Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history

Understanding how traits are integrated at the organismal level remains a fundamental problem at the interface of developmental and evolutionary biology. Hormones, regulatory signaling molecules that coordinate multiple developmental and physiological processes, are major determinants underlying phenotypic integration. The probably best example for this is the lipid‐like juvenile hormone (JH) in insects. Here we review the manifold effects of JH, the most versatile animal hormone, with an emphasis on the fruit fly Drosophila melanogaster, an organism amenable to both genetics and endocrinology. JH affects a remarkable number of processes and traits in Drosophila development and life history, including metamorphosis, behavior, reproduction, diapause, stress resistance and aging. While many molecular details underlying JH signaling remain unknown, we argue that studying “hormonal pleiotropy” offers intriguing insights into phenotypic integration and the mechanisms underlying life history evolution. In particular, we illustrate the role of JH as a key mediator of life history trade‐offs. BioEssays 27:999–1010, 2005. © 2005 Wiley Periodicals, Inc.

[1]  The Physiology of Ecdysis in Rhodnius Pro- lixus (Hemiptera). II. Factors controlling Moulting and 'Metamorphosis' , 2006 .

[2]  M. Tatar,et al.  Mutations in insulin signaling pathway alter juvenile hormone synthesis in Drosophila melanogaster. , 2005, General and comparative endocrinology.

[3]  You Zhou,et al.  Insulin signaling is necessary for vitellogenesis in Drosophila melanogaster independent of the roles of juvenile hormone and ecdysteroids: female sterility of the chico1 insulin signaling mutation is autonomous to the ovary. , 2005, Journal of insect physiology.

[4]  K. Miura,et al.  Characterization of the Drosophila Methoprene ‐tolerant gene product , 2005, The FEBS journal.

[5]  A. Yashin,et al.  What evidence is there for the existence of individual genes with antagonistic pleiotropic effects? , 2005, Mechanisms of Ageing and Development.

[6]  E. Dubrovsky Hormonal cross talk in insect development , 2005, Trends in Endocrinology & Metabolism.

[7]  Andreas Heyland,et al.  Hormone signaling in evolution and development: a non-model system approach. , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[8]  M. Tatar,et al.  Juvenile and Steroid Hormones in Drosophila melanogaster Longevity , 2005 .

[9]  T. Kawecki,et al.  Pleiotropic Effects of methoprene-tolerant(Met), a Gene Involved in Juvenile Hormone Metabolism, on Life History Traits in Drosophila melanogaster , 2004, Genetica.

[10]  S. Kato,et al.  Juvenile hormones antagonize ecdysone actions through co-repressor recruitment to EcR/USP heterodimers. , 2004, Biochemical and biophysical research communications.

[11]  M. Tatar,et al.  Drosophila dFOXO controls lifespan and regulates insulin signalling in brain and fat body , 2004, Nature.

[12]  A. Heyland,et al.  HETEROCHRONIC DEVELOPMENTAL SHIFT CAUSED BY THYROID HORMONE IN LARVAL SAND DOLLARS AND ITS IMPLICATIONS FOR PHENOTYPIC PLASTICITY AND THE EVOLUTION OF NONFEEDING DEVELOPMENT , 2004, Evolution; international journal of organic evolution.

[13]  Darren W. Williams,et al.  Mechanisms of Dendritic Elaboration of Sensory Neurons in Drosophila: Insights from In Vivo Time Lapse , 2004, The Journal of Neuroscience.

[14]  L. Gilbert,et al.  An ultrastructural and developmental analysis of the corpus allatum of juvenile hormone deficient mutants ofDrosophila melanogaster , 1993, Roux's archives of developmental biology.

[15]  Gerd B. Müller,et al.  Environment, development, and evolution : toward a synthesis , 2004 .

[16]  O. Catuneanu,et al.  Towards a Synthesis , 2004 .

[17]  T. Wilson,et al.  Juvenile hormone involvement in Drosophila melanogaster male reproduction as suggested by the Methoprene-tolerant(27) mutant phenotype. , 2003, Insect biochemistry and molecular biology.

[18]  C. Gillott Male accessory gland secretions: modulators of female reproductive physiology and behavior. , 2003, Annual review of entomology.

[19]  M. Rantala,et al.  The role of juvenile hormone in immune function and pheromone production trade-offs: a test of the immunocompetence handicap principle , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[20]  C. E. Allen,et al.  Genotype to Phenotype: Physiological Control of Trait Size and Scaling in Insects1 , 2003, Integrative and comparative biology.

[21]  A. Zera The Endocrine Regulation of Wing Polymorphism in Insects: State of the Art, Recent Surprises, and Future Directions1 , 2003, Integrative and comparative biology.

[22]  H. Nijhout,et al.  A perspective for understanding the modes of juvenile hormone action as a lipid signaling system. , 2003, BioEssays : news and reviews in molecular, cellular and developmental biology.

[23]  E. Kubli Sex-peptides: seminal peptides of the Drosophila male , 2003, Cellular and Molecular Life Sciences CMLS.

[24]  N. Perrimon,et al.  The retinoic-like juvenile hormone controls the looping of left-right asymmetric organs in Drosophila , 2003, Development.

[25]  M. Tatar,et al.  The Endocrine Regulation of Aging by Insulin-like Signals , 2003, Science.

[26]  M. West-Eberhard Developmental plasticity and evolution , 2003 .

[27]  E. Berger,et al.  Juvenile hormone signaling during oogenesis in Drosophila melanogaster. , 2002, Insect biochemistry and molecular biology.

[28]  B. Sinervo,et al.  Correlational selection and the evolution of genomic architecture , 2002, Heredity.

[29]  Jean-René Martin,et al.  Neuroendocrine control of a sexually dimorphic behavior by a few neurons of the pars intercerebralis in Drosophila , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[30]  M. Tatar,et al.  The demography of slow aging in male and female Drosophila mutant for the insulin‐receptor substrate homologue chico , 2002, Aging cell.

[31]  K. Nairz,et al.  Nutrient-Dependent Expression of Insulin-like Peptides from Neuroendocrine Cells in the CNS Contributes to Growth Regulation in Drosophila , 2002, Current Biology.

[32]  J. Rolff,et al.  Copulation corrupts immunity: A mechanism for a cost of mating in insects , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[33]  J. Apfeld,et al.  Regulation of Life-Span by Germ-Line Stem Cells in Caenorhabditis elegans , 2002, Science.

[34]  James W Truman,et al.  Endocrine insights into the evolution of metamorphosis in insects. , 2002, Annual review of entomology.

[35]  S. Dhar,et al.  Juvenile hormone III-dependent conformational changes of the nuclear receptor ultraspiracle. , 2001, Insect biochemistry and molecular biology.

[36]  L. Harshman,et al.  The Physiology of Life History Trade-Offs in Animals , 2001 .

[37]  R. Maleszka,et al.  Effect of Juvenile Hormone on Short-Term Olfactory Memory in Young Honeybees (Apis mellifera) , 2001, Hormones and Behavior.

[38]  R. Cooper,et al.  Effects of the ecdysoneless mutant on synaptic efficacy and structure at the neuromuscular junction in Drosophila larvae during normal and prolonged development , 2001, Neuroscience.

[39]  Nicholas K. Priest,et al.  Negligible Senescence during Reproductive Dormancy in Drosophila melanogaster , 2001, The American Naturalist.

[40]  D. Marx,et al.  A COST OF REPRODUCTION IN DROSOPHILA MELANOGASTER: STRESS SUSCEPTIBILITY , 2001, Evolution; international journal of organic evolution.

[41]  Jennifer M. Jones,et al.  Vitellogenesis in diapausing and mutant Drosophila melanogaster: further evidence for the relative roles of ecdysteroids and juvenile hormones , 2001 .

[42]  C. Kenyon,et al.  Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling , 2001, Nature Genetics.

[43]  M. Tatar,et al.  A Mutant Drosophila Insulin Receptor Homolog That Extends Life-Span and Impairs Neuroendocrine Function , 2001, Science.

[44]  E. Hafen,et al.  Extension of Life-Span by Loss of CHICO, a Drosophila Insulin Receptor Substrate Protein , 2001, Science.

[45]  M. Tatar,et al.  Slow aging during insect reproductive diapause: why butterflies, grasshoppers and flies are like worms , 2001, Experimental Gerontology.

[46]  E. Hafen,et al.  An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control , 2001, Current Biology.

[47]  Michelle M. Elekonich,et al.  Organizational and activational effects of hormones on insect behavior. , 2000, Journal of insect physiology.

[48]  C. Thummel,et al.  Steroid Regulation of Postembryonic Development and Reproduction in Drosophila , 2000, Trends in Endocrinology & Metabolism.

[49]  M. Ashok,et al.  Intracellular localization and tissue specificity of the Methoprene-tolerant (Met) gene product in Drosophila melanogaster. , 2000, Insect biochemistry and molecular biology.

[50]  K. Hartfelder Insect juvenile hormone: from "status quo" to high society. , 2000, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[51]  A. T. Proveaux,et al.  Mating experience and juvenile hormone enhance sexual signaling and mating in male Caribbean fruit flies. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[52]  S. Tobe,et al.  The Regulation of Juvenile Hormone Production in Arthropods: Functional and Evolutionary Perspectives , 1999, Annals of the New York Academy of Sciences.

[53]  Cynthia Kenyon,et al.  Signals from the reproductive system regulate the lifespan of C. elegans , 1999, Nature.

[54]  M. Bownes,et al.  Control of oocyte maturation in sexually mature Drosophila females. , 1999, Developmental biology.

[55]  D. Emlen,et al.  The developmental basis for allometry in insects. , 1999, Development.

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

[57]  B. Sinervo,et al.  MECHANISTIC AND SELECTIVE CAUSES OF LIFE HISTORY TRADE-OFFS AND PLASTICITY , 1998 .

[58]  C. Thummel,et al.  The RXR homolog ultraspiracle is an essential component of the Drosophila ecdysone receptor. , 1998, Development.

[59]  M. Ashok,et al.  Insecticide resistance resulting from an absence of target-site gene product. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[60]  L. Riddiford,et al.  The ecdysone receptor and ultraspiracle regulate the timing and progression of ovarian morphogenesis during Drosophila metamorphosis , 1998, Development Genes and Evolution.

[61]  L. Gilbert,et al.  Ecdysteroids regulate yolk protein uptake by Drosophila melanogaster oocytes. , 1998, Journal of insect physiology.

[62]  M. Ashok,et al.  Insect juvenile hormone resistance gene homology with the bHLH-PAS family of transcriptional regulators. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[63]  L. Restifo,et al.  A juvenile hormone agonist reveals distinct developmental pathways mediated by ecdysone-inducible broad complex transcription factors. , 1998, Developmental genetics.

[64]  P. Sharp,et al.  Ultraspiracle: an invertebrate nuclear receptor for juvenile hormones. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[65]  G. Prestwich,et al.  Hydroxy juvenile hormones: new putative juvenile hormones biosynthesized by locust corpora allata in vitro. , 1997, Biochemical and biophysical research communications.

[66]  G. Gäde,et al.  Hormonal regulation in insects: facts, gaps, and future directions. , 1997, Physiological reviews.

[67]  C. Strambi,et al.  Specific requirement of putrescine for the mitogenic action of juvenile hormone on adult insect neuroblasts. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[68]  H. Dingle,et al.  JUVENILE HORMONE AS A MEDIATOR OF PLASTICITY IN INSECT LIFE HISTORIES , 1997 .

[69]  S. Newton,et al.  Breeding biology and seasonal abundance of Lappet‐faced Vultures Torgos tracheliotus in western Saudi Arabia , 1996 .

[70]  M. Bownes,et al.  20-Hydroxyecdysone, but not juvenile hormone, regulation of yolk protein gene expression can be mapped to cis-acting DNA sequences. , 1996, Developmental biology.

[71]  L. Gilbert,et al.  2 – Endocrine Cascade in Insect Metamorphosis , 1996 .

[72]  L. Gilbert,et al.  Metamorphosis : postembryonic reprogramming of gene expression in amphibian and insect cells , 1996 .

[73]  G. R. Wyatt,et al.  Cellular and Molecular Actions of Juvenile Hormone. II. Roles of Juvenile Hormone in Adult Insects , 1996 .

[74]  D. Mangelsdorf,et al.  Activation of mammalian retinoid X receptors by the insect growth regulator methoprene. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[75]  C. Finch,et al.  Hormones and the Physiological Architecture of Life History Evolution , 1995, The Quarterly Review of Biology.

[76]  G. Jones Molecular mechanisms of action of juvenile hormone. , 1995, Annual review of entomology.

[77]  C. Strambi,et al.  Neurogenesis in an adult insect brain and its hormonal control , 1994, Nature.

[78]  L. Riddiford Cellular and Molecular Actions of Juvenile Hormone I. General Considerations and Premetamorphic Actions , 1994 .

[79]  M. Bate,et al.  The development of Drosophila melanogaster , 1993 .

[80]  D. Segal Prospects of using Drosophila for insect neuroendocrine research. , 1993, Archives of insect biochemistry and physiology.

[81]  E. Ketterson,et al.  Hormones and Life Histories: An Integrative Approach , 1992, The American Naturalist.

[82]  T. Wilson,et al.  The competitive ability and fitness components of the Methoprene-tolerant (Met) Drosophila mutant resistant to juvenile hormone analog insecticides. , 1992, Genetics.

[83]  L. Gilbert,et al.  Regulation of juvenile hormone synthesis in wild-type and apterous mutant Drosophila , 1991, Molecular and Cellular Endocrinology.

[84]  D. Segal,et al.  Female sexual receptivity is defective in juvenile hormone-deficient mutants of theapterous gene ofDrosophila melanogaster , 1991, Behavior genetics.

[85]  M. Ashburner,et al.  Effects of juvenile hormone mimics on larval development and metamorphosis of Drosophila melanogaster. , 1991, General and comparative endocrinology.

[86]  C. M. Lessells,et al.  The Evolution of Life Histories , 1994 .

[87]  L. Gilbert,et al.  Photoperiodic diapause in Drosophila melanogaster involves a block to the juvenile hormone regulation of ovarian maturation. , 1990, General and comparative endocrinology.

[88]  T. Wilson,et al.  Resistance to juvenile hormone and an insect growth regulator in Drosophila is associated with an altered cytosolic juvenile hormone-binding protein. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[89]  R. Matsuda Animal evolution in changing environments: with special reference to abnormal metamorphosis , 1989 .

[90]  M. Bownes,et al.  cricklet: A locus regulating a number of adult functions of Drosophila melanogaster. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[91]  L. Gilbert,et al.  Juvenile hormone bisepoxide biosynthesis in vitro by the ring gland of Drosophila melanogaster: a putative juvenile hormone in the higher Diptera. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[92]  M. Bownes The roles of juvenile hormone, ecdysone and the ovary in the control of Drosophila vitellogenesis , 1989 .

[93]  Judit Fabian,et al.  A Drosophila melanogaster mutant resistant to a chemical analog of juvenile hormone. , 1986, Developmental biology.

[94]  T. Kelly,et al.  The effects of nutrition and methoprene treatment on ovarian ecdysteroid synthesis in Drosophila melanogaster , 1985 .

[95]  S. Tobe,et al.  Structure and Regulation of the Corpus Allatum , 1985 .

[96]  T. Wilson,et al.  Precocene I and II inhibition of vitellogenic oöcyte development in Drosophila melanogaster , 1983 .

[97]  M. Bownes Hormonal and Genetic Regulation of Vitellogenesis in Drosophila , 1982, The Quarterly Review of Biology.

[98]  Diana E. Wheeler,et al.  Juvenile Hormone and the Physiological Basis of Insect Polymorphisms , 1982, The Quarterly Review of Biology.

[99]  J. Postlethwait,et al.  The Regulation of yolk polypeptide synthesis in Drosophila ovaries and fat body by 20-hydroxyecdysone and a juvenile hormone analog. , 1980, Developmental biology.

[100]  A. Handler,et al.  Nonvitellogenic female sterile mutants and the regulation of vitellogenesis in Drosophila melanogaster. , 1978, Developmental biology.

[101]  J. Postlethwait,et al.  Endocrine control of larval fat body histolysis in normal and mutant Drosophila melanogaster. , 1978, The Journal of experimental zoology.

[102]  R. H. Richardson The Screwworm problem: Evolution of resistance to biological control , 1978 .

[103]  A. Handler,et al.  Endocrine control of vitellogenesis in Drosophila melanogaster: effects of the brain and corpus allatum. , 1977, The Journal of experimental zoology.

[104]  J. Postlethwait,et al.  Vitellogenesis induced by juvenile hormone in the female sterile mutant apterous-four in Drosophila melanogaster. , 1973, Nature: New biology.

[105]  L. Lichtenstein,et al.  Increase in Histamine Receptors on Thymus-derived Effector Lymphocytes during the Primary Immune Response to Alloantigens , 1973, Nature.

[106]  C. Sweeley,et al.  The structure of juvenile hormone , 1967 .

[107]  A. Manning Corpus Allatum and Sexual Receptivity in Female Drosophila melanogaster , 1966, Nature.

[108]  R. King,et al.  The comparative submicroscopic cytology of the corpus allatum-corpus cardiacum complex of wild type and fes adult female Drosophila melanogaster , 1966 .

[109]  V B WIGGLESWORTH,et al.  INSECT HORMONES. , 1965, Endeavour.

[110]  W. W. Doane,et al.  Developmental physiology of the mutant female sterile(2)adipose of Drosophila melanogaster. III. Corpus allatum-complex and ovarian transplantations. , 1961, The Journal of experimental zoology.

[111]  D. Bodenstein HORMONES AND TISSUE COMPETENCE IN THE DEVELOPMENT OF DROSOPHILA , 1943 .

[112]  E. Hadorn,et al.  The Structure of the Ring-Gland (Corpus Allatum) in Normal and Lethal Larvae of Drosophila Melanogaster. , 1938, Proceedings of the National Academy of Sciences of the United States of America.

[113]  E. Hadorn An Accelerating Effect of Normal "Ring-Glands" on Puparium-Formation in Lethal Larvae of Drosophila Melanogaster. , 1937, Proceedings of the National Academy of Sciences of the United States of America.

[114]  V. Wigglesworth Memoirs: The Physiology of Ecdysis in Rhodnius Prolixus (Hemiptera). II. Factors controlling Moulting and ‘Metamorphosis’ , 1934 .

[115]  J. C. Li,et al.  Development in DROSOPHILA MELANOGASTER. , 1927, Genetics.