Comparative developmental genetics and the evolution of arthropod body plans.

The arthropods display a wide range of morphological diversity, varying tagmosis, as well as other aspects of the body plan, such as appendage and cuticular morphology. Here we review the roles of developmental regulatory genes in the evolution of arthropod morphology, with an emphasis on what is known from morphologically diverse species. Examination of tagmatic evolution reveals that these changes have been accompanied by changes in the expression patterns of Hox genes. In contrast, review of the modifications to wing morphology seen in insects shows that these body plan changes have generally favored alterations in downstream target genes. These and other examples are used to discuss the evolutionary implications of comparative developmental genetic data.

[1]  J. Kukalová-Peck Origin of the insect wing and wing articulation from the arthropodan leg , 1983 .

[2]  M. Kimura Evolutionary Rate at the Molecular Level , 1968, Nature.

[3]  D. Stern A role of Ultrabithorax in morphological differences between Drosophila species , 1998, Nature.

[4]  J. W. Flower On the origin of flight in insects , 1964 .

[5]  E. Davidson,et al.  Developmental gene regulatory network architecture across 500 million years of echinoderm evolution , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[6]  A. Abzhanov,et al.  Understanding the genetic basis of morphological evolution: the role of homeotic genes in the diversification of the arthropod bauplan. , 1998, The International journal of developmental biology.

[7]  T. Kaufman,et al.  Hox genes and the evolution of the arthropod body plan 1 , 2002, Evolution & development.

[8]  T. Kaufman,et al.  Functional analyses in the hemipteran Oncopeltus fasciatus reveal conserved and derived aspects of appendage patterning in insects. , 2004, Developmental biology.

[9]  R. Fortey,et al.  The Early Radiation and Relationships of the Major Arthropod Groups , 1989, Science.

[10]  J. Stuart,et al.  Genetic analysis of the homeotic gene complex (HOM-C) in the beetle Tribolium castaneum. , 1989, Developmental biology.

[11]  Tadao Matsumoto,et al.  Wing disc development during caste differentiation in the ant Pheidole megacephala (Hymenoptera: Formicidae) , 2004, Evolution & development.

[12]  R. H. Thomas,et al.  Expression of homeobox genes shows chelicerate arthropods retain their deutocerebral segment. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[13]  R. A. Fisher,et al.  The Genetical Theory of Natural Selection , 1931 .

[14]  One small step for worms, one giant leap for “Bauplan?” * , 2002, Evolution & development.

[15]  James M. Carpenter,et al.  The Phylogeny of the Extant Hexapod Orders , 2001, Cladistics : the international journal of the Willi Hennig Society.

[16]  A. Abzhanov,et al.  The Drosophila proboscis is specified by two Hox genes, proboscipedia and Sex combs reduced, via repression of leg and antennal appendage genes. , 2001, Development.

[17]  D. Tautz,et al.  Mitochondrial protein phylogeny joins myriapods with chelicerates , 2001, Nature.

[18]  S. Carroll,et al.  Ultrabithorax function in butterfly wings and the evolution of insect wing patterns , 1999, Current Biology.

[19]  J. Shultz,et al.  Elongation factor-2: a useful gene for arthropod phylogenetics. , 2001, Molecular phylogenetics and evolution.

[20]  T. Kaufman,et al.  Expression patterns of the rogue Hox genes Hox3/zen and fushi tarazu in the apterygote insect Thermobia domestica , 2004, Evolution & development.

[21]  Sean B. Carroll,et al.  Homeotic genes and the regulation and evolution of insect wing number , 1995, Nature.

[22]  Sean Carroll,et al.  Evolution of homeotic gene regulation and function in flies and butterflies , 1994, Nature.

[23]  T. Tregenza,et al.  Sexual selection and speciation. , 2001, Trends in ecology & evolution.

[24]  A. Abzhanov,et al.  Homologs of Drosophila appendage genes in the patterning of arthropod limbs. , 2000, Developmental biology.

[25]  D. Stern,et al.  Divergence of larval morphology between Drosophila sechellia and its sibling species caused by cis-regulatory evolution of ovo/shaven-baby. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Susan J. Brown,et al.  Homeotic evidence for the appendicular origin of the labrum in Tribolium castaneum , 2001, Development Genes and Evolution.

[27]  J. Gerhart,et al.  Inversion of the chordate body axis: are there alternatives? , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[28]  A. Abzhanov,et al.  Novel regulation of the homeotic gene Scr associated with a crustacean leg-to-maxilliped appendage transformation. , 1999, Development.

[29]  K. Ober,et al.  Hypothesis testing in evolutionary developmental biology: a case study from insect wings. , 2004, The Journal of heredity.

[30]  Taylor J. Maxwell,et al.  Loss and recovery of wings in stick insects , 2003, Nature.

[31]  L. Hood,et al.  Regulatory gene networks and the properties of the developmental process , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[32]  S. Carroll,et al.  Genetic control and evolution of sexually dimorphic characters in Drosophila , 2000, Nature.

[33]  M. Akam,et al.  Hox genes, homeosis and the evolution of segment identity: no need for hopeless monsters. , 1998, The International journal of developmental biology.

[34]  M. Schoppmeier,et al.  Double-stranded RNA interference in the spider Cupiennius salei: the role of Distal-less is evolutionarily conserved in arthropod appendage formation , 2001, Development Genes and Evolution.

[35]  J. M. MacLennan,et al.  Principles of Comparative Anatomy of Invertebrates , 1969 .

[36]  R. Snodgrass,et al.  Principles of Insect Morphology , 1993 .

[37]  J. Boore,et al.  Hexapod Origins: Monophyletic or Paraphyletic? , 2003, Science.

[38]  Eric H Davidson,et al.  Developmental gene network analysis. , 2003, The International journal of developmental biology.

[39]  S. Prescott,et al.  Regulatory evolution of shavenbaby / ovo underlies multiple cases of morphological parallelism , 2003 .

[40]  R. Cook,et al.  Behavioral role of the sexcombs inDrosophila melanogaster andDrosophila simulans , 1977, Behavior genetics.

[41]  T. Kaufman,et al.  RNAi analysis of Deformed, proboscipedia and Sex combs reduced in the milkweed bug Oncopeltus fasciatus: novel roles for Hox genes in the hemipteran head. , 2000, Development.

[42]  Michael Levine,et al.  Ciona intestinalis: an emerging model for whole-genome analyses. , 2003, Trends in genetics : TIG.

[43]  Stephen Jay Gould,et al.  The Return of Hopeful Monsters , 2006 .

[44]  U. Walldorf,et al.  Hox genes in the honey bee Apis mellifera , 2000, Development Genes and Evolution.

[45]  Z. Zheng,et al.  Homeotic gene expression in the wild-type and a homeotic mutant of the moth Manduca sexta , 1999, Development Genes and Evolution.

[46]  P. Ehrlich,et al.  Introduction to insect biology and diversity , 1978 .

[47]  N. Patel,et al.  Crustacean appendage evolution associated with changes in Hox gene expression , 1997, Nature.

[48]  P. Dong,et al.  Drosophila spalt/spalt-related mutants exhibit Townes-Brocks' syndrome phenotypes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[49]  M. Akam,et al.  Hox genes and the diversification of insect and crustacean body plans , 1995, Nature.

[50]  S. Cohen,et al.  Evolutionary origin of insect wings from ancestral gills , 1997, Nature.

[51]  A. Abzhanov,et al.  Crustacean (malacostracan) Hox genes and the evolution of the arthropod trunk. , 2000, Development.

[52]  G. Wray,et al.  Abundant raw material for cis-regulatory evolution in humans. , 2002, Molecular biology and evolution.

[53]  Y. Tomoyasu,et al.  Ultrabithorax is required for membranous wing identity in the beetle Tribolium castaneum , 2005, Nature.

[54]  Richard Owen,et al.  Lectures on the Comparative Anatomy and Physiology of Invertebrate Animals, Delivered at the Royal College of Surgeons in 1843 , 1844, Edinburgh Medical and Surgical Journal.

[55]  M. Averof,et al.  Diverse Adaptations of an Ancestral Gill A Common Evolutionary Origin for Wings, Breathing Organs, and Spinnerets , 2002, Current Biology.

[56]  Matthew W. Hahn,et al.  Positive Selection on a Human-Specific Transcription Factor Binding Site Regulating IL4 Expression , 2003, Current Biology.

[57]  J. True,et al.  Developmental system drift and flexibility in evolutionary trajectories , 2001, Evolution & development.

[58]  D. Tautz,et al.  A conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[59]  T. Kaufman,et al.  Exploring the myriapod body plan: expression patterns of the ten Hox genes in a centipede. , 2002, Development.

[60]  N. B. Eales,et al.  Invertebrates , 2003 .

[61]  W. Wheeler,et al.  Insect homeotic transformation , 1994, Nature.

[62]  C. Wilson,et al.  Identification of target genes of the homeotic gene Antennapedia by enhancer detection. , 1991, Genes & development.

[63]  T. Kaufman,et al.  The homeotic gene Sex combs reduced of Drosophila melanogaster is differentially regulated in the embryonic and imaginal stages of development. , 1991, Genetics.

[64]  R. Goldschmidt,et al.  Richard Goldschmidt : hopeful monsters and other ‘ heresies , 2002 .

[65]  E. Lewis A gene complex controlling segmentation in Drosophila , 1978, Nature.

[66]  J. Kukalová-Peck,et al.  New Homoiopteridae (Insecta: Paleodictyoptera) with wing articulation from Upper Carboniferous strata of Mazon Creek, Illinois , 1983 .

[67]  D. Tautz,et al.  Ribosomal DNA phylogeny of the major extant arthropod classes and the evolution of myriapods , 1995, Nature.

[68]  C. Waddington Canalization of Development and the Inheritance of Acquired Characters , 1942, Nature.

[69]  A. Abzhanov,et al.  Chelicerate Hox genes and the homology of arthropod segments , 1999, Evolution & development.

[70]  R. Goldschmidt,et al.  The material basis of evolution , 1941 .

[71]  A. Abzhanov,et al.  Embryonic expression patterns of the Hox genes of the crayfish Procambarus clarkii (Crustacea, Decapoda) , 2000, Evolution & development.

[72]  V. Hypša,et al.  Arthropod phylogeny: taxonomic congruence, total evidence and conditional combination approaches to morphological and molecular data sets , 1998 .

[73]  V. Laudet,et al.  The chordate amphioxus: an emerging model organism for developmental biology , 2004, Cellular and Molecular Life Sciences CMLS.

[74]  J. Shultz,et al.  Molecular phylogeny of the major arthropod groups indicates polyphyly of crustaceans and a new hypothesis for the origin of hexapods. , 1997, Molecular biology and evolution.

[75]  S. Ono Effect of juvenile hormone on the caste determination in the ant, Pheidole fervida SMITH (Hymenoptera: Formicidae) , 1982 .

[76]  M J White,et al.  Models of speciation. New concepts suggest that the classical sympatric and allopatric models are not the only alternatives. , 1968, Science.

[77]  T. Kaufman,et al.  Evolution of the insect body plan as revealed by the Sex combs reduced expression pattern. , 1997, Development.

[78]  Luis Puelles,et al.  Field homology as a way to reconcile genetic and developmental variability with adult homology , 2002, Brain Research Bulletin.

[79]  D. Parichy,et al.  Pigment patterns: fish in stripes and spots , 2003, Current Biology.

[80]  Susan J. Brown,et al.  Molecular and genetic analysis of the Tribolium Ultrabithorax ortholog, Ultrathorax , 1999, Development Genes and Evolution.

[81]  D. Hogness,et al.  Effect of Polymorphism in the Drosophila Regulatory Gene Ultrabithorax on Homeotic Stability , 1996, Science.

[82]  Gregory A. Wray,et al.  Evolution of the Gene Network Underlying Wing Polyphenism in Ants , 2002, Science.

[83]  R. Bajpai,et al.  Regulation of Wingless and Vestigial expression in wing and haltere discs of Drosophila , 2003, Development.

[84]  G. Odell,et al.  Design and constraints of the Drosophila segment polarity module: robust spatial patterning emerges from intertwined cell state switches. , 2002, The Journal of experimental zoology.

[85]  G. Budd A palaeontological solution to the arthropod head problem , 2002, Nature.

[86]  S. Carroll,et al.  Pattern formation and eyespot determination in butterfly wings. , 1994, Science.

[87]  R. Snodgrass,et al.  Principles of Insect Morphology , 1993 .

[88]  R. Beeman A homoeotic gene cluster in the red flour beetle , 1987, Nature.

[89]  Timothy M. Collins,et al.  Deducing the pattern of arthropod phytogeny from mitochondrial DNA rearrangements , 1995, Nature.

[90]  D. Lewis,et al.  Distinct roles of the homeotic genes Ubx and abd-A in beetle embryonic abdominal appendage development. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[91]  Maryline Blin,et al.  Possible implication of Hox genes Abdominal-B and abdominal-A in the specification of genital and abdominal segments in cirripedes , 2003, Development Genes and Evolution.

[92]  M. Pigliucci,et al.  PERSPECTIVE: GENETIC ASSIMILATION AND A POSSIBLE EVOLUTIONARY PARADOX: CAN MACROEVOLUTION SOMETIMES BE SO FAST AS TO PASS US BY? , 2003, Evolution; international journal of organic evolution.

[93]  W. McGinnis,et al.  The Drosophila Hox Gene Deformed Sculpts Head Morphology via Direct Regulation of the Apoptosis Activator reaper , 2002, Cell.

[94]  J. Kukalová-Peck The "Uniramia" do not exist: the ground plan of the Pterygota as revealed by Permian Diaphanopterodea from Russia (Insecta: Paleodictyopteroidea) , 1992 .

[95]  H. A. Orr,et al.  The evolutionary genetics of speciation. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[96]  N. Takahata,et al.  Paleo-demography of the Drosophila melanogaster subgroup: application of the maximum likelihood method. , 1999, Genes & genetic systems.

[97]  R. Beeman,et al.  Pondering the procephalon: the segmental origin of the labrum , 2001, Development Genes and Evolution.

[98]  S. Carroll,et al.  Ultrabithorax regulates genes at several levels of the wing-patterning hierarchy to shape the development of the Drosophila haltere. , 1998, Genes & development.

[99]  G. Morata How drosophila appendages develop , 2001, Nature Reviews Molecular Cell Biology.