Methods for the analysis of developmental sequence data

SUMMARY Heterochrony, evolutionary changes in developmental timing, can be studied either by examining changes in growth or changes in the sequence of developmental events. Developmental sequence data has the potential to address many important questions in the field of developmental evolution, but methodological challenges remain due to the biological and logical dependence of events in a ranked sequence. In the past 10 years, the study of sequence heterochrony has undergone a rebirth, with the creation of several new methods for the analysis of this type of data. These methods can be divided into two broad categories: phenetic comparisons between terminal taxa that strive to uncover integrations within the developmental sequences and putative shared sequence heterochronies, and phylogeny‐based methods that derive ancestor‐descendent sequence heterochronies and establish statements of sequence evolution. In this review, we will discuss the strengths and weaknesses of the methodologies that have been proposed to quantitatively examine developmental sequence data, and studies that have attempted to implement them in an evolutionary context.

[1]  H. Larsson,et al.  Comparative ossification sequence and skeletal development of the postcranium of palaeognathous birds (Aves: Palaeognathae) , 2009 .

[2]  V. Weisbecker,et al.  Conserved relative timing of cranial ossification patterns in early mammalian evolution , 2008, Evolution & development.

[3]  E. Maxwell Ossification sequence of the avian order anseriformes, with comparison to other precocial birds , 2008, Journal of morphology.

[4]  S. Wroe,et al.  Ossification Heterochrony in the Therian Postcranial Skeleton and the Marsupial–Placental Dichotomy , 2008, Evolution; international journal of organic evolution.

[5]  M. Colbert,et al.  Ontogenetic Sequence Analysis: using parsimony to characterize developmental sequences and sequence polymorphism. , 2008, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[6]  H. Larsson,et al.  Estimating evolution of temporal sequence changes: a practical approach to inferring ancestral developmental sequences and sequence heterochrony. , 2008, Systematic biology.

[7]  A. Blejec,et al.  Can heterochrony help explain the high morphological diversity within the genus Niphargus (Crustacea: Amphipoda)? , 2008 .

[8]  E. Maxwell Comparative embryonic development of the skeleton of the domestic turkey (Meleagris gallopavo) and other galliform birds. , 2008, Zoology.

[9]  J. Hanken,et al.  Forelimb-hindlimb developmental timing changes across tetrapod phylogeny , 2007, BMC Evolutionary Biology.

[10]  L. Olsson,et al.  Heterochronic shifts during early cranial neural crest cell migration in two ranid frogs , 2007 .

[11]  A. Goswami Cranial modularity and sequence heterochrony in mammals , 2007, Evolution & development.

[12]  J. Spicer,et al.  An integrative approach identifies developmental sequence heterochronies in freshwater basommatophoran snails , 2007, Evolution & development.

[13]  R. Carroll,et al.  Limb ossification in the Paleozoic branchiosaurid Apateon (Temnospondyli) and the early evolution of preaxial dominance in tetrapod limb development , 2007, Evolution & development.

[14]  S. Poe TEST OF VON BAER'S LAW OF THE CONSERVATION OF EARLY DEVELOPMENT , 2006, Evolution; international journal of organic evolution.

[15]  R. Schoch Skull ontogeny: developmental patterns of fishes conserved across major tetrapod clades , 2006, Evolution & development.

[16]  M. Coates,et al.  A new technique for identifying sequence heterochrony. , 2005, Systematic biology.

[17]  S. King Relative timing of ontogenetic events in primates , 2004 .

[18]  M. Wake,et al.  Quantitative Tests of General Models for the Evolution of Development , 2004, The American Naturalist.

[19]  S. Poe A TEST FOR PATTERNS OF MODULARITY IN SEQUENCES OF DEVELOPMENTAL EVENTS , 2004, Evolution; international journal of organic evolution.

[20]  Ward C Wheeler,et al.  Comparative and phylogenetic analysis of developmental sequences , 2004, Evolution & development.

[21]  M. Richardson,et al.  Is Sequence Heterochrony an Important Evolutionary Mechanism in Mammals? , 2003, Journal of Mammalian Evolution.

[22]  Kathleen K. Smith Time's arrow: heterochrony and the evolution of development. , 2003, The International journal of developmental biology.

[23]  G. Schlosser Mosaic evolution of neural development in anurans: acceleration of spinal cord development in the direct developing frog Eleutherodactylus coqui , 2003, Anatomy and Embryology.

[24]  J. Yeh THE EVOLUTION OF DEVELOPMENT: TWO PORTRAITS OF SKULL OSSIFICATION IN PIPOID FROGS , 2002, Evolution; international journal of organic evolution.

[25]  M. Sánchez-Villagra Comparative patterns of postcranial ontogeny in therian mammals: an analysis of relative timing of ossification events. , 2002, The Journal of experimental zoology.

[26]  J. Maisano The potential utility of postnatal skeletal developmental patterns in squamate phylogenetics , 2002 .

[27]  M. Coates,et al.  Analyzing evolutionary patterns in amniote embryonic development * , 2002, Evolution & development.

[28]  M. Coates,et al.  Analyzing developmental sequences within a phylogenetic framework. , 2002, Systematic biology.

[29]  G. Schlosser Using heterochrony plots to detect the dissociated coevolution of characters. , 2001, The Journal of experimental zoology.

[30]  R. Guralnick,et al.  RECONNECTING CELL AND ANIMAL LINEAGES: WHAT DO CELL LINEAGES TELL US ABOUT THE EVOLUTION AND DEVELOPMENT OF SPIRALIA? , 2001, Evolution; international journal of organic evolution.

[31]  Kathleen K. Smith Heterochrony revisited: the evolution of developmental sequences , 2001 .

[32]  E. Tchernov,et al.  Variation in anuran embryogenesis: differences in sequence and timing of early developmental events. , 2000, The Journal of experimental zoology.

[33]  Paula M. Mabee,et al.  AN EXPERIMENTAL STUDY OF INTRASPECIFIC VARIATION, DEVELOPMENTAL TIMING, AND HETEROCHRONY IN FISHES , 2000, Evolution; international journal of organic evolution.

[34]  B. Sanchiz,et al.  Evolutionary mechanisms of rib loss in anurans: A comparative developmental approach , 2000, Journal of morphology.

[35]  H. Larsson A new method for comparing ontogenetic and phylogenetic data and its application to the evolution of the crocodilian secondary palate , 1998 .

[36]  C. Nunn,et al.  Statistical Analyses of Developmental Sequences: The Craniofacial Region in Marsupial and Placental Mammals , 1998, The American Naturalist.

[37]  Kathleen K. Smith COMPARATIVE PATTERNS OF CRANIOFACIAL DEVELOPMENT IN EUTHERIAN AND METATHERIAN MAMMALS , 1997, Evolution; international journal of organic evolution.

[38]  G. Roth,et al.  Evolution of Nerve Development in Frogs; pp. 112–128 , 1997 .

[39]  W. A. Velhagen,et al.  Analyzing developmental sequences using sequence units. , 1997, Systematic biology.

[40]  Paula M. Mabee,et al.  Development of the cranium and paired fins in Betta splendens (Teleostei: Percomorpha): Intraspecific variation and interspecific comparisons , 1996, Journal of morphology.

[41]  Kathleen K. Smith Integration of Craniofacial Structures During Development in Mammals , 1996 .

[42]  Paula M. Mabee,et al.  Coding Polymorphic Data: Examples from Allozymes and Ontogeny , 1993 .

[43]  R. Strauss HETEROCHRONIC VARIATION IN THE DEVELOPMENTAL TIMING OF CRANIAL OSSIFICATIONS IN POECILIID FISHES (CYPRINODONTIFORMES) , 1990, Evolution; international journal of organic evolution.

[44]  P. Alberch,et al.  Problems with the Interpretation of Developmental Sequences , 1985 .

[45]  Olaf R. P. Bininda-Emonds,et al.  From Haeckel to event-pairing: the evolution of developmental sequences , 2002, Theory in Biosciences.

[46]  S. Koenemann,et al.  The limitations of ontogenetic data in phylogenetic analyses , 2002 .

[47]  John O. Reiss The phylogeny of amphibian metamorphosis. , 2002, Zoology.

[48]  G. Roth,et al.  Evolution of nerve development in frogs. I. The development of the peripheral nervous system in Discoglossus pictus (Discoglossidae). , 1997, Brain, behavior and evolution.