Genes, Evolution and the Development of the Embryo

  • Giuseppina Barsacchi


Evolutionary Developmental Biology (Evo-Devo) deals with the relationships between the individual development and the phenotypic changes of the organism during evolution. Major morphological transitions in evolution are presently recognized to be accommodated by a few key developmental genetic changes (part of a “developmental reprogramming”) and “case studies” in snakes, ducks, bats, dolphins, insects, and finches, providing examples of developmental bases of evolutionary change, are presented. On the other hand, the molecular changes occur in an otherwise conserved developmental genetics tool-kit (e.g., the Hox genes for anterior-posterior patterning, the network for eye formation) representing the “deep homology” underlying diversity of forms. Based on a relationship between embryo development and organism evolution, Evo-Devo represents a synthesis between Developmental and Evolutionary Biology.


Apical Ectodermal Ridge Evolutionary Developmental Biology Developmental Regulatory Gene Rhabdomeric Photoreceptor Ciliary Photoreceptor 
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.



I regret that space constraints make it impossible to cite all relevant work and I therefore apologize to those whose work could not be cited. Additional references may be found in the cited papers. I am grateful to all Authors who were the source for this work and in particular to Prof. S.F. Gilbert, whose seminars and writings raised my interest in Evo-Devo. I wish to thank Prof. S.F. Gilbert and Prof. A. Abzhanov for their kind and generous gift of some pictures. I am also grateful to the Academies that organized the meeting on “The Theory of evolution and its impact” in Turin, May 27–29, 2010, for giving me the opportunity to present some of the present work in the genetics program of Evo-Devo.


  1. 1.
    Arthur W (2004) Biased embryos and evolution. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  2. 2.
    Darwin Francis (1887) The life and letters of Charles Darwin, including an autobiographical chapter, vol 2. John Murray, LondonGoogle Scholar
  3. 3.
    Darwin CR (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life, 1st edn. John Murray, LondonGoogle Scholar
  4. 4.
    Darwin CR (1854) A monograph on the sub-class Cirripedia, with figures of all the species. The Balanidæ, (or sessile cirripedes); the Verrucidæ, etc. etc. etc, vol 2. The Ray Society, LondonGoogle Scholar
  5. 5.
    Darwin CR (1874) The descent of man, and selection in relation to sex, 2nd edn. John Murray, LondonGoogle Scholar
  6. 6.
    Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965–968PubMedCrossRefGoogle Scholar
  7. 7.
    Huxley TH (1893) Evolution in biology. Darwiniana. Collected essays. II. Macmillan, LondonGoogle Scholar
  8. 8.
    Huxley J (1942) Evolution: the modern synthesis. George Allan & Unwin, LondonGoogle Scholar
  9. 9.
    Jacob F (1977) Evolution and tinkering. Science 196:1161–1166PubMedCrossRefGoogle Scholar
  10. 10.
    Carrol SB, Grenier JK, Weatherbee SD (2005) From DNA to diversity. Molecular genetics and the evolution of animal design, 2nd edn. Blackwell, MaldenGoogle Scholar
  11. 11.
    Gilbert SF (2010) Developmental biology, 9th edn. Sinauer Associates, SunderlandGoogle Scholar
  12. 12.
    Shubin N, Tabin C, Carrol S (2009) Deep homology and the origin of evolutionary novelty. Nature 457:818–823PubMedCrossRefGoogle Scholar
  13. 13.
    Salvini-Plawen LV, Mayr E (1977) On the evolution of photoreceptors and eyes. In: Hecht MK, Steere WC, Wallace B (eds) Evolutionary biology, vol 10. Plenum, New York, pp 207–263Google Scholar
  14. 14.
    Gehring WJ, Ikeo K (1999) Pax6: mastering eye morphogenesis and eye evolution. Trends Genet 15:371–377PubMedCrossRefGoogle Scholar
  15. 15.
    Kumar JP, Moses K (2001) Eye specification in Drosophila: perspectives and implications. Semin Cell Dev Biol 12:469–474PubMedCrossRefGoogle Scholar
  16. 16.
    Zuber ME, Gestri G, Viczian AS, Barsacchi G, Harris WA (2003) Specification of the vertebrate eye by a network of eye field transcription factors. Development 130:5155–5167PubMedCrossRefGoogle Scholar
  17. 17.
    Kozmik Z, Daube M, Frei E, Norman B, Kos L, Dishaw LJ, Noll M, Piatigorsky J (2003) Role of Pax genes in eye evolution: a cnidarian PaxB gene uniting Pax2 and Pax6 functions. Dev Cell 5:773–785PubMedCrossRefGoogle Scholar
  18. 18.
    Tomarev SI, Callaerts P, Kos L, Zinovieva R, Halder G, Gehring W, Piatigorsky J (1997) Squid Pax-6 and eye development. Proc Natl Acad Sci USA 94:2421–2426PubMedCrossRefGoogle Scholar
  19. 19.
    Glardon S, Callaerts P, Halder G, Gehring WJ (1997) Conservation of Pax-6 in a lower chordate, the ascidian Phallusia mammillata. Development 124:817–825PubMedGoogle Scholar
  20. 20.
    Gehring WJ (2005) New perspectives on eye development and the evolution of eyes and photoreceptors. J Hered 96:171–184PubMedCrossRefGoogle Scholar
  21. 21.
    Arendt D, Wittbrodt J (2001) Recostructing the eyes of Urbilateria. Phil Trans R Soc Lond B 356:1545–1563CrossRefGoogle Scholar
  22. 22.
    Arendt D (2003) Evolution of eyes and photoreceptor cell types. Int J Dev Biol 47:563–571PubMedGoogle Scholar
  23. 23.
    Arendt D, Tessmar-Raible K, Snyman H, Dorresteijn AW, Wittbrodt J (2004) Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science 306:869–871PubMedCrossRefGoogle Scholar
  24. 24.
    Arendt D (2008) The evolution of cell types in animals: Emerging principles from molecular studies. Nature 9:868–880Google Scholar
  25. 25.
    Kozmik Z, Ruzickova J, Jonasova K, Matsumoto Y, Vopalensky P, Kozmikova I, Strnad H, Kawamura S, Piatigorsky J, Paces V, Vlcek C (2008) Assembly of the cnidarian camera-type eye from vertebrate-like components. Proc Natl Acad Sci USA 105:8989–8993PubMedCrossRefGoogle Scholar
  26. 26.
    Suga H, Schmid V, Gehring WJ (2008) Evolution and functional diversity of jellyfish opsins. Curr Biol 18:51–55PubMedCrossRefGoogle Scholar
  27. 27.
    González-Menéndez I, Contreras F, Cernuda-Cernuda R, García-Fernández JM (2009) Daily rhythm of melanopsin-expressing cells in the mouse retina. Front Cell Neurosci 3:1–7CrossRefGoogle Scholar
  28. 28.
    Lim J, Choi K (2003) Bar homeodomain proteins are anti-proneural in the Drosophila eye: transcriptional repression of atonal by bar prevents ectopic retinal neurogenesis. Development 130:5965–5974PubMedCrossRefGoogle Scholar
  29. 29.
    Poggi L, Vottari T, Barsacchi G, Wittbrodt J, Vignali R (2004) The homeobox gene Xbh1 cooperates with proneural genes to specify ganglion cell fate within the Xenopus neural retina. Development 131:2305–2315PubMedCrossRefGoogle Scholar
  30. 30.
    Brown NL, Patel S, Brzezinski J, Glaser T (2001) Math5 is required for retinal ganglion cell and optic nerve formation. Development 128:2497–2508PubMedGoogle Scholar
  31. 31.
    Bateson W (1894) Materials for the study of variation treated with special regard to discontinuity in the origin of species. Macmillan, London/New YorkGoogle Scholar
  32. 32.
    Lemons D, McGinnis W (2006) Genomic evolution of Hox gene clusters. Science 313:1918–1922PubMedCrossRefGoogle Scholar
  33. 33.
    Duboule D (2007) The rise and fall of Hox gene clusters. Development 134:2549–2560PubMedCrossRefGoogle Scholar
  34. 34.
    De Robertis EM (2008) Evo-Devo: variations on ancestral themes. Cell 132:185–195PubMedCrossRefGoogle Scholar
  35. 35.
    Yekta S, Tabin CJ, Bartel DP (2008) MicroRNAs in the Hox network: an apparent link to posterior prevalence. Nat Rev Genet 9:789–796PubMedCrossRefGoogle Scholar
  36. 36.
    Cohn MJ, Tickle C (1999) Developmental basis of limblessness and axial patterning in snakes. Nature 399:474–479PubMedCrossRefGoogle Scholar
  37. 37.
    Di-Poï N, Montoya-Burgos JI, Miller H, Pourquié O, Milinkovitch MC, Duboule D (2010) Changes in Hox genes’ structure and function during the evolution of the squamate body plan. Nature 464:99–103PubMedCrossRefGoogle Scholar
  38. 38.
    McGlinn E, Yekta S, Mansfield JH, Soutschekd J, Bartel DP, Tabin CJ (2009) In ovo application of antagomiRs indicates a role for miR-196 in patterning the chick axial skeleton through Hox gene regulation. Proc Natl Acad Sci 106:18610–18615PubMedCrossRefGoogle Scholar
  39. 39.
    Graham A, McGonnell I (1999) Developmental evolution: this side of paradise. Curr Biol 9:R630–R632PubMedCrossRefGoogle Scholar
  40. 40.
    Woltering JM, Vonk FJ, Müller H, Bardine N, Tuduce IL, de Bakker MA, Knöchel W, Sirbu IO, Durston AJ, Richardson MK (2009) Axial patterning in snakes and caecilians: evidence for an alternative interpretation of the Hox code. Dev Biol 332:82–89PubMedCrossRefGoogle Scholar
  41. 41.
    Merino R, Rodriguez-Leon J, Macias D, Gañan Y, Economides AN, Hurle JM (1999) The BMP antagonist Gremlin regulates outgrowth, chondrogenesis and programmed cell death in the developing limb. Development 126:5515–5522PubMedGoogle Scholar
  42. 42.
    Laufer E et al (1997) BMP expression in duck interdigital webbing: a reanalysis. Science 278:305PubMedCrossRefGoogle Scholar
  43. 43.
    Cooper KL, Tabin CJ (2008) Understanding of bat wing evolution takes flight. Genes Dev 22:121–124PubMedCrossRefGoogle Scholar
  44. 44.
    Weatherbee SD, Behringer RR, Rasweiler JJ, Niswander LA (2006) Interdigital webbing retention in bat wings illustrates genetic changes underlying amniote limb diversification. Proc Natl Acad Sci USA 103:15103–15107PubMedCrossRefGoogle Scholar
  45. 45.
    Cretekos CJ, Wang Y, Green ED, Martin JF, Rasweiler JJ, Behringer RR (2008) Regulatory divergence modifies limb length between mammals. Genes Dev 22:141–151PubMedCrossRefGoogle Scholar
  46. 46.
    Weatherbee SD (2008) Mammalian limbs take flight. Dev Cell 14:149–150PubMedCrossRefGoogle Scholar
  47. 47.
    Wang Z, Yuan L, Rossiter SJ, Zuo X, Ru B, Zhong H, Han N, Jones G, Jepson PD, Zhang S (2009) Adaptive evolution of 5′HoxD genes in the origin and diversification of the cetacean flipper. Mol Biol Evol 26:613–622PubMedCrossRefGoogle Scholar
  48. 48.
    Fedak TJ, Hall BK (2004) Perspectives on hyperphalangy: patterns and processes. J Anat 204:151–163PubMedCrossRefGoogle Scholar
  49. 49.
    Richardson MK, Oelschläger HHA (2002) Time, pattern, and heterochrony: a study of hyperphalangy in the dolphin embryo flipper. Evol Dev 4:435–444PubMedCrossRefGoogle Scholar
  50. 50.
    Ronshaugen M, McGinnis N, McGinnis W (2002) Hox protein mutation and macroevolution of the insect body plan. Nature 415:914–917PubMedCrossRefGoogle Scholar
  51. 51.
    Galant R, Carroll SB (2002) Evolution of a transcriptional repression domain in an insect Hox protein. Nature 415:910–913PubMedCrossRefGoogle Scholar
  52. 52.
    Sears KE, Behringer RR, Rasweiler JJ, Niswander LA (2006) Development of bat flight: morphologic and molecular evolution of bat wing digits. Proc Natl Acad Sci USA 103:6581–6586PubMedCrossRefGoogle Scholar
  53. 53.
    Darwin C (1839) The voyage of the beagle. Natural history library, 1962nd edn. Anchor Press, NorwellGoogle Scholar
  54. 54.
    Grant PR, Grant BR (2008) How and why species multiply. The radiation of Darwin’s finches. Princeton University Press, PrincetonGoogle Scholar
  55. 55.
    Abzhanov A, Protas M, Grant BR, Grant PR, Tabin CJ (2004) Bmp4 and morphological variation of beaks in Darwin’s finches. Science 305:1462–1465PubMedCrossRefGoogle Scholar
  56. 56.
    Wu P, Jiang T-X, Suksaweang S, Widelitz RB, Chuong C-M (2004) Molecular shaping of the beak. Science 305:1465–1466PubMedCrossRefGoogle Scholar
  57. 57.
    Abzhanov A, Kuo WP, Hartmann C, Grant B, Grant PR, Tabin CJ (2006) The calmodulin pathway and evolution of elongated beak morphology in Darwin’s finches. Nature 443:563–567CrossRefGoogle Scholar
  58. 58.
    Muller GB (2007) Evo–devo: extending the evolutionary synthesis. Nature 8:943–949Google Scholar
  59. 59.
    Gilbert SF, Epel D (2009) Ecological developmental biology. Integrating epigenetics, medicine and evolution. Sinauer Associates, SunderlandGoogle Scholar
  60. 60.
    Minelli A, Fusco G (eds) (2008) Evolving Pathways. Key themes in evolutionary developmental biology. Cambridge University Press, Cambridge, UKGoogle Scholar

Copyright information

© Springer-Verlag Italia S.r.l.  2012

Authors and Affiliations

  1. 1.Lab. of Cell and Developmental Biology, Department of BiologyUniversity of PisaPisaItaly

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