How different types of pattern formation mechanisms affect the evolution of form and development

Here we investigate how development and evolution can affect each other by exploring what kind of phenotypic variation is produced by different types of developmental mechanisms. A limited number of developmental mechanisms are capable of pattern formation in development. Two main types have been identified. In morphodynamic mechanisms, induction events and morphogenetic processes, such as simple growth, act at the same time. In morphostatic mechanisms, induction events happen before morphogenetic mechanisms, and thus growth cannot influence the induction of a pattern. We present a study of the variational properties of these developmental mechanisms that can help to understand how and why a developmental mechanism may become involved in the evolution and development of a particular morphological structure. Using existing models of pattern formation in teeth, an extensive simulation analysis of the phenotypic variation produced by different types of developmental mechanisms is performed. The studied properties include the amount and diversity of the phenotypic variation produced, the complexity of the phenotypic variation produced, and the relationship between phenotype and genotype. These variational properties are so different between different types of mechanisms that the relative involvement of these types of mechanisms in evolutionary innovation and in different stages of development can be estimated. In addition, type of mechanism affects the tempo and mode of morphological evolution. These results suggest that the basic principles by which development is organized can influence the likelihood of morphological evolution.

[1]  R. Solé,et al.  Phenotypic and dynamical transitions in model genetic networks I. Emergence of patterns and genotype‐phenotype relationships , 2001, Evolution & development.

[2]  P. Alberch.  Ontogenesis and Morphological Diversification , 1980 .

[3]  G. Wagner,et al.  NOVELTY IN EVOLUTION: RESTRUCTURING THE CONCEPT , 1991 .

[4]  L. Wolpert.  Positional information and the spatial pattern of cellular differentiation. , 1969, Journal of theoretical biology.

[5]  Isaac Salazar-Ciudad,et al.  A gene network model accounting for development and evolution of mammalian teeth , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[6]  D. Tautz,et al.  Redundancies, development and the flow of information. , 1992, BioEssays : news and reviews in molecular, cellular and developmental biology.

[7]  M. Félix.  Evolution of developmental mechanisms in nematodes. , 1999, The Journal of experimental zoology.

[8]  P. Alberch,et al.  Size dependence during the development of the amphibian foot. Colchicine-induced digital loss and reduction. , 1983, Journal of embryology and experimental morphology.

[9]  G B Müller,et al.  Epigenetic mechanisms of character origination. , 2000, The Journal of experimental zoology.

[10]  Walter J. Bock,et al.  PREADAPTATION AND MULTIPLE EVOLUTIONARY PATHWAYS , 1959 .

[11]  L. Wolpert.  Positional information revisited. , 1989, Development.

[12]  S. Fullerton,et al.  Phenogenetic drift and the evolution of genotype-phenotype relationships. , 2000, Theoretical population biology.

[13]  P. Sternberg,et al.  Two nested gonadal inductions of the vulva in nematodes. , 1997, Development.

[14]  S. Carroll,et al.  Drosophila wing melanin patterns form by vein-dependent elaboration of enzymatic prepatterns , 1999, Current Biology.

[15]  R V Solé,et al.  Phenotypic and dynamical transitions in model genetic networks II. Application to the evolution of segmentation mechanisms , 2001, Evolution & development.

[16]  Neil Shubin,et al.  EVOLUTION AND MORPHOGENETIC RULES: THE SHAPE OF THE VERTEBRATE LIMB IN ONTOGENY AND PHYLOGENY , 1988, Evolution; international journal of organic evolution.

[17]  Isaac Salazar-Ciudad,et al.  Mechanisms of pattern formation in development and evolution , 2003, Development.

[18]  Arnold H. Buss.  Pathways , 2002, Journal of personality assessment.

[19]  P. Gingerich,et al.  Rates of evolution in the dentition of early Eocene Cantius: comparison of size and shape , 1994, Paleobiology.

[20]  I. Thesleff,et al.  Reiterative signaling and patterning during mammalian tooth morphogenesis , 2000, Mechanisms of Development.

[21]  Günter P. Wagner,et al.  How can a character be developmentally constrained despite variation in developmental pathways? , 1993 .

[22]  P. Alberch,et al.  Developmental Constraints in Evolutionary Processes , 1982 .

[23]  Brian C. Goodwin,et al.  How the Leopard Changed Its Spots , 1995 .

[24]  Stuart A. Newman,et al.  24 – Epigenetic Mechanisms of Character Origination , 2001 .

[25]  P. Sternberg,et al.  Competence and commitment of Caenorhabditis elegans vulval precursor cells. , 1999, Developmental biology.

[26]  Ernst Mayr,et al.  The emergence of evolutionary novelties , 1976 .

[27]  S. Wright.  Notes on the Anatomy of the Trematode, Microphallus opacus , 1912 .

[28]  P. R. Sheldon.  Plus ça change — a model for stasis and evolution in different environments , 1996 .

[29]  P. D. Polly.  On morphological clocks and paleophylogeography: towards a timescale for Sorex hybrid zones , 2004, Genetica.

[30]  G. Townsend,et al.  Molar Intercuspal Dimensions: Genetic Input to Phenotypic Variation , 2003, Journal of dental research.

[31]  An exercise in rational taxonomy. , 1990, Journal of theoretical biology.

[32]  H. Nijhout,et al.  The development and evolution of butterfly wing patterns , 1991 .

[33]  S. A. Barnett,et al.  The major features of evolution , 1955 .

[34]  Karel F. Liem,et al.  Evolutionary Strategies and Morphological Innovations: Cichlid Pharyngeal Jaws , 1973 .

[35]  Neil Shubin,et al.  MORPHOLOGICAL VARIATION IN THE LIMBS OF TARICHA GRANULOSA (CAUDATA: SALAMANDRIDAE): EVOLUTIONARY AND PHYLOGENETIC IMPLICATIONS , 1995, Evolution; international journal of organic evolution.

[36]  R. Solé,et al.  Gene networks capable of pattern formation: from induction to reaction-diffusion. , 2000, Journal of theoretical biology.

[37]  D. Wake,et al.  On the problem of stasis in organismal evolution , 1983 .

[38]  S. Gould,et al.  Punctuated equilibria: the tempo and mode of evolution reconsidered , 1977, Paleobiology.

[39]  Martin A. Nowak,et al.  Evolution of genetic redundancy , 1997, Nature.

[40]  J. Jernvall.  Linking development with generation of novelty in mammalian teeth. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[41]  M. England.  Morphogenesis: The Cellular and Molecular Processes of Developmental Anatomy. , 1991 .

[42]  Natural and experimental reduction of the avian fibula: Developmental thresholds and evolutionary constraint , 1992, Journal of morphology.