Development Genes and Evolution

, Volume 216, Issue 7–8, pp 385–394

Unburdening evo-devo: ancestral attractions, model organisms, and basal baloney

Review

Abstract

Although flourishing, I argue that evo-devo is not yet a mature scientific discipline. Its philosophical foundation exhibits an internal inconsistency that results from a metaphysical confusion. In modern evolutionary biology, species and other taxa are most commonly considered as individuals. I accept this thesis to be the best available foundation for modern evolutionary biology. However, evo-devo is characterized by a remarkable degree of typological thinking, which instead treats taxa as classes. This metaphysical incompatibility causes much distorted thinking. In this paper, I will discuss the logical implications of accepting the individuality thesis for evo-devo. First, I will illustrate the degree to which typological thinking pervades evo-devo. This ranges from the relatively innocent use of typologically tainted language to the more serious misuse of differences between taxa as evidence against homology and monophyly, and the logically flawed concept of partial homology. Second, I will illustrate how, in a context of typological thinking, evo-devo's harmless preoccupation with distant ancestors has become transformed into a pernicious problem afflicting the choice of model organisms. I will expose the logical flaws underlying the common assumption that model organisms can be expected to represent the clades they are a part of in an unambiguous way. I will expose the logical flaws underlying the general assumption that basal taxa are the best available stand-ins for ancestors and that they best represent the clade of which they are a part, while also allowing for optimal extrapolation of results.

Keywords

Metaphysics Model organisms Basal taxa Evo-devo Individuality thesis 

References

  1. Amundson R (1998) Typology reconsidered: two doctrines on the history of evolutionary biology. Biol Philos 13:153–177CrossRefGoogle Scholar
  2. Amundson R (2003) Phylogenic reconstruction then and now. Biol Philos 17:679–694CrossRefGoogle Scholar
  3. Amundson R (2005) The changing role of the embryo in evolutionary thought. Roots of evo-devo. Cambridge University Press, Cambridge, UKGoogle Scholar
  4. Anderson DT (1973) Embryology and phylogeny of annnelids and arthropods. Pergamon, OxfordGoogle Scholar
  5. Arthur W (2002) The emerging conceptual framework of evolutionary developmental biology. Nature 415:757–764PubMedGoogle Scholar
  6. Bolker JA (1995) Model systems in developmental biology. BioEssays 17:451–455PubMedCrossRefGoogle Scholar
  7. Bromham L, Woolfit M, Lee MSY, Rambaut A (2002) Testing the relationship between morphological and molecular rates of change along phylogenies. Evolution 56:1921–1930PubMedGoogle Scholar
  8. Carroll RL (1997) Patterns and processes of vertebrate evolution. Cambridge University Press, Cambridge, UKGoogle Scholar
  9. Crane JK (2004) On the metaphysics of species. Philosophy of Science Assocation 71:156–173CrossRefGoogle Scholar
  10. Crisp MD, Cook LG (2005) Do early branching lineages signify ancestral traits? TREE 20:122–128PubMedCrossRefGoogle Scholar
  11. Damen WGM, Weller M, Tautz D (2000) Expression patterns of hairy, even-skipped, and runt in the spider Cupiennius salei imply that these genes were segmentation genes in a basal arthropod. Proc Natl Acad Sci U S A 97:4515–4519PubMedCrossRefGoogle Scholar
  12. Darwin C (1859) The origin of species, edition from 1985. Penguin Book, LondonGoogle Scholar
  13. Davidson EH (1991) Spatial mechanisms of gene regulation in metazoan embryos. Development 113:1–26PubMedGoogle Scholar
  14. Davidson EH (2001) Genomic regulatory systems. Academic, San DiegoGoogle Scholar
  15. Davidson EH, Peterson KJ, Cameron RA (1995) Origin of bilaterian body plans: evolution of developmental regulatory mechanisms. Science 270:1319–1325PubMedGoogle Scholar
  16. Fitch WM, Beintema JJ (1990) Correcting parsimonious trees for unseen nucleotide substitutions: the effect of dense branching as exemplified by ribonuclease. Mol Biol Evol 7:438–443PubMedGoogle Scholar
  17. Fryer G (1996) Reflections on arthropod evolution. Biol J Linn Soc 58:1–55CrossRefGoogle Scholar
  18. Ghiselin MT (1974) A radical solution to the species problem. Syst Zool 23:536–544CrossRefGoogle Scholar
  19. Ghiselin MT (1997) Metaphysics and the origin of species. State University of New York Press, New YorkGoogle Scholar
  20. Ghiselin MT (2005a) The Darwinian revolution as viewed by a philosophical biologist. J Hist Biol 38:123–136CrossRefGoogle Scholar
  21. Ghiselin MT (2005b) Homology as a relation of correspondence between parts of individuals. Theory in Biosciences 24:91–103CrossRefGoogle Scholar
  22. Gould SJ (2002) The structure of evolutionary theory. The Belknap Press of Harvard University Press, Cambridge, MAGoogle Scholar
  23. Grant T, Kluge AG (2004) Transformation series as an ideographic character concept. Cladistics 20:23–31CrossRefGoogle Scholar
  24. Hall BK (1999) Evolutionary developmental biology. Kluwer, DordrechtGoogle Scholar
  25. Hall BK (2003) Evo-devo: evolutionary developmental mechanisms. Int J Dev Biol 47:491–495PubMedGoogle Scholar
  26. Hrycaj S, Popadic A (2005) Resolving arthropod relationships: present and future insights from evo-devo studies. In Koenemann S, Jenner RA (eds) Crustacea and arthropod relationships. CRC Press, Boca Raton, FL, pp 167–182Google Scholar
  27. Hughes CL, Kaufman TC (2000) A diverse approach to arthropod development. Evol Dev 2:6–8PubMedCrossRefGoogle Scholar
  28. Jenner RA (2005) The tainting of Proc. Biol. Soc. Wash. Palaeontol Assoc Newsl 57:10–17Google Scholar
  29. Keller RA, Boyd RN, Wheeler QD (2003) The illogical basis of phylogenetic nomenclature. Bot Rev 69:93–110Google Scholar
  30. Krell FT, Cranston PS (2004) Which side of the tree is more basal? Syst Entomol 29:279–281CrossRefGoogle Scholar
  31. Ladurner P, Schärer L, Salvenmoser W, Rieger RM (2005) A new model organism among the lower Bilateria and the use of digital microscopy in taxonomy of meiobenthic Platyhelminthes: Macrostomum lignano, n. sp. (Rhabditophora, Macrostomorpha). JZS 43:114–126CrossRefGoogle Scholar
  32. Leroi AM (1998) The burden of the bauplan. TREE 13:82–83Google Scholar
  33. Levinton JS (2001) Genetics, paleontology, and macroevolution. Cambridge University Press, Cambridge, UKGoogle Scholar
  34. Manton SM, Harding JP (1964) Mandibular mechanisms and the evolution of arthropods. Philos Trans R Soc Lond B 247:1–183Google Scholar
  35. Mayr E, Bock WJ (2002) Classifications and other ordering systems. J Zoolog Syst Evol Res 40:169–194CrossRefGoogle Scholar
  36. Minelli A (1998) Molecules, developmental modules, and phenotypes: a combinatorial approach to homology. Mol Phylogenet Evol 9:340–347PubMedCrossRefGoogle Scholar
  37. Minelli A (2003) The development of animal form. Cambridge University Press, Cambridge, UKGoogle Scholar
  38. Muller WEG, Muller IM (2003) The hypothetical ancestral animal the Urmetazoa: telomerase activity in sponges (Porifera). J Serb Chem Soc 68:257–268CrossRefGoogle Scholar
  39. Nezlin LP (2000) Tornaria of hemichordates and other dipleurula-type larvae: a comparison. J Zoolog Syst Evol Res 38:149–156CrossRefGoogle Scholar
  40. O’Hara RJ (1992) Telling the tree: narrative representation and the study of evolutionary history. Biol Philos 7:135–160CrossRefGoogle Scholar
  41. Peterson MD, Popadic A, Kaufman TC (1998) The expression of two engrailed-related genes in an apterygote insect and a phylogenetic analysis of insect engrailed-related genes. Dev Genes Evol 208:547–557PubMedCrossRefGoogle Scholar
  42. Pilato G, Binda Mg, Biondi O, D’urso V, Lisi O, Marletta A, Maugeri S, Nobile V, Rappazzo G, Sabella G, Sammartano F, Turrisi G, Viglianisi F (2005) The clade Ecdysozoa, perplexities and questions. Zool Anz 244:43–50Google Scholar
  43. Raff RA (1996) The shape of life. University of Chicago Press, Chigaco, ILGoogle Scholar
  44. Reydon TAC (2003) Discussion: species are individuals—or are they? Philos Sci 70:49–56CrossRefGoogle Scholar
  45. Reydon TAC (2004) Why does the species problem still persist? BioEssays 26:300–305PubMedCrossRefGoogle Scholar
  46. Richards RJ (2002) The Romantic conception of life. Science and philosophy in the age of Goethe. University of Chicago Press, Chicago, ILGoogle Scholar
  47. Richardson MK, Minelli A, Coates MI (1999) Some problems with typological thinking in evolution and development. Evol Dev 1:5–7PubMedCrossRefGoogle Scholar
  48. Richardson MK, Jeffery JE, Coates MI, Bininda-Emonds ORP (2001) Comparative methods in developmental biology. Zoology 104: 278–283PubMedCrossRefGoogle Scholar
  49. Rieppel O (2005a) Proper names in twin worlds: monophyly, paraphyly, and the world around us. Org Divers Evol 5:89–100CrossRefGoogle Scholar
  50. Rieppel O (2005b) Modules, kinds, and homology. J Exp Zool (Mol Dev Evol) 304B:18–27CrossRefGoogle Scholar
  51. Ruse M (1996) Monad to man. The concept of progress in evolutionary biology. Harvard University Press, Cambridge, MAGoogle Scholar
  52. Sanetra M, Begemann G, Becker MB, Meyer A (2005) Conservation and co-option in developmental programmes: the importance of homology relations. Frontiers in Zoology 2:15PubMedCrossRefGoogle Scholar
  53. Scholtz G (2005) Homology and ontogeny: pattern and process in comparative developmental biology. Theory Biosci 124:121–143CrossRefGoogle Scholar
  54. Schoppmeier W, Damen WGM (2001) Double-stranded RNA interference in the spider Cupiennius salei: the role of Distall-less is evolutionarily conserved in arthropod appendage formation. Dev Genes Evol 211:76–82PubMedCrossRefGoogle Scholar
  55. Schram FR (1978) Arthropods: a convergent phenomenon. Fieldiana Geol 39:61–108Google Scholar
  56. Schram FR, Koenemann S (2001) Developmental genetics and arthropod evolution: part I, on legs. Evol Dev 3:343–354PubMedCrossRefGoogle Scholar
  57. Sereno PC (2005) The logical basis of phylogenetic taxonomy. Syst Biol 54:595–619PubMedCrossRefGoogle Scholar
  58. Slack JMW, Holland PHW, Graham CF (1993) The zootype and the phylotypic stage. Nature 361:490–492PubMedCrossRefGoogle Scholar
  59. Stamos DN (2002) Species, languages, and the horizontal/vertical distinction. Biol Philos 17:171–198CrossRefGoogle Scholar
  60. Stanley SM (1998) Macroevolution. The Johns Hopkins University Press, Baltimore, MDGoogle Scholar
  61. Struck TH, Halanych KM, Purschke G (2005) Dinophilidae (Annelida) is most likely not a progenetic Eunicida: evidence from 18S and 28S rDNA. Mol Phylogenet Evol 37:619–623PubMedCrossRefGoogle Scholar
  62. Svensson M (2004) Homology and homocrasy revisited: gene expression patterns and hypotheses of homology. Dev Genes Evol 214:418–421PubMedCrossRefGoogle Scholar
  63. Tessmar-Raible K, Arendt D (2003) Emerging systems: between vertebrates and arthropods, the Lophotrochozoa. Curr Opin Genet Dev 13:331–340PubMedCrossRefGoogle Scholar
  64. Tudge C (2000) The variety of life. Oxford University Press, London, UKGoogle Scholar
  65. Wägele J-W (2005) Foundations of phylogenetic systematics. Verlag Dr. Friedrich Pfeil, MünchenGoogle Scholar
  66. Wagner GP (2001) Characters, units and natural kinds: an introduction. In: Wagner GP (ed) The character concept in evolutionary biology. Academic, San Diego, pp 1–10Google Scholar
  67. Webster AJ, Payne RJH, Pagel M (2003) Molecular phylogenies link rates of evolution and speciation. Science 301:478PubMedCrossRefGoogle Scholar
  68. Wilkins AS (2002) The evolution of developmental pathways. Sinauer, SunderlandGoogle Scholar
  69. Willmer P (1990) Invertebrate relationships. Cambridge University Press, Cambridge, UKGoogle Scholar
  70. Winsor MP (2003) Non-essentialist methods in pre-Darwian taxonomy. Biol Philos 18:387–400CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Department of Biology and BiochemistryUniversity of BathBathUK

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