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Connecting the Dots: Anatomical Network Analysis in Morphological EvoDevo

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Abstract

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.

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References

  • Adams DC, Rohlf FJ, Slice DE (2013) A field comes of age: geometric morphometrics in the 21st century. Ital J Mammal 24:7–14

  • Albert R, Barabási A-L (2002) Statistical mechanics of complex networks. Rev Mod Phys 74:47–97

    Article  Google Scholar 

  • Appel TA (1987) The Cuvier–Geoffroy debate: French biology in the decades before Darwin. Oxford University Press, New York

    Google Scholar 

  • Barabási A-L (2009) Scale-free networks: a decade and beyond. Science 325:412–413

    Article  Google Scholar 

  • Barabasi A-L, Oltvai ZN (2004) Network biology: understanding the cell’s functional organization. Nat Rev Genet 5:101–113

    Article  Google Scholar 

  • Callebaut W, Rasskin-Gutman D (eds) (2005) Modularity: understanding the development and evolution of natural complex systems. MIT Press, Cambridge

    Google Scholar 

  • Carroll SB, Grenier J, Weatherbee S (2005) From DNA to diversity: molecular genetics and the evolution of animal design, 2nd edn. Wiley, New York

    Google Scholar 

  • Dorogovtsev R, Mendes JFF (2003) Evolution of networks: from biological networks to the Internet and WWW. Oxford University Press, Oxford

    Book  Google Scholar 

  • Dullemeijer (1974) Concepts and approaches in animal morphology. Van Gorcum, Assen

    Google Scholar 

  • Dunne JA, Williams RJ, Martínez ND (2002) Food-web structure and network theory: the role of connectance and size. Proc Natl Acad Sci USA 99:12917–12922

    Article  Google Scholar 

  • 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 221–238

    Google Scholar 

  • 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)

  • Esteve-Altava B, Rasskin-Gutman D (2014b) Theoretical morphology of tetrapod skull networks. C R Palevol 13:41–50

    Article  Google Scholar 

  • Esteve-Altava B, Marugán-Lobón J, Botella H et al (2011) Network models in anatomical systems. J Anthropol Sci 89:175–184

    Google Scholar 

  • 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) 320:489–500

    Article  Google Scholar 

  • 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 40:209–219

    Article  Google Scholar 

  • 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 41:52–61

    Google Scholar 

  • Fox-Keller E (2005) Revisiting ‘scale-free’ networks. BioEssays 27:1060–1068

    Article  Google Scholar 

  • Gaffney ES (1979) Comparative cranial morphology of recent and fossil turtles. Bull Am Mus Nat Hist 164:65–376

    Google Scholar 

  • Geoffroy Saint-Hilaire E (1818) Philosophie anatomique. J. B. Baillière, Paris

    Google Scholar 

  • 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 142:367–379

    Article  Google Scholar 

  • Gould SJ (2002) The structure of evolutionary theory. Harvard University Press, Cambridge

    Google Scholar 

  • Gregory WK (1935) ‘Williston’s law’ relating to the evolution of skull bones in the vertebrates. Am J Phys Anthropol 20:123–152

    Article  Google Scholar 

  • Guimerà R, Amaral LAN (2005) Functional cartography of complex metabolic networks. Nature 433:895–900

    Article  Google Scholar 

  • Guimerà R, Sales-Pardo M, Amaral LAN (2007) Classes of complex networks defined by role-to-role connectivity profiles. Nat Phys 3:63–69

    Article  Google Scholar 

  • Hallgrímsson B, Hall BK (eds) (2011) Epigenetics: linking genotype and phenotype in development and evolution. University of California Press, Berkeley

    Google Scholar 

  • Hasty J, Mcmillen D, Isaacs F et al (2001) Computational studies of gene regulatory networks. Nat Rev Genet 2:268–279

    Article  Google Scholar 

  • Horvath S, Dong J (2008) Geometric interpretation of gene coexpression network analysis. PLoS Comput Biol 4:e1000117

    Article  Google Scholar 

  • 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 79–90

    Chapter  Google Scholar 

  • Hull DL (1988) Science as a process: an evolutionary account of the social and conceptual development of science. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Humphries MD, Gurney K (2008) Network ‘small-world-ness’: a quantitative method for determining canonical network equivalence. PLoS One 3:e0002051

    Article  Google Scholar 

  • Huxley J (1932) Problems of relative growth. Methuen, London

    Google Scholar 

  • Jacob F (1977) Evolution and tinkering. Science 196:1161–1166

    Article  Google Scholar 

  • Jaslow CR (1990) Mechanical properties of cranial sutures. J Biomech 23:313–321

    Article  Google Scholar 

  • Klingenberg CP (2010) Evolution and development of shape: integrating quantitative approaches. Nat Rev Genet 11:623–635

    Google Scholar 

  • Knight CG, Pinney JW (2009) Making the right connections: biological networks in the light of evolution. BioEssays 31:1080–1090

    Article  Google Scholar 

  • Le Guyader H (2003) Geoffroy Saint-Hilaire: a visionary naturalist. University of Chicago Press, Chicago

    Google Scholar 

  • Magwene PM (2001) New tools for studying integration and modularity. Evolution 55:1734–1745

    Article  Google Scholar 

  • Magwene PM (2008) Using correlation proximity graphs to study phenotypic integration. Evol Biol 35:191–198

    Article  Google Scholar 

  • Mason O, Verwoerd M (2007) Graph theory and networks in biology. Syst Biol 1:89–119

    Google Scholar 

  • Mayr E (1982) The growth of biological thought: diversity, evolution, and inheritance. Harvard University Press, Cambridge

    Google Scholar 

  • McShea DW (1993) Evolutionary change in the morphological complexity of the mammalian vertebral column. Evolution 47:730–740

    Article  Google Scholar 

  • Mcshea DW, Brandon RN (2010) Biology’s first law: the tendency for diversity and complexity to increase in evolutionary systems. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Mcshea DW, Hordijk W (2013) Complexity by subtraction. Evol Biol 40:504–520

    Article  Google Scholar 

  • 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 276:39–46

    Article  Google Scholar 

  • 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 499–524

    Google Scholar 

  • Müller GB, Newman SA (eds) (2003) Origination of organismal form: beyond the gene in developmental and evolutionary biology. MIT Press, Cambridge

    Google Scholar 

  • Newman ME (2005) Power laws, Pareto distributions and Zipf’s law. Contemp Phys 46:323–351

    Article  Google Scholar 

  • 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 49–95

    Chapter  Google Scholar 

  • Newman ME, Girvan M (2004) Finding and evaluating community structure in networks. Phys Rev E 69:026113

    Article  Google Scholar 

  • 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 

  • 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 Paris

  • Ochoa C, Barahona A (2009) El debate entre Cuvier y Geoffroy, y el origen de la homología y la analogía. Ludus Vitalis 17:37–54

    Google Scholar 

  • Opperman LA (2000) Cranial sutures as intramembranous bone growth sites. Dev Dyn 219:472–485

    Article  Google Scholar 

  • Pearson K, Woo T (1935) Further investigation of the morphometric characters of the individual bones of the human skull. Biometrika 27:424–465

    Article  Google Scholar 

  • Porter MA, Onnela J-P, Mucha PJ (2009) Communities in networks. Not Am Math Soc 56:1082–1097

    Google Scholar 

  • Proulx SR, Promislow DE, Phillips PC (2005) Network thinking in ecology and evolution. Trends Ecol Evol 20:345–353

    Article  Google Scholar 

  • Raff RA (1996) The shape of life: genes, development, and the evolution of animal form. University of Chicago Press, Chicago

    Google Scholar 

  • Rafferty KL, Herring SW, Marshall CD (2003) Biomechanics of the rostrum and the role of facial sutures. J Morphol 257:33–44

    Article  Google Scholar 

  • Rashevsky N (1954) Topology and life: in search of general mathematical principles in biology and sociology. Bull Math Biophys 16:317–348

    Article  Google Scholar 

  • Rashevsky N (1960) Contributions to relational biology. Bull Math Biophys 22:73–84

    Article  Google Scholar 

  • 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 305–322

    Google Scholar 

  • 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 67–84

    Google Scholar 

  • Rasskin-Gutman D, Buscalioni AD (2001) Theoretical morphology of the Archosaur (Reptilia: Diapsida) pelvic girdle. Paleobiology 27:59–78

    Article  Google Scholar 

  • Ravasz E, Barabási A-L (2003) Hierarchical organization in complex networks. Phys Rev E 67:026112

    Article  Google Scholar 

  • Ravasz E, Somera AL, Mongru DA et al (2002) Hierarchical organization of modularity in metabolic networks. Science 297:1551–1555

    Article  Google Scholar 

  • Rice D (2008) Developmental anatomy of craniofacial sutures. In: Rice DP (ed) Craniofacial sutures, development, disease and treatment. Karger, Basel, pp 1–21

    Chapter  Google Scholar 

  • Riedl R (1978) Order in living organisms: a systems analysis of evolution. Wiley, New York

    Google Scholar 

  • Rieppel O (2006) ‘Type’ in morphology and phylogeny. J Morphol 267:528–535

    Article  Google Scholar 

  • Rosen R (1991) Life itself: a comprehensive inquiry into the nature, origin, and fabrication of life. Columbia University Press, New York

    Google Scholar 

  • Rosen R (2000) Essays on life itself. Columbia University Press, New York

    Google Scholar 

  • Russell ES (1916) Form and function: a contribution to the history of animal morphology. John Murray, London

    Book  Google Scholar 

  • Sales-Pardo M, Guimera R, Moreira AA et al (2007) Extracting the hierarchical organization of complex systems. Proc Natl Acad Sci 104:15224–15229

    Article  Google Scholar 

  • Sardi ML, Ramirez Rozzi F, Pucciarelli HM (2004) The Neolithic transition in Europe and North Africa: the functional craneology contribution. Anthropol Anz 62:129–145

    Google Scholar 

  • Schoch RR (2010) Riedl’s burden and the body plan: selection, constraint, and deep time. J Exp Zool B (Mol Dev Evol) 314:1–10

    Article  Google Scholar 

  • Sidor CA (2001) Simplification as a trend in synapsid cranial evolution. Evolution 55:1419–1442

    Article  Google Scholar 

  • Simon HA (1962) The architecture of complexity. Proc Am Philos Soc 106:467–482

    Google Scholar 

  • Simpson GG (1961) Principles of animal taxonomy. Columbia University Press, New York

    Google Scholar 

  • Solé RV, Valverde S, Rodríguez-Caso C (2006) Modularity in biological networks. In: Képès F (ed) Biological networks. World Scientific, Singapore, pp 21–40

    Google Scholar 

  • Sorkin A, Von Zastrow M (2009) Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol 10:609–622

    Article  Google Scholar 

  • Sporns O (2002) Network analysis, complexity, and brain function. Complexity 8:56–60

    Article  Google Scholar 

  • Thompson DW (1942) On growth and form. Cambridge University Press, Cambridge

    Google Scholar 

  • Thomson KS (1995) Graphical analysis of dermal skull roof patterns. In: Thomason JJ (ed) Functional morphology in vertebrate paleontology. Cambridge University Press, Cambridge, pp 193–204

    Google Scholar 

  • 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) 302:92–102

    Article  Google Scholar 

  • Wagner GP, Pavlicev M, Cheverud JM (2007) The road to modularity. Nat Rev Genet 8:921–931

    Article  Google Scholar 

  • Watts DJ, Strogatz SH (1998) Collective dynamics of ‘small-world’ networks. Nature 393:440–442

    Article  Google Scholar 

  • 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 303–344

    Google Scholar 

  • Weiss PA (1971) The basic concept of hierarchic system. In: Weiss PA (ed) Hierarchically organized systems in theory and practice. Hafner, New York, pp 1–44

    Google Scholar 

  • Woo T (1931) On the asymmetry of the human skull. Biometrika 22:324–352

    Article  Google Scholar 

  • 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 95–120

    Google Scholar 

  • 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 165–181

    Chapter  Google Scholar 

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Acknowledgments

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.

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  1. Theoretical Biology Research Group, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, Valencia, Spain

    Diego Rasskin-Gutman & Borja Esteve-Altava

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  1. Diego Rasskin-Gutman
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Correspondence to Diego Rasskin-Gutman.

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Rasskin-Gutman, D., Esteve-Altava, B. Connecting the Dots: Anatomical Network Analysis in Morphological EvoDevo. Biol Theory 9, 178–193 (2014). https://doi.org/10.1007/s13752-014-0175-x

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