Modularity, evolvability, and adaptive radiations: a comparison of the hemi‐ and holometabolous insects

SUMMARY Despite recent attention given to the concept of modularity and its potential contribution to the evolvability of organisms, there has been little mention of how such a contribution may affect rates of diversification or how this would be assessed. A first key prediction is that lineages with relatively greater degrees of modularity in given traits should exhibit higher rates of diversification. Four general conditions for testing this prediction of the modular evolvability hypothesis are outlined here. The potential role of modularity as a deterministic factor in adaptive radiations is best examined by looking at historic patterns of diversification rather than just levels of extant diversity, the focus of most analyses of key innovations.

[1]  B. Ebenman.  Evolution in Organisms that Change Their Niches during the Life Cycle , 1992, The American Naturalist.

[2]  M. West-Eberhard,et al.  Evolution in the light of developmental and cell biology, and vice versa. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[3]  M. Conrad.  The geometry of evolution. , 1990, Bio Systems.

[4]  Brian D. Farrell,et al.  The Phylogenetic Study of Adaptive Zones: Has Phytophagy Promoted Insect Diversification? , 1988, The American Naturalist.

[5]  J. Sepkoski,et al.  Insect diversity in the fossil record. , 1993, Science.

[6]  J. Truman,et al.  The origins of insect metamorphosis , 1999, Nature.

[7]  C. Mitter,et al.  EVOLUTIONARY ORIGIN OF THE CYCLORRHAPHA (DIPTERA): TEST OF ALTERNATIVE MORPHOLOGICAL HYPOTHESES , 1993, Cladistics : the international journal of the Willi Hennig Society.

[8]  Robert N. Brandon,et al.  The Units of Selection Revisited: The Modules of Selection , 1999 .

[9]  R. Zack.  The Insects of Australia—A Textbook for Students and Research Workers , 1993 .

[10]  J. Kukalová-Peck.  Fossil history and the evolution of Hexapod structures , 1991 .

[11]  G. Wagner.  HOMOLOGUES, NATURAL KINDS AND THE EVOLUTION OF MODULARITY , 1996 .

[12]  N. Moran.  Adaptation and Constraint in the Complex Life Cycles of Animals , 1994 .

[13]  R. Lande.  The dynamics of peak shifts and the pattern of morphological evolution , 1986, Paleobiology.

[14]  A System Favoring the Evolution of Holometabolous Development , 1969 .

[15]  Lennart Persson,et al.  Size-Structured Populations , 1988, Springer Berlin Heidelberg.

[16]  E. Paradis.  Detecting Shifts in Diversification Rates without Fossils , 1998, The American Naturalist.

[17]  B. Ebenman.  Niche differences between age classes and intraspecific competition in age-structured populations , 1987 .

[18]  I. Mackerras.  The insects of Australia. A textbook for students and research workers. , 1970 .

[19]  M. Wake,et al.  The origin and evolution of larval forms , 1999 .

[20]  E. Werner.  Size, Scaling, and the Evolution of Complex Life Cycles , 1988 .

[21]  Joseph B. Slowinski,et al.  Testing the Stochasticity of Patterns of Organismal Diversity: An Improved Null Model , 1989, The American Naturalist.

[22]  P. Švácha.  What are and what are not imaginal discs: reevaluation of some basic concepts (Insecta, Holometabola). , 1992, Developmental biology.

[23]  M. Donoghue,et al.  Shifts in Diversification Rate with the Origin of Angiosperms , 1994, Science.

[24]  F. Sehnal,et al.  1 – Evolution of Insect Metamorphosis , 1996 .

[25]  C. Guyer,et al.  COMPARISONS OF OBSERVED PHYLOGENETIC TOPOLOGIES WITH NULL EXPECTATIONS AMONG THREE MONOPHYLETIC LINEAGES , 1991, Evolution; international journal of organic evolution.

[26]  J. Cheverud.  Developmental Integration and the Evolution of Pleiotropy , 1996 .

[27]  Joe C. Campbell,et al.  Developmental Constraints and Evolution: A Perspective from the Mountain Lake Conference on Development and Evolution , 1985, The Quarterly Review of Biology.

[28]  D. Brooks,et al.  Comparative Study of Adaptive Radiations with an Example Using Parasitic Flatworms (Platyhelminthes: Cercomeria) , 1993, The American Naturalist.

[29]  C. Labandeira,et al.  A Carboniferous insect gall: insight into early ecologic history of the Holometabola. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[30]  L. Nagy,et al.  CHANGING PATTERNS OF GENE REGULATION IN THE EVOLUTION OF ARTHROPOD MORPHOLOGY , 1998 .

[31]  R. Raikow.  The Analysis of Evolutionary Success , 1988 .

[32]  R. Raff.  Understanding Evolution: The Next Step. (Book Reviews: The Shape of Life. Genes, Development, and the Evolution of Animal Form.) , 1996 .

[33]  C. Guyer,et al.  ADAPTIVE RADIATION AND THE TOPOLOGY OF LARGE PHYLOGENIES , 1993, Evolution; international journal of organic evolution.

[34]  J. Cheverud,et al.  Quantitative genetics and developmental constraints on evolution by selection. , 1984, Journal of theoretical biology.

[35]  C. Labandeira.  INSECT MOUTHPARTS:Ascertaining the Paleobiology of Insect Feeding Strategies , 1997 .

[36]  E. Paradis.  Assessing temporal variations in diversification rates from phylogenies: estimation and hypothesis testing , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[37]  D. Borror,et al.  An introduction to the study of insects , 1954 .

[38]  An introduction to the study of insects . 6th edition. By D. J. Borror, C. A. Triplehorn and N. F. Johnson. (Philadelphia, Saunders College Publishing, 1989) 875 pp. Hard cover £23.50. ISBN 0-03-025397-7. , 1991 .

[39]  Conrad C. Labandeira,et al.  EARLY HISTORY OF ARTHROPOD AND VASCULAR PLANT ASSOCIATIONS , 1998 .

[40]  L. Nagy,et al.  Cell Lineages in Larval Development and Evolution of Holometabolous Insects , 1999 .

[41]  R. Raikow,et al.  Why are there so Many Kinds of Passerine Birds , 1986 .

[42]  J. Jernvall,et al.  The hypocone as a key innovation in mammalian evolution. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[43]  A. D. Imms.  general textbook of entomology , 1957 .

[44]  R. Raff,et al.  Modularity and dissociation in the evolution of gene expression territories in development , 2000, Evolution & development.

[45]  Brian D. Farrell,et al.  "Inordinate Fondness" explained: why are there So many beetles? , 1998, Science.

[46]  Robin Andrews,et al.  The Science of Entomology , 1975 .

[47]  C. Mitter,et al.  Diversification of Carnivorous Parasitic Insects: Extraordinary Radiation or Specialized Dead End? , 1993, The American Naturalist.

[48]  Stephen Jay Gould,et al.  Stochastic Models of Phylogeny and the Evolution of Diversity , 1973, The Journal of Geology.

[49]  K. Dial,et al.  Nonrandom Diversification within Taxonomic Assemblages , 1989 .

[50]  L. Altenberg,et al.  PERSPECTIVE: COMPLEX ADAPTATIONS AND THE EVOLUTION OF EVOLVABILITY , 1996, Evolution; international journal of organic evolution.

[51]  M. Donoghue,et al.  Reconstructing shifts in diversification rates on phylogenetic trees. , 1996, Trends in ecology & evolution.

[52]  H. Evans.  Insect Biology: A Textbook of Entomology , 1984 .

[53]  K. Dial,et al.  Nonrandom Diversification with in Taxonomic Assemblages , 1989 .

[54]  P. Cranston,et al.  The Insects - An Outline of Entomology , 1994 .

[55]  M. Mckitrick,et al.  Phylogenetic Constraint in Evolutionary Theory: Has It Any Explanatory Power? , 1993 .

[56]  G. von Dassow,et al.  Modularity in animal development and evolution: elements of a conceptual framework for EvoDevo. , 1999, The Journal of experimental zoology.

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

[58]  J. Gerhart,et al.  Cells, Embryos and Evolution , 1997 .

[59]  R. Raff,et al.  Dissociability, modularity, evolvability , 2000, Evolution & development.

[60]  J. Whitfield.  The Insects: An Outline of Entomology , 1995 .

[61]  J. Slowinski,et al.  Evidence from molecular systematics for decreased avian diversification in the pleistocene Epoch. , 1995, Proceedings of the National Academy of Sciences of the United States of America.