMedGoogle Scholar
  8. Belting HG, Shashikant CS, Ruddle FH (1998) Modification of expression and cis-regulation of Hoxc8 in the evolution of diverged axial morphology. Proc Natl Acad Sci USA 95:2355–2360CrossRefPubMedGoogle Scholar
  9. Callaerts P, Leng S, Clements J, Benassayag C, Cribbs D, Kang YY, Walldorf U, Fischbach K-K, Strauss R (2001) Drosophila Pax-6/eyeless is essential for normal adult brain structure and function. J Neurobiol 46:73–88CrossRefPubMedGoogle Scholar
  10. Caracciolo A, Di Gregorio A, Aniello F, Di Lauro R, Branno M (2000) Identification and developmental expression of three Distal-less homeobox-containing genes in the ascidian Ciona intestinalis. Mech Dev 99:173–176CrossRefPubMedGoogle Scholar
  11. Carosa E, Kozmik Z, Rall JE, Piatigorsky J (2002) Structure and expression of the scallop Ω-crystallin gene. J Biol Chem 277:656–664CrossRefPubMedGoogle Scholar
  12. Cohen SM (1990) Specification of limb development in the Drosophila embryo by positional cues from segmentation genes. Nature 343:173–177PubMedGoogle Scholar
  13. Cohen SM, Bronner G, Kuttner F, Jurgens G, Jackle H (1989) Distal-less encodes a homoeodomain protein required for limb development in Drosophila. Nature 338:432–434PubMedGoogle Scholar
  14. Conklin EG (1897) The embryology of Crepidula. J Morphol 13:1-226, pls 1–9Google Scholar
  15. Czihak G (1960) Untersuchungen über die Coelomanlagen und die Metamorphose des Pluteus von Psammechinus miliaris (Gmelin). Zool Jb Anat 78:235–256, pls 1–2Google Scholar
  16. Darwin C (1859) On the origin of species by means of natural selection. John Murray, LondonGoogle Scholar
  17. Davidson EH (2001) Genomic regulatory systems. Development and evolution. Academic Press, San DiegoGoogle Scholar
  18. Davidson EH, Rast JP, Oliveri P, Ransick A, Calestani C, Yuh CH, Minokawa T, Amore G, Hinman V, Arenas-Mena C, Otim O, Brown CT, Livi CB, Lee PY, Revilla R, Rust AG, Pan Z, Schilstra MJ, Clarke PJ, Arnone MI, Rowen L, Cameron RA, McClay DR, Hood L, Bolouri H (2002) A genomic regulatory network for development. Science 295:1669–1678CrossRefPubMedGoogle Scholar
  19. Dobzhansky T (1973) Nothing in biology makes sense except in the light of evolution. Am Biol Teach 35:125–129Google Scholar
  20. Gauchat D, Mazet F, Berney C, Summer M, Kreger S, Pawlowsky J, Galliot B (2000) Evolution of Antp-class genes and differential expression of Hydra Hox/paraHox genes in anterior patterning. Proc Natl Acad Sci USA 97:4493–4498CrossRefPubMedGoogle Scholar
  21. Gehring WJ (2002) The genetic control of eye development and its implications for the evolution of the various eye-types. Int J Dev Biol 46:65–73Google Scholar
  22. Gehring W, Ikeo K (1999) Pax 6 mastering eye morphogenesis and eye evolution. Trends Genet 15:371–377Google Scholar
  23. Gilbert SF, Bolker JA (2001) Homologies of process and modular elements of embryonic construction. J Exp Zool 291:1-12CrossRefPubMedGoogle Scholar
  24. Gonzalez-Crespo S, Morata G (1996) Genetic evidence for the subdivision of the arthropod limb into coxopodite and telopodite. Development 122:3921–3928PubMedGoogle Scholar
  25. Gorfinkiel N, Sanchez L, Guerrero I (1999) Drosophila terminalia as an appendage-like structure. Mech Dev 86:113–123CrossRefPubMedGoogle Scholar
  26. Gould SJ (2002) The structure of evolutionary theory. Harvard University Press, Cambridge, Mass.Google Scholar
  27. Hall BK (1994) Introduction. In: BK Hall (ed) Homology. The hierarchical basis of comparative biology. Academic Press, San Diego, pp 1–19Google Scholar
  28. Harada Y, Okai N, Taguchi S, Shoguchi E, Tagawa K, Humphreys T, Satoh N (2001) Embryonic expression of a hemichordate distal-less gene. Zool Sci 18:57–61Google Scholar
  29. Haun C, Alexander J, Stainier DY, Okkema PG (1998) Rescue of Caenorhabditis elegans pharyngeal development by a vertebrate heart specification gene. Proc Natl Acad Sci USA 95:5072–5075CrossRefPubMedGoogle Scholar
  30. Holland ND, Panganiban G, Henyey EL, Holland LZ (1996) Sequence and developmental expression of AmphiDll, an amphioxus Distal-less gene transcribed in the ectoderm, epidermis and nervous system: insights into evolution of craniate forebrain and neural crest. Development 122:2911–2920PubMedGoogle Scholar
  31. Jockusch EL, Nulsen C, Newfeld SJ, Nagy LM (2000) Leg development in flies versus grasshoppers: differences in dpp expression do not lead to differences in the expression of downstream components of the leg patterning pathway. Development 127:1617–1626PubMedGoogle Scholar
  32. Kaestner A (1963) Lehrbuch der Speziellen Zoologie, Teil 1. 5. Lieferung. Fischer, Jena, pp 981–1423Google Scholar
  33. Kishinouye K (1891) On the development of Limulus longispinus. J Coll Sci Imp Univ Tokyo 5:53–100, pls 5–11Google Scholar
  34. Larsson L-I, St-Onge L, Hougaard DM, Sosa-Pineda B, Gruss P (1998). Pax 4 and 6 regulate gastrointestinal endocrine cell development. Mech Dev 79:153–159CrossRefPubMedGoogle Scholar
  35. Lee SE, Jacobs DK (1999) Expression of Distal-less in molluscan eggs, embryos, and larvae. Evol Dev 1:172–179CrossRefPubMedGoogle Scholar
  36. Lowe CJ, Wray GA (1997) Radical alterations in the roles of homeobox genes during echinoderm evolution. Nature 389:718–721PubMedGoogle Scholar
  37. Lowe CJ, Issel-Tarver L, Wray GA (2002) Gene expression and larval evolution: changing roles of distal-less and orthodenticle in echinoderm larvae. Evol Dev 4:111–123CrossRefPubMedGoogle Scholar
  38. Ludwig MZ, Bergman C, Patel NH, Kreitman M (2000) Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 403:564–567CrossRefPubMedGoogle Scholar
  39. Maduro MF, Meneghini MD, Bowerman B, Broitman-Maduro G, Tothman JH (2001) Restriction of mesendoderm to a single blastomere by the combined action of SKN-1 and a GSK-3β homolog is mediated by MED-1 and 1- in C. elegans. Mol Cell 7:475–485PubMedGoogle Scholar
  40. Merlo GR, Zerega B, Paleari L, Trombino S, Mantero S, Levi G (2000) Multiple functions of Dlx genes. Int J Dev Biol 44(6):619–626PubMedGoogle Scholar
  41. Miller DJ, Hayward DC, Reece-Hoyes JS, Scholten I, Catmull J, Gehring WJ, Callaerts P, Larsen JE, Ball EE (2000) Pax gene diversity in the basal cnidarian Acropora millepora (Cnidaria, Anthozoa): implications for the evolution of the Pax gene family. Proc Natl Acad Sci USA 97:4475–4480CrossRefPubMedGoogle Scholar
  42. Mittmann B, Scholtz G (2001) Distal-less expression in embryos of Limulus polyphemus (Chelicerata, Xiphosura) and Lepisma saccharina (Insecta, Zygentoma) suggests a role in the development of mechanoreceptors, chemoreceptors, and the CNS. Dev Genes Evol 211:232–243CrossRefPubMedGoogle Scholar
  43. Morasso MI, Mahon KA, Sargent TD (1995) A Xenopus distal-less gene in transgenic mice: conserved regulation in distal limb epidermis and other sites of epithelial-mesenchymal interaction. Proc Natl Acad Sci USA 92:3968–3972PubMedGoogle Scholar
  44. Neidert AH, Virupannavar V, Hooker GW, Langeland JA (2001) Lamprey Dlx genes and early vertebrate evolution. Proc Natl Acad Sci USA 98:1665–1670CrossRefPubMedGoogle Scholar
  45. Niehrs C, Pollett N (1999) Synexpression groups in eukaryotes. Nature 402:483–487CrossRefPubMedGoogle Scholar
  46. Nielsen C (2001) Animal evolution. Interrelationships of the living phyla, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  47. Nilsson D-E (1990) From cornea to retinal image in invertebrate eyes. Trends Neurosci 13:55–64PubMedGoogle Scholar
  48. Nilsson D-E (1994). Eyes as optical alarm systems in fan worms and ark clams. Philos Trans R Soc B 346:195–212Google Scholar
  49. Nilsson D-E (1996) Eye ancestry: old genes for new eyes. Curr Biol 6:39–42PubMedGoogle Scholar
  50. Nilsson D-E, Pelger S (1994) A pessimistic estimate of the time required for an eye to evolve. Proc R Soc Lond B 256:53–58PubMedGoogle Scholar
  51. Oakley TH, Cunningham CW (2002) Molecular phylogenetic evidence for the independent evolutionary origin of an arthropod compound eye. Proc Natl Acad Sci USA 99:1426–1430CrossRefPubMedGoogle Scholar
  52. Owen R (1843) Lectures on the comparative anatomy and physiology of the invertebrate animals. Longman, Brown, Green and Longman, LondonGoogle Scholar
  53. Panganiban G (2000) Distal-less function during Drosophila appendage and sense organ development. Dev Dyn 218:554–562CrossRefPubMedGoogle Scholar
  54. Panganiban G, Irvine SM, Lowe C, Roehl H, Corley LS, Sherbon B, Grenier JK, Fallon JF, Kimble J, Walker M, Wray GA, Swalla BJ, Martindale MQ, Carroll SB. (1997) The origin and evolution of animal appendages. Proc Natl Acad Sci USA 94(10):5162–5166CrossRefPubMedGoogle Scholar
  55. Piatigorsky J, Horwitz J, Kuwabara T, Cutress CE (1989) The cellular eye lens and crystallins of cubomedusan jellyfish. J Comp Physiol A 164:577–587PubMedGoogle Scholar
  56. Pineda D, Rossi L, Batistoni R, Salvetti A, Marsal M, Gremigni V, Falleni A, Gonzalez-Linares J, Deri P, Salo E (2002) The genetic network of prototypic planarian eye regeneration is Pax6 independent. Development 129:1423–1434PubMedGoogle Scholar
  57. Price M, Lemaistre M, Pischetola M, Di Lauro R, Duboule D (1991) A mouse gene related to Distal-less shows a restricted expression in the developing forebrain. Nature 351:748–751PubMedGoogle Scholar
  58. Prpic NM, Wigand B, Damen WG, Klingler M (2001) Expression of dachshund in wild-type and Distal-less mutant Tribolium corroborates serial homologies in insect appendages. Dev Genes Evol 211:467–477CrossRefPubMedGoogle Scholar
  59. Quint E, Zerucha T, Ekker M (2000) Differential expression of orthologous Dlx genes in zebrafish and mice: implications for the evolution of the Dlx homeobox gene family. J Exp Zool 288:235–241CrossRefPubMedGoogle Scholar
  60. Robledo RF, Rajan L, Li X, Lufkin T (2002) The Dlx5 and Dlx6 homeobox genes are essential for craniofacial, axial, and appendicular skeletal development. Genes Dev 16:1089–1101CrossRefPubMedGoogle Scholar
  61. Rodaway A, Patient R (2001) Mesendoderm: an ancient germ layer? Cell 105:169–172CrossRefPubMedGoogle Scholar
  62. Schilling TF, Knight RD (2001) Origins of anteroposterior patterning and Hox gene regulation during chordate evolution. Philos Trans R Soc Lond B 356:1599–1613CrossRefGoogle Scholar
  63. Schoppmeier M, Damen WG (2001) Double-stranded RNA interference in the spider Cupiennius salei: the role of Distal-less is evolutionarily conserved in arthropod appendage formation. Dev Genes Evol 211:76–82CrossRefPubMedGoogle Scholar
  64. Tabin CJ, Carroll SB, Panganiban G (1999) Out on a limb: parallels in vertebrate and invertebrate limb patterning and the origin of appendages. Am Zool 39:650–663Google Scholar
  65. Tautz D (1998) Debatable homologies. Nature 395:17–19CrossRefPubMedGoogle Scholar
  66. Tautz D (2000) Evolution of transcriptional regulation. Curr Opin Genet Dev 10(5):575–579CrossRefPubMedGoogle Scholar
  67. Tomarev SI, Callaerts SI, Kos L, Zinovieva R, Halder G, Gehring W, Piatigorsky J (1997) Squid Pax-6 and eye development. Proc Natl Acad Sci USA 94:2421–2426CrossRefPubMedGoogle Scholar
  68. Williams TA, Nulsen C, Nagy LM (2002). A complex role for distal-less in crustacean appendage development. Dev Biol 241:302–312CrossRefPubMedGoogle Scholar
  69. Zerucha T, Ekker M (2000) Distal-less-related homeobox genes of vertebrates: evolution, function, and regulation. Biochem Cell Biol 78:593–601CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Zoological MuseumUniversity of Copenhagen CopenhagenDenmark
  2. 2.Department of Anatomy and Cell BiologyUniversity of Bergen BergenNorway

Personalised recommendations