Biological Theory

, Volume 9, Issue 2, pp 178–193 | Cite as

Connecting the Dots: Anatomical Network Analysis in Morphological EvoDevo

  • Diego Rasskin-Gutman
  • Borja Esteve-Altava
Long Article


Morphological EvoDevo is a field of biological inquiry in which explicit relations between evolutionary patterns and growth or morphogenetic processes are made. Historically, morphological EvoDevo results from the coming together of several traditions, notably Naturphilosophie, embryology, the study of heterochrony, and developmental constraints. A special feature binding different approaches to morphological EvoDevo is the use of formalisms and mathematical models. Here we will introduce anatomical network analysis, a new approach centered on connectivity patterns formed by anatomical parts, with its own concepts and tools specifically designed for the study of morphological EvoDevo questions. Riedl’s concept of burden is tightly related to the use of anatomical networks, providing a nexus between the evolutionary patterns and the structural constraints that shape them.


Morphology EvoDevo Anatomical network analysis (AnNA) 



The research project that led to AnNA was initially supported by grant BFU2008-00643 from the Spanish Ministerio de Ciencia e Innovación. We also thank the Cavanilles Institute for Biodiversity and Evolutionary Biology for further funding support and the KLI, where it all began. Jesús Marugán-Lobón and Héctor Botella contributed to the early development of AnNA; many ideas were also refined thanks to the thoughtful comments made by the members of BEA’s PhD thesis committee.


  1. Adams DC, Rohlf FJ, Slice DE (2013) A field comes of age: geometric morphometrics in the 21st century. Ital J Mammal 24:7–14Google Scholar
  2. Albert R, Barabási A-L (2002) Statistical mechanics of complex networks. Rev Mod Phys 74:47–97CrossRefGoogle Scholar
  3. Appel TA (1987) The Cuvier–Geoffroy debate: French biology in the decades before Darwin. Oxford University Press, New YorkGoogle Scholar
  4. Barabási A-L (2009) Scale-free networks: a decade and beyond. Science 325:412–413CrossRefGoogle Scholar
  5. Barabasi A-L, Oltvai ZN (2004) Network biology: understanding the cell’s functional organization. Nat Rev Genet 5:101–113CrossRefGoogle Scholar
  6. Callebaut W, Rasskin-Gutman D (eds) (2005) Modularity: understanding the development and evolution of natural complex systems. MIT Press, CambridgeGoogle Scholar
  7. Carroll SB, Grenier J, Weatherbee S (2005) From DNA to diversity: molecular genetics and the evolution of animal design, 2nd edn. Wiley, New YorkGoogle Scholar
  8. Dorogovtsev R, Mendes JFF (2003) Evolution of networks: from biological networks to the Internet and WWW. Oxford University Press, OxfordCrossRefGoogle Scholar
  9. Dullemeijer (1974) Concepts and approaches in animal morphology. Van Gorcum, AssenGoogle Scholar
  10. Dunne JA, Williams RJ, Martínez ND (2002) Food-web structure and network theory: the role of connectance and size. Proc Natl Acad Sci USA 99:12917–12922CrossRefGoogle Scholar
  11. Eble GJ (2005) Morphological modularity and macroevolution. In: Callebaut W, Rasskin-Gutman D (eds) Modularity: understanding the development and evolution of natural complex systems. MIT Press, Cambridge, pp 221–238Google Scholar
  12. Esteve-Altava B, Rasskin-Gutman D (2014a) Evo-Devo insights from pathological networks: exploring craniosynostosis as a developmental mechanism for modularity and complexity in the human skull. J Anthropol Sci (in press)Google Scholar
  13. Esteve-Altava B, Rasskin-Gutman D (2014b) Theoretical morphology of tetrapod skull networks. C R Palevol 13:41–50CrossRefGoogle Scholar
  14. Esteve-Altava B, Marugán-Lobón J, Botella H et al (2011) Network models in anatomical systems. J Anthropol Sci 89:175–184Google Scholar
  15. Esteve-Altava B, Marugán-Lobón J, Botella H et al (2013a) Grist for Riedl’s mill: a network model perspective on the integration and modularity of the human skull. J Exp Zool B (Mol Dev Evol) 320:489–500CrossRefGoogle Scholar
  16. Esteve-Altava B, Marugán-Lobón J, Botella H et al (2013b) Structural constraints in the evolution of the tetrapod skull complexity: Williston’s law revisited using network models. Evol Biol 40:209–219CrossRefGoogle Scholar
  17. Esteve-Altava B, Marugán-Lobón J, Botella H et al (2014) Random loss and selective fusion of bones originate morphological complexity trends in tetrapod skull networks. Evol Biol 41:52–61Google Scholar
  18. Fox-Keller E (2005) Revisiting ‘scale-free’ networks. BioEssays 27:1060–1068CrossRefGoogle Scholar
  19. Gaffney ES (1979) Comparative cranial morphology of recent and fossil turtles. Bull Am Mus Nat Hist 164:65–376Google Scholar
  20. Geoffroy Saint-Hilaire E (1818) Philosophie anatomique. J. B. Baillière, ParisGoogle Scholar
  21. González PN, Pérez SI, Bernal V (2010) Ontogeny of robusticity of craniofacial traits in modern humans: a study of South American populations. Am J Phys Anthropol 142:367–379CrossRefGoogle Scholar
  22. Gould SJ (2002) The structure of evolutionary theory. Harvard University Press, CambridgeGoogle Scholar
  23. Gregory WK (1935) ‘Williston’s law’ relating to the evolution of skull bones in the vertebrates. Am J Phys Anthropol 20:123–152CrossRefGoogle Scholar
  24. Guimerà R, Amaral LAN (2005) Functional cartography of complex metabolic networks. Nature 433:895–900CrossRefGoogle Scholar
  25. Guimerà R, Sales-Pardo M, Amaral LAN (2007) Classes of complex networks defined by role-to-role connectivity profiles. Nat Phys 3:63–69CrossRefGoogle Scholar
  26. Hallgrímsson B, Hall BK (eds) (2011) Epigenetics: linking genotype and phenotype in development and evolution. University of California Press, BerkeleyGoogle Scholar
  27. Hasty J, Mcmillen D, Isaacs F et al (2001) Computational studies of gene regulatory networks. Nat Rev Genet 2:268–279CrossRefGoogle Scholar
  28. Horvath S, Dong J (2008) Geometric interpretation of gene coexpression network analysis. PLoS Comput Biol 4:e1000117CrossRefGoogle Scholar
  29. Hukki J, Saarinem P, Kangasniemi M (2008) Single suture craniosynostosis: diagnosis and imaging. In: Rice DP (ed) Craniofacial sutures, development, disease and treatment. Karger, Basel, pp 79–90CrossRefGoogle Scholar
  30. Hull DL (1988) Science as a process: an evolutionary account of the social and conceptual development of science. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  31. Humphries MD, Gurney K (2008) Network ‘small-world-ness’: a quantitative method for determining canonical network equivalence. PLoS One 3:e0002051CrossRefGoogle Scholar
  32. Huxley J (1932) Problems of relative growth. Methuen, LondonGoogle Scholar
  33. Jacob F (1977) Evolution and tinkering. Science 196:1161–1166CrossRefGoogle Scholar
  34. Jaslow CR (1990) Mechanical properties of cranial sutures. J Biomech 23:313–321CrossRefGoogle Scholar
  35. Klingenberg CP (2010) Evolution and development of shape: integrating quantitative approaches. Nat Rev Genet 11:623–635Google Scholar
  36. Knight CG, Pinney JW (2009) Making the right connections: biological networks in the light of evolution. BioEssays 31:1080–1090CrossRefGoogle Scholar
  37. Le Guyader H (2003) Geoffroy Saint-Hilaire: a visionary naturalist. University of Chicago Press, ChicagoGoogle Scholar
  38. Magwene PM (2001) New tools for studying integration and modularity. Evolution 55:1734–1745CrossRefGoogle Scholar
  39. Magwene PM (2008) Using correlation proximity graphs to study phenotypic integration. Evol Biol 35:191–198CrossRefGoogle Scholar
  40. Mason O, Verwoerd M (2007) Graph theory and networks in biology. Syst Biol 1:89–119Google Scholar
  41. Mayr E (1982) The growth of biological thought: diversity, evolution, and inheritance. Harvard University Press, CambridgeGoogle Scholar
  42. McShea DW (1993) Evolutionary change in the morphological complexity of the mammalian vertebral column. Evolution 47:730–740CrossRefGoogle Scholar
  43. Mcshea DW, Brandon RN (2010) Biology’s first law: the tendency for diversity and complexity to increase in evolutionary systems. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  44. Mcshea DW, Hordijk W (2013) Complexity by subtraction. Evol Biol 40:504–520CrossRefGoogle Scholar
  45. Moazen M, Curtis N, O’higgins P et al (2009) Assessment of the role of sutures in a lizard skull: a computer modelling study. Proc R Soc B 276:39–46CrossRefGoogle Scholar
  46. Müller GB (2007) Six memos for evo-devo. In: Laubichler MD, Maienschein J (eds) From embryology to evo-devo: a history of developmental evolution. MIT Press, Cambridge, pp 499–524Google Scholar
  47. Müller GB, Newman SA (eds) (2003) Origination of organismal form: beyond the gene in developmental and evolutionary biology. MIT Press, CambridgeGoogle Scholar
  48. Newman ME (2005) Power laws, Pareto distributions and Zipf’s law. Contemp Phys 46:323–351CrossRefGoogle Scholar
  49. Newman SA, Forgacs G (2005) Complexity and self-organization in biological development and evolution. In: Bonchev DD, Rouvray D (eds) Complexity in chemistry, biology, and ecology. Springer, New York, pp 49–95CrossRefGoogle Scholar
  50. Newman ME, Girvan M (2004) Finding and evaluating community structure in networks. Phys Rev E 69:026113CrossRefGoogle Scholar
  51. Nicholson DJ, Gawne R (2013) Rethinking Woodger’s legacy in the philosophy of biology. J Hist Biol. doi: 10.1007/s10739-013-9364-x Google Scholar
  52. Nuño De La Rosa L (2012) El concepto de forma en la biología contemporanea. Examen filosófico. PhD Thesis, Universidad Complutense de Madrid and Université Paris 1 Panthéon-Sorbone, Madrid and ParisGoogle Scholar
  53. Ochoa C, Barahona A (2009) El debate entre Cuvier y Geoffroy, y el origen de la homología y la analogía. Ludus Vitalis 17:37–54Google Scholar
  54. Opperman LA (2000) Cranial sutures as intramembranous bone growth sites. Dev Dyn 219:472–485CrossRefGoogle Scholar
  55. Pearson K, Woo T (1935) Further investigation of the morphometric characters of the individual bones of the human skull. Biometrika 27:424–465CrossRefGoogle Scholar
  56. Porter MA, Onnela J-P, Mucha PJ (2009) Communities in networks. Not Am Math Soc 56:1082–1097Google Scholar
  57. Proulx SR, Promislow DE, Phillips PC (2005) Network thinking in ecology and evolution. Trends Ecol Evol 20:345–353CrossRefGoogle Scholar
  58. Raff RA (1996) The shape of life: genes, development, and the evolution of animal form. University of Chicago Press, ChicagoGoogle Scholar
  59. Rafferty KL, Herring SW, Marshall CD (2003) Biomechanics of the rostrum and the role of facial sutures. J Morphol 257:33–44CrossRefGoogle Scholar
  60. Rashevsky N (1954) Topology and life: in search of general mathematical principles in biology and sociology. Bull Math Biophys 16:317–348CrossRefGoogle Scholar
  61. Rashevsky N (1960) Contributions to relational biology. Bull Math Biophys 22:73–84CrossRefGoogle Scholar
  62. Rasskin-Gutman D (2003) Boundary constraints for the emergence of form. In: Müller G, Newman S (eds) Origination of organismal form. MIT Press, Cambridge, pp 305–322Google Scholar
  63. Rasskin-Gutman D (2009) Molecular evo-devo: the path not taken by Pere Alberch. In: Rasskin-Gutman D, De Renzi M (eds) Pere Alberch: the creative trajectory of an evo-devo biologist. Publicaciones de la Universidad de Valencia, Valencia, pp 67–84Google Scholar
  64. Rasskin-Gutman D, Buscalioni AD (2001) Theoretical morphology of the Archosaur (Reptilia: Diapsida) pelvic girdle. Paleobiology 27:59–78CrossRefGoogle Scholar
  65. Ravasz E, Barabási A-L (2003) Hierarchical organization in complex networks. Phys Rev E 67:026112CrossRefGoogle Scholar
  66. Ravasz E, Somera AL, Mongru DA et al (2002) Hierarchical organization of modularity in metabolic networks. Science 297:1551–1555CrossRefGoogle Scholar
  67. Rice D (2008) Developmental anatomy of craniofacial sutures. In: Rice DP (ed) Craniofacial sutures, development, disease and treatment. Karger, Basel, pp 1–21CrossRefGoogle Scholar
  68. Riedl R (1978) Order in living organisms: a systems analysis of evolution. Wiley, New YorkGoogle Scholar
  69. Rieppel O (2006) ‘Type’ in morphology and phylogeny. J Morphol 267:528–535CrossRefGoogle Scholar
  70. Rosen R (1991) Life itself: a comprehensive inquiry into the nature, origin, and fabrication of life. Columbia University Press, New YorkGoogle Scholar
  71. Rosen R (2000) Essays on life itself. Columbia University Press, New YorkGoogle Scholar
  72. Russell ES (1916) Form and function: a contribution to the history of animal morphology. John Murray, LondonCrossRefGoogle Scholar
  73. Sales-Pardo M, Guimera R, Moreira AA et al (2007) Extracting the hierarchical organization of complex systems. Proc Natl Acad Sci 104:15224–15229CrossRefGoogle Scholar
  74. Sardi ML, Ramirez Rozzi F, Pucciarelli HM (2004) The Neolithic transition in Europe and North Africa: the functional craneology contribution. Anthropol Anz 62:129–145Google Scholar
  75. Schoch RR (2010) Riedl’s burden and the body plan: selection, constraint, and deep time. J Exp Zool B (Mol Dev Evol) 314:1–10CrossRefGoogle Scholar
  76. Sidor CA (2001) Simplification as a trend in synapsid cranial evolution. Evolution 55:1419–1442CrossRefGoogle Scholar
  77. Simon HA (1962) The architecture of complexity. Proc Am Philos Soc 106:467–482Google Scholar
  78. Simpson GG (1961) Principles of animal taxonomy. Columbia University Press, New YorkGoogle Scholar
  79. Solé RV, Valverde S, Rodríguez-Caso C (2006) Modularity in biological networks. In: Képès F (ed) Biological networks. World Scientific, Singapore, pp 21–40Google Scholar
  80. Sorkin A, Von Zastrow M (2009) Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol 10:609–622CrossRefGoogle Scholar
  81. Sporns O (2002) Network analysis, complexity, and brain function. Complexity 8:56–60CrossRefGoogle Scholar
  82. Thompson DW (1942) On growth and form. Cambridge University Press, CambridgeGoogle Scholar
  83. Thomson KS (1995) Graphical analysis of dermal skull roof patterns. In: Thomason JJ (ed) Functional morphology in vertebrate paleontology. Cambridge University Press, Cambridge, pp 193–204Google Scholar
  84. Wagner GP, Laubichler MD (2004) Rupert Riedl and the re-synthesis of evolutionary and developmental biology: body plans and evolvability. J Exp Zool B (Mol Dev Evol) 302:92–102CrossRefGoogle Scholar
  85. Wagner GP, Pavlicev M, Cheverud JM (2007) The road to modularity. Nat Rev Genet 8:921–931CrossRefGoogle Scholar
  86. Watts DJ, Strogatz SH (1998) Collective dynamics of ‘small-world’ networks. Nature 393:440–442CrossRefGoogle Scholar
  87. Weishampel DB (1993) Beams and machines: modeling approaches to analysis of skull form and function. In: Hanken J, Hall BK (eds) The vertebrate skull. University of Chicago Press, Chicago, pp 303–344Google Scholar
  88. Weiss PA (1971) The basic concept of hierarchic system. In: Weiss PA (ed) Hierarchically organized systems in theory and practice. Hafner, New York, pp 1–44Google Scholar
  89. Woo T (1931) On the asymmetry of the human skull. Biometrika 22:324–352CrossRefGoogle Scholar
  90. Woodger J (1945) On biological transformations. In: Gross WEL, Medawar PB (eds) Essays on growth and form presented to D’Arcy Wentworth Thompson. Oxford University Press, Oxford, pp 95–120Google Scholar
  91. Wuchty S, Ravasz E, Barabási A-L (2006) The architecture of biological networks. In: Deisboeck TS, Kresh JT (eds) Complex systems science in biomedicine. Springer, New York, pp 165–181CrossRefGoogle Scholar

Copyright information

© Konrad Lorenz Institute for Evolution and Cognition Research 2014

Authors and Affiliations

  1. 1.Theoretical Biology Research Group, Cavanilles Institute of Biodiversity and Evolutionary BiologyUniversity of ValenciaValenciaSpain

Personalised recommendations