Biological Theory

, Volume 8, Issue 3, pp 286–292 | Cite as

The Causality Horizon and the Developmental Bases of Morphological Evolution

  • Isaac Salazar-Ciudad
  • Jukka JernvallEmail author
Thematic Issue Article: Emergence of Shape


With the advent of evolutionary developmental research, or EvoDevo, there is hope of discovering the roles that the genetic bases of development play in morphological evolution. Studies in EvoDevo span several levels of organismal organization. Low-level studies identify the ultimate genetic changes responsible for morphological variation and diversity. High-level studies of development focus on how genetic differences affect the dynamics of gene networks and epigenetic interactions to modify morphology. Whereas an increasing number of studies link independent acquisition of homoplastic or convergent morphologies to similar changes in the genomes, homoplasies are not always found to have identical low-level genetic underpinnings. This suggests that a combination of low- and high-level approaches may be useful in understanding the relationship between genetic and morphological variation. Therefore, as an empirical and conceptual framework, we propose the causality horizon to signify the lowest level that allows linking homoplastic morphologies to similar changes in the development. A change in a system below the causality horizon cannot be generalized. In more concrete terms, homoplastic morphologies cannot be reduced to the same change in gene regulation when that change occurs below the causality horizon; rather, a higher-level mechanism should be identified.


Causality horizon EvoDevo Genotype–Phenotype map Patterning 



We thank Jeffrey Schwartz for providing a forum to develop ideas presented in the article, and David Polly and Kate MacCord for critically reviewing the manuscript.


  1. Abouheif E, Wray GA (2002) Evolution of the gene network underlying wing polyphenism in ants. Science 297:249–252CrossRefGoogle Scholar
  2. Abzhanov A, Protas M, Grant BR, Grant PR, Tabin CJ (2004) Bmp4 and morphological variation of beaks in Darwin’s finches. Science 305:1462–1465CrossRefGoogle Scholar
  3. Abzhanov A, Kuo WP, Hartmann C, Grant BR, Grant PR, Tabin CJ (2006) The calmodulin pathway and evolution of elongated beak morphology in Darwin’s finches. Nature 442:563–567CrossRefGoogle Scholar
  4. Akam M (1998) Hox genes: from master genes to micromanagers. Curr Biol 8:R676–R678CrossRefGoogle Scholar
  5. Alberch P (1982) Developmental constraints in evolutionary processes. In: Bonner JT (ed) Evolution and development. Dahlem Konferenzen. Springer, Heidelberg, pp 313–332CrossRefGoogle Scholar
  6. Atchley WR (1987) Developmental quantitative genetics and the evolution of ontogenies. Evolution 41:316–330CrossRefGoogle Scholar
  7. Barton N, Partridge L (2000) Limits to natural selection. BioEssays 22:1075–1084CrossRefGoogle Scholar
  8. Beloussov LV (1998) The dynamic architecture of a developing organism: an interdisciplinary approach to the development of organisms. Kluwer, DordrechtCrossRefGoogle Scholar
  9. Carroll SB, Grenier JK, Weatherbee SD (2001) From DNA to diversity: molecular genetics and the evolution of animal design. Blackwell, MaldenGoogle Scholar
  10. Charlesworth B, Lande R (1982) Morphological stasis and developmental constraint–no problem for Neo-Darwinism. Nature 296:610CrossRefGoogle Scholar
  11. Collier JR, Monk NA, Maini PK, Lewis JH (1996) Pattern formation by lateral inhibition with feedback: a mathematical model of delta-notch intercellular signalling. J Theor Biol 183:429–446CrossRefGoogle Scholar
  12. Coyne JA (2006) Comment on “Gene regulatory networks and the evolution of animal body plans.” Science 313:761CrossRefGoogle Scholar
  13. DeFaveri J, Shikano T, Shimada Y, Goto A, Merilä J (2011) Global analysis of genes involved in freshwater adaptation in threespine sticklebacks (Gasterosteus aculeatus). Evolution 65:1800–1807CrossRefGoogle Scholar
  14. Dworkin I, Gibson G (2006) Epidermal growth factor receptor and transforming growth factor-beta signaling contributes to variation for wing shape in Drosophila melanogaster. Genetics 173:1417–1431CrossRefGoogle Scholar
  15. Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, OxfordGoogle Scholar
  16. Frankel N, Erezyilmaz DF, McGregor AP, Wang S, Payre F, Stern DL (2011) Morphological evolution caused by many subtle-effect substitutions in regulatory DNA. Nature 474:598–603CrossRefGoogle Scholar
  17. Gehring WJ (1993) Exploring the homeobox. Gene 135:215–221CrossRefGoogle Scholar
  18. Gibson G, Hogness DS (1996) Effect of polymorphism in the Drosophila regulatory gene Ultrabithorax on homeotic stability. Science 271:200–203CrossRefGoogle Scholar
  19. Gilbert SF, Sarkar S (2000) Embracing complexity: organicism for the 21st century. Dev Dyn 219:1–9CrossRefGoogle Scholar
  20. Gong Z, Matzke NJ, Ermentrout B, Song D, Vendetti JE, Slatkin M, Oster G (2012) Evolution of patterns on Conus shells. Proc Natl Acad Sci USA 109:E234–E241CrossRefGoogle Scholar
  21. Goodwin BC (1994) How the leopard changed its spots. Weidenfeld and Nicolson, LondonGoogle Scholar
  22. Haldane JBS (1932) The causes of evolution. Longmans, London. Reprint: Princeton University Press, Princeton (1990)Google Scholar
  23. Hallgrímsson B, Brown JJY, Hall BK (2005) The study of phenotypic variability: an emerging research agenda for understanding the developmental-genetic architecture underlying phenotypic variation. In: Hallgrímsson B, Hall BK (eds) Variation: a central concept in biology. Academic Press, New York, pp 525–551Google Scholar
  24. Harjunmaa E, Kallonen A, Voutilainen M, Hämäläinen K, Mikkola ML, Jernvall J (2012) On the difficulty of increasing dental complexity. Nature 483:324–327CrossRefGoogle Scholar
  25. Harris MP, Williamson S, Fallon JF, Meinhardt H, Prum RO (2005) Molecular evidence for an activator-inhibitor mechanism in development of embryonic feather branching. Proc Natl Acad Sci USA 102:11734–11739CrossRefGoogle Scholar
  26. Janssens H, Hou S, Jaeger J, Kim AR, Myasnikova E, Sharp D, Reinitz J (2006) Quantitative and predictive model of transcriptional control of the Drosophila melanogaster even skipped gene. Nat Genet 38:1159–1165CrossRefGoogle Scholar
  27. Jeffery WR (2009) Regressive evolution in Astyanax cavefish. Annu Rev Genet 43:25–47CrossRefGoogle Scholar
  28. Knecht AK, Hosemann KE, Kingsley DM (2007) Constraints on utilization of the EDA-signaling pathway in threespine stickleback evolution. Evol Dev 9:141–154CrossRefGoogle Scholar
  29. Leinonen T, McCairns RJS, Herczeg G, Merilä J (2012) Multiple evolutionary pathways to decreased lateral plate coverage in freshwater threespine sticklebacks. Evolution 66:3866–3875CrossRefGoogle Scholar
  30. Marcellini S, Simpson P (2006) Two or four bristles: functional evolution of an enhancer of scute in Drosophilidae. PLoS Biol 4:2252–2261CrossRefGoogle Scholar
  31. Marcucio RS, Young NM, Hu D, Hallgrimsson B (2011) Mechanisms that underlie co-variation of the brain and face. Genesis 49:177–189CrossRefGoogle Scholar
  32. Meinhardt H (1982) Models of biological pattern formation. Academic Press, LondonGoogle Scholar
  33. Mezey JG, Houle D, Nuzhdin SV (2005) Naturally segregating quantitative trait loci affecting wing shape of Drosophila melanogaster. Genetics 169:2101–2113CrossRefGoogle Scholar
  34. Moreira J, Deutsch A (2005) Pigment pattern formation in zebrafish during late larval stages: a model based on local interactions. Dev Dyn 232:33–42CrossRefGoogle Scholar
  35. Nakamasu A, Takahashi G, Kanbe A, Kondo S (2009) Interactions between zebrafish pigment cells responsible for the generation of Turing patterns. Proc Natl Acad Sci USA 106:8429–8434CrossRefGoogle Scholar
  36. Nebot A, Medina S, Cellier FE (1994) The causality horizon: limitations to predictability of behavior using fuzzy inductive reasoning. Proc Conf Model Simul 3:492–496Google Scholar
  37. Newman SA, Comper WD (1990) “Generic” physical mechanisms of morphogenesis and pattern formation. Development 110:1–18Google Scholar
  38. Newman SA, Müller GB (2005) Origination and innovation in the vertebrate limb skeleton: an epigenetic perspective. J Exp Zool B Mol Dev Evol 304:593–609CrossRefGoogle Scholar
  39. Nijhout HF (1990) Metaphors and the role of genes in development. BioEssays 12:441–446CrossRefGoogle Scholar
  40. Palsson A, Gibson G (2000) Quantitative developmental genetic analysis reveals that the ancestral dipteran wing vein prepattern is conserved in Drosophila melanogaster. Dev Genes Evol 210:617–622CrossRefGoogle Scholar
  41. Pennisi E (2002) Evolutionary biology: evo-devo enthusiasts get down to details. Science 298:953–955CrossRefGoogle Scholar
  42. Plikus MV, Zeichner-David M, Mayer JA, Reyna J, Bringas P, Thewissen JG, Snead ML, Chai Y, Chuong CM (2005) Morphoregulation of teeth: modulating the number, size, shape and differentiation by tuning Bmp activity. Evol Dev 7:440–457CrossRefGoogle Scholar
  43. Prum RO (2005) Evolution of the morphological innovations of feathers. J Exp Zool B Mol Dev Evol 304:570–579CrossRefGoogle Scholar
  44. Rebeiz M, Pool JE, Kassner VA, Aquadro CF, Carroll SB (2009) Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science 326:1663–1667CrossRefGoogle Scholar
  45. Salazar-Ciudad I (2006) Developmental constraints versus variational properties: how pattern formation can help to understand evolution and development. J Exp Zool B Mol Dev Evol 306:107–125CrossRefGoogle Scholar
  46. Salazar-Ciudad I (2008) Tooth morphogenesis in vivo, in vitro, and in silico. Curr Top Dev Biol 81:341–371CrossRefGoogle Scholar
  47. Salazar-Ciudad I (2009) Looking at the origin of phenotypic variation from pattern formation gene networks. J Biosci 34:573–587CrossRefGoogle Scholar
  48. Salazar-Ciudad I, Jernvall J (2002) A gene network model accounting for development and evolution of mammalian teeth. Proc Natl Acad Sci USA 99:8116–8120CrossRefGoogle Scholar
  49. Salazar-Ciudad I, Jernvall J (2010) A computational model of teeth and the developmental origins of morphological variation. Nature 464:583–586CrossRefGoogle Scholar
  50. Salazar-Ciudad I, Jernvall J, Newman SA (2003) Mechanisms of pattern formation in development and evolution. Development 130:2027–2037CrossRefGoogle Scholar
  51. Sheth R, Marcon L, Bastida MF, Junco M, Quintana L, Dahn R, Kmita M, Sharpe J, Ros MA (2012) Hox genes regulate digit patterning by controlling the wavelength of a turing-type mechanism. Science 338:1476–8140CrossRefGoogle Scholar
  52. Shvartsman SY, Muratov CB, Lauffenburger DA (2002) Modeling and computational analysis of EGF receptor-mediated cell communication in Drosophila oogenesis. Development 129:2577–2589Google Scholar
  53. True JR, Haag ES (2001) Developmental system drift and flexibility in evolutionary trajectories. Evol Dev 3:109–119CrossRefGoogle Scholar
  54. von Dassow M, Davidson LA (2007) Variation and robustness of the mechanics of gastrulation: the role of tissue mechanical properties during morphogenesis. Birth Defects Res C Embryo Today 81:253–269CrossRefGoogle Scholar
  55. Weiss K, Fullerton SM (2000) Phenogenetic drift and the evolution of genotype–phenotype relationships. Theor Popul Biol 57:187–195CrossRefGoogle Scholar
  56. Wu P, Jiang TX, Shen JY, Widelitz RB, Chuong CM (2006) Morphoregulation of avian beaks: comparative mapping of growth zone activities and morphological evolution. Dev Dyn 235:1400–1412CrossRefGoogle Scholar

Copyright information

© Konrad Lorenz Institute for Evolution and Cognition Research 2013

Authors and Affiliations

  1. 1.Developmental Biology Program, Institute of BiotechnologyUniversity of HelsinkiHelsinkiFinland
  2. 2.Department of Genetics and MicrobiologyUniversitat Autònoma de BarcelonaCerdanyola del VallèsSpain

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