Insulin signaling and the regulation of insect diapause

A rich chapter in the history of insect endocrinology has focused on hormonal control of diapause, especially the major roles played by juvenile hormones (JHs), ecdysteroids, and the neuropeptides that govern JH and ecdysteroid synthesis. More recently, experiments with adult diapause in Drosophila melanogaster and the mosquito Culex pipiens, and pupal diapause in the flesh fly Sarcophaga crassipalpis provide strong evidence that insulin signaling is also an important component of the regulatory pathway leading to the diapause phenotype. Insects produce many different insulin-like peptides (ILPs), and not all are involved in the diapause response; ILP-1 appears to be the one most closely linked to diapause in C. pipiens. Many steps in the pathway leading from perception of daylength (the primary environmental cue used to program diapause) to generation of the diapause phenotype remain unknown, but the role for insulin signaling in mosquito diapause appears to be upstream of JH, as evidenced by the fact that application of exogenous JH can rescue the effects of knocking down expression of ILP-1 or the Insulin Receptor. Fat accumulation, enhancement of stress tolerance, and other features of the diapause phenotype are likely linked to the insulin pathway through the action of a key transcription factor, FOXO. This review highlights many parallels for the role of insulin signaling as a regulator in insect diapause and dauer formation in the nematode Caenorhabditis elegans.

[1]  D. Denlinger,et al.  Evolutionary links between circadian clocks and photoperiodic diapause in insects. , 2013, Integrative and comparative biology.

[2]  C. Sim,et al.  Juvenile hormone III suppresses forkhead of transcription factor in the fat body and reduces fat accumulation in the diapausing mosquito, Culex pipiens , 2013, Insect molecular biology.

[3]  D. Saunders Insect photoperiodism: seeing the light , 2012 .

[4]  D. Denlinger,et al.  Cross-talk between the fat body and brain regulates insect developmental arrest , 2012, Proceedings of the National Academy of Sciences.

[5]  D. Nässel,et al.  Identified peptidergic neurons in the Drosophila brain regulate insulin-producing cells, stress responses and metabolism by coexpressed short neuropeptide F and corazonin , 2012, Cellular and Molecular Life Sciences.

[6]  Monica F. Poelchau,et al.  Transcript profiling reveals mechanisms for lipid conservation during diapause in the mosquito, Aedes albopictus. , 2012, Journal of insect physiology.

[7]  K. Hughes,et al.  Age-Specific Variation in Immune Response in Drosophila melanogaster Has a Genetic Basis , 2012, Genetics.

[8]  M. Carlsson,et al.  Insulin-Producing Cells in the Drosophila Brain also Express Satiety-Inducing Cholecystokinin-Like Peptide, Drosulfakinin , 2012, Front. Endocrin..

[9]  X. Vafopoulou,et al.  Rhythmic release of prothoracicotropic hormone from the brain of an adult insect during egg development. , 2012, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[10]  Mark R. Brown,et al.  Insulin-Like Peptides: Structure, Signaling, and Function , 2012 .

[11]  D. Denlinger,et al.  10 – Hormonal Control of Diapause , 2012 .

[12]  Monica F. Poelchau,et al.  A de novo transcriptome of the Asian tiger mosquito, Aedes albopictus, to identify candidate transcripts for diapause preparation , 2011, BMC Genomics.

[13]  J. Feder,et al.  Developmental trajectories of gene expression reveal candidates for diapause termination: a key life-history transition in the apple maggot fly Rhagoletis pomonella , 2011, Journal of Experimental Biology.

[14]  I. Hope,et al.  DAF-16 and Δ9 Desaturase Genes Promote Cold Tolerance in Long-Lived Caenorhabditis elegans age-1 Mutants , 2011, PloS one.

[15]  C. Sim,et al.  Catalase and superoxide dismutase-2 enhance survival and protect ovaries during overwintering diapause in the mosquito Culex pipiens. , 2011, Journal of insect physiology.

[16]  D. Denlinger,et al.  Dormancy and developmental arrest in invertebrates. , 2011, Journal of insect physiology.

[17]  V. Košťál Insect photoperiodic calendar and circadian clock: independence, cooperation, or unity? , 2011, Journal of insect physiology.

[18]  M. Toner,et al.  Metabolic restructuring during energy-limited states: insights from Artemia franciscana embryos and other animals. , 2011, Journal of insect physiology.

[19]  Yun Zhang,et al.  Specific insulin-like peptides encode sensory information to regulate distinct developmental processes , 2011, Development.

[20]  E. Siegel,et al.  Modulation of lipid biosynthesis contributes to stress resistance and longevity of C. elegans mutants , 2011, Aging.

[21]  L. Schoofs,et al.  Signalling through pigment dispersing hormone-like peptides in invertebrates , 2011, Progress in Neurobiology.

[22]  A. Gould,et al.  Fat cells reactivate quiescent neuroblasts via TOR and glial Insulin relays in Drosophila , 2011, Nature.

[23]  L. Vesala,et al.  Effects of photoperiodically induced reproductive diapause and cold hardening on the cold tolerance of Drosophila montana. , 2011, Journal of insect physiology.

[24]  A. Brand,et al.  Nutrition-Responsive Glia Control Exit of Neural Stem Cells from Quiescence , 2010, Cell.

[25]  N. Perrimon,et al.  FOXO/4E-BP Signaling in Drosophila Muscles Regulates Organism-wide Proteostasis during Aging , 2010, Cell.

[26]  S. Goto,et al.  Photoperiodic diapause under the control of circadian clock genes in an insect , 2010, BMC Biology.

[27]  D. Denlinger,et al.  Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly , 2010, Proceedings of the National Academy of Sciences.

[28]  A. Sehgal,et al.  AKT and TOR Signaling Set the Pace of the Circadian Pacemaker , 2010, Current Biology.

[29]  S. Luckhart,et al.  Activation of Akt Signaling Reduces the Prevalence and Intensity of Malaria Parasite Infection and Lifespan in Anopheles stephensi Mosquitoes , 2010, PLoS pathogens.

[30]  S. Moharramipour,et al.  Cold Hardiness and Supercooling Capacity in the Overwintering Larvae of the Codling Moth, Cydia pomonella , 2010, Journal of insect science.

[31]  T. MacRae Gene expression, metabolic regulation and stress tolerance during diapause , 2010, Cellular and Molecular Life Sciences.

[32]  T. Andrews,et al.  Molecular Evolution and Functional Characterization of Drosophila Insulin-Like Peptides , 2010, PLoS genetics.

[33]  Richard E. Lee,et al.  Low Temperature Biology of Insects: Index , 2010 .

[34]  W. Bradshaw,et al.  Light, time, and the physiology of biotic response to rapid climate change in animals. , 2010, Annual review of physiology.

[35]  P. Schmidt,et al.  Photoperiodism in Insects: Molecular Basis and Consequences of Diapause , 2009 .

[36]  S. Goto,et al.  Photoperiodism in Insects: Perception of Light and the Role of Clock Genes , 2009 .

[37]  H. Numata,et al.  Photoperiodism in Mollusks , 2009 .

[38]  D. Saunders Photoperiodism in Insects: Migration and Diapause Responses , 2009 .

[39]  M. Birnbaum,et al.  The immune response attenuates growth and nutrient storage in Drosophila by reducing insulin signaling , 2009, Proceedings of the National Academy of Sciences.

[40]  L. Pick,et al.  Deletion of Drosophila insulin-like peptides causes growth defects and metabolic abnormalities , 2009, Proceedings of the National Academy of Sciences.

[41]  C. Sim,et al.  Transcription profiling and regulation of fat metabolism genes in diapausing adults of the mosquito Culex pipiens. , 2009, Physiological genomics.

[42]  M. Birnbaum,et al.  Regulation of Fat Cell Mass by Insulin in Drosophila melanogaster , 2009, Molecular and Cellular Biology.

[43]  C. Sim,et al.  A shut‐down in expression of an insulin‐like peptide, ILP‐1, halts ovarian maturation during the overwintering diapause of the mosquito Culex pipiens , 2009, Insect molecular biology.

[44]  Kevin J. Emerson,et al.  Complications of complexity: integrating environmental, genetic and hormonal control of insect diapause. , 2009, Trends in genetics : TIG.

[45]  E. Hafen,et al.  Reduction of DILP2 in Drosophila Triages a Metabolic Phenotype from Lifespan Revealing Redundancy and Compensation among DILPs , 2008, PloS one.

[46]  C. Sherlock,et al.  Hormonal regulation of the humoral innate immune response in Drosophila melanogaster , 2008, Journal of Experimental Biology.

[47]  S. Goto,et al.  Peripheral circadian clock for the cuticle deposition rhythm in Drosophila melanogaster , 2008, Proceedings of the National Academy of Sciences.

[48]  H. Numata,et al.  Neurons important for the photoperiodic control of diapause in the bean bug, Riptortus pedestris , 2008, Journal of Comparative Physiology A.

[49]  C. Sim,et al.  Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens , 2008, Proceedings of the National Academy of Sciences.

[50]  R. Lehmann,et al.  Drosophila germ-line modulation of insulin signaling and lifespan , 2008, Proceedings of the National Academy of Sciences.

[51]  M. Tatar,et al.  Drosophila short neuropeptide F signalling regulates growth by ERK-mediated insulin signalling , 2008, Nature Cell Biology.

[52]  H. Hsu,et al.  Diet controls normal and tumorous germline stem cells via insulin-dependent and -independent mechanisms in Drosophila. , 2008, Developmental biology.

[53]  M. Allen What Makes a Fly Enter Diapause? , 2007, Fly.

[54]  D. Denlinger,et al.  Meeting the energetic demands of insect diapause: nutrient storage and utilization. , 2007, Journal of insect physiology.

[55]  X. Vafopoulou,et al.  Neuroanatomical relations of prothoracicotropic hormone neurons with the circadian timekeeping system in the brain of larval and adult Rhodnius prolixus (Hemiptera) , 2007, The Journal of comparative neurology.

[56]  T. Kawecki,et al.  JUVENILE HORMONE AS A REGULATOR OF THE TRADE-OFF BETWEEN REPRODUCTION AND LIFE SPAN IN DROSOPHILA MELANOGASTER , 2007, Evolution; international journal of organic evolution.

[57]  D. Denlinger,et al.  Shifts in the carbohydrate, polyol, and amino acid pools during rapid cold-hardening and diapause-associated cold-hardening in flesh flies (Sarcophaga crassipalpis): a metabolomic comparison , 2007, Journal of Comparative Physiology B.

[58]  J. Watts,et al.  Fatty Acid Desaturation and the Regulation of Adiposity in Caenorhabditis elegans , 2007, Genetics.

[59]  L. Partridge,et al.  Role of insulin-like signalling in Drosophila lifespan. , 2007, Trends in biochemical sciences.

[60]  S. Hayward,et al.  An explicit test of the phospholipid saturation hypothesis of acquired cold tolerance in Caenorhabditis elegans , 2007, Proceedings of the National Academy of Sciences.

[61]  Robert M Peitzsch,et al.  High-resolution dynamics of the transcriptional response to nutrition in Drosophila: a key role for dFOXO. , 2007, Physiological genomics.

[62]  Jean-René Martin,et al.  Hmgcr in the Corpus Allatum Controls Sexual Dimorphism of Locomotor Activity and Body Size via the Insulin Pathway in Drosophila , 2007, PloS one.

[63]  S. Luckhart,et al.  The insulin signaling cascade from nematodes to mammals: insights into innate immunity of Anopheles mosquitoes to malaria parasite infection. , 2007, Developmental and comparative immunology.

[64]  M. Suster,et al.  Natural variation in Drosophila melanogaster diapause due to the insulin-regulated PI3-kinase , 2006, Proceedings of the National Academy of Sciences.

[65]  D. Denlinger,et al.  Oleic acid is elevated in cell membranes during rapid cold-hardening and pupal diapause in the flesh fly, Sarcophaga crassipalpis. , 2006, Journal of insect physiology.

[66]  S. Bray Notch signalling: a simple pathway becomes complex , 2006, Nature Reviews Molecular Cell Biology.

[67]  David Gems,et al.  Diapause-associated metabolic traits reiterated in long-lived daf-2 mutants in the nematode Caenorhabditis elegans , 2006, Mechanisms of Ageing and Development.

[68]  C. Kahn,et al.  Critical nodes in signalling pathways: insights into insulin action , 2006, Nature Reviews Molecular Cell Biology.

[69]  Michael R. Green,et al.  Identification of direct DAF-16 targets controlling longevity, metabolism and diapause by chromatin immunoprecipitation , 2006, Nature Genetics.

[70]  Jean-René Martin,et al.  Disruption of insulin pathways alters trehalose level and abolishes sexual dimorphism in locomotor activity in Drosophila. , 2006, Journal of neurobiology.

[71]  Brian A. Hemmings,et al.  Protein kinase B/Akt at a glance , 2005, Journal of Cell Science.

[72]  D. Denlinger,et al.  Diapause in the mosquito Culex pipiens evokes a metabolic switch from blood feeding to sugar gluttony. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[73]  M. Tatar,et al.  Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[74]  L. Partridge,et al.  Dietary restriction in Drosophila , 2005, Mechanisms of Ageing and Development.

[75]  D. Drummond-Barbosa,et al.  Direct Control of Germline Stem Cell Division and Cyst Growth by Neural Insulin in Drosophila , 2005, Science.

[76]  L. Matzkin,et al.  GEOGRAPHIC VARIATION IN DIAPAUSE INCIDENCE, LIFE‐HISTORY TRAITS, AND CLIMATIC ADAPTATION IN DROSOPHILA MELANOGASTER , 2005, Evolution; international journal of organic evolution.

[77]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]/Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

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

[79]  G. Ruvkun,et al.  A systematic RNAi screen for longevity genes in C. elegans. , 2005, Genes & development.

[80]  E. Hafen,et al.  Susi, a negative regulator of Drosophila PI3-kinase. , 2005, Developmental cell.

[81]  H. Jasper,et al.  JNK Extends Life Span and Limits Growth by Antagonizing Cellular and Organism-Wide Responses to Insulin Signaling , 2005, Cell.

[82]  E. Hafen,et al.  Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[83]  J. Rogers,et al.  Coping with cold: An integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[84]  R. Nusse,et al.  The Wnt signaling pathway in development and disease. , 2004, Annual review of cell and developmental biology.

[85]  I. Gout,et al.  The TSC1-2 tumor suppressor controls insulin–PI3K signaling via regulation of IRS proteins , 2004, The Journal of cell biology.

[86]  E. Hafen,et al.  Long-Lived Drosophila with Overexpressed dFOXO in Adult Fat Body , 2004, Science.

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

[88]  C. Kahn,et al.  Suppressor of Cytokine Signaling 1 (SOCS-1) and SOCS-3 Cause Insulin Resistance through Inhibition of Tyrosine Phosphorylation of Insulin Receptor Substrate Proteins by Discrete Mechanisms , 2004, Molecular and Cellular Biology.

[89]  S. Benzer,et al.  Regulation of Lifespan in Drosophila by Modulation of Genes in the TOR Signaling Pathway , 2004, Current Biology.

[90]  B. Hemmings,et al.  Structure, regulation and function of PKB/AKT--a major therapeutic target. , 2004, Biochimica et biophysica acta.

[91]  J. Dupont,et al.  Biology of insulin-like growth factors in development. , 2003, Birth defects research. Part C, Embryo today : reviews.

[92]  M. Cohen,et al.  The hedgehog signaling network , 2003, American journal of medical genetics. Part A.

[93]  C. Kenyon,et al.  Tissue-Specific Activities of C. elegans DAF-16 in the Regulation of Lifespan , 2003, Cell.

[94]  R. Tjian,et al.  Control of cell number by Drosophila FOXO: downstream and feedback regulation of the insulin receptor pathway. , 2003, Genes & development.

[95]  E. Hafen,et al.  The Drosophila Forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling , 2003, Journal of biology.

[96]  Cori Bargmann,et al.  Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans , 2003, Nature.

[97]  J. Kramer,et al.  Expression of Drosophila FOXO regulates growth and can phenocopy starvation , 2003, BMC Developmental Biology.

[98]  Gary Ruvkun,et al.  Long-Lived C. elegans daf-2 Mutants Are Resistant to Bacterial Pathogens , 2003, Science.

[99]  Marc Montminy,et al.  TRB3: A tribbles Homolog That Inhibits Akt/PKB Activation by Insulin in Liver , 2003, Science.

[100]  Y. Le Marchand-Brustel,et al.  Reduced activation of phosphatidylinositol-3 kinase and increased serine 636 phosphorylation of insulin receptor substrate-1 in primary culture of skeletal muscle cells from patients with type 2 diabetes. , 2003, Diabetes.

[101]  John M Asara,et al.  Insulin-stimulated Phosphorylation of a Rab GTPase-activating Protein Regulates GLUT4 Translocation* , 2003, The Journal of Biological Chemistry.

[102]  Stuart K. Kim,et al.  Global analysis of dauer gene expression in Caenorhabditis elegans , 2003, Development.

[103]  G. Lithgow,et al.  Lifespan extension in C. elegans by a molecular chaperone dependent upon insulin‐like signals , 2003, Aging cell.

[104]  D. Denlinger,et al.  Regulation of diapause. , 2003, Annual review of entomology.

[105]  Cynthia Kenyon,et al.  Timing Requirements for Insulin/IGF-1 Signaling in C. elegans , 2002, Science.

[106]  Geert J. P. L. Kops,et al.  Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress , 2002, Nature.

[107]  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.

[108]  J. Tower,et al.  Induced overexpression of mitochondrial Mn-superoxide dismutase extends the life span of adult Drosophila melanogaster. , 2002, Genetics.

[109]  R. Nusse,et al.  Ablation of Insulin-Producing Neurons in Flies: Growth and Diabetic Phenotypes , 2002, Science.

[110]  E. Lam,et al.  Control of Cell Cycle Exit and Entry by Protein Kinase B-Regulated Forkhead Transcription Factors , 2002, Molecular and Cellular Biology.

[111]  J. S. Britton,et al.  Drosophila's insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. , 2002, Developmental cell.

[112]  M. Tatar,et al.  Juvenile hormone regulation of longevity in the migratory monarch butterfly , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[113]  Adam Claridge‐Chang,et al.  Circadian Regulation of Gene Expression Systems in the Drosophila Head , 2001, Neuron.

[114]  M. Boxem,et al.  lin-35 Rb and cki-1 Cip/Kip cooperate in developmental regulation of G1 progression in C. elegans. , 2001, Development.

[115]  P. Cohen,et al.  A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation. , 2001, Molecular Cell.

[116]  Mark R. Brown,et al.  Localization of an insulin-like peptide in brains of two flies , 2001, Cell and Tissue Research.

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

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

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

[120]  S. Leevers Growth control: Invertebrate insulin surprises! , 2001, Current Biology.

[121]  G. Lithgow,et al.  Longevity and heavy metal resistance in daf‐2 and age‐1 long‐lived mutants of Caenorhabditis elegans , 2001, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

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

[123]  Michael J. McDonald,et al.  Wild-Type Circadian Rhythmicity Is Dependent on Closely Spaced E Boxes in the Drosophila timelessPromoter , 2001, Molecular and Cellular Biology.

[124]  H. Numata,et al.  The Role of Neurosecretory Neurons in the Pars Intercerebralis and Pars Lateralis in Reproductive Diapause of the Blowfly, Protophormia terraenovae , 2000, Naturwissenschaften.

[125]  D. Goberdhan,et al.  Drosophila tumor suppressor PTEN controls cell size and number by antagonizing the Chico/PI3-kinase signaling pathway. , 1999, Genes & development.

[126]  Y Honda,et al.  The daf‐2 gene network for longevity regulates oxidative stress resistance and Mn‐superoxide dismutase gene expression in Caenorhabditis elegans , 1999, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[127]  E. Hafen,et al.  Autonomous Control of Cell and Organ Size by CHICO, a Drosophila Homolog of Vertebrate IRS1–4 , 1999, Cell.

[128]  B. Kennedy,et al.  Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. , 1999, Science.

[129]  J. Apfeld,et al.  Cell Nonautonomy of C. elegans daf-2 Function in the Regulation of Diapause and Life Span , 1998, Cell.

[130]  R. DePinho,et al.  Suppression of cell transformation by the cyclin-dependent kinase inhibitor p57KIP2 requires binding to proliferating cell nuclear antigen. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[131]  D. Denlinger,et al.  G0/G1 cell cycle arrest in the brain of Sarcophaga crassipalpis during pupal diapause and the expression pattern of the cell cycle regulator, proliferating cell nuclear antigen. , 1998, Insect biochemistry and molecular biology.

[132]  Koutarou D. Kimura,et al.  daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. , 1997, Science.

[133]  L. Brower,et al.  USE OF LIPID RESERVES BY MONARCH BUTTERFLIES OVERWINTERING IN MEXICO: IMPLICATIONS FOR CONSERVATION , 1997 .

[134]  Simon Conway Morris,et al.  The shape of life, genes, development, and the evolution of animal form , 1996 .

[135]  U. Shankavaram,et al.  Activation of cJun NH2-terminal kinase/stress-activated protein kinase by insulin. , 1996, Biochemistry.

[136]  R. Garofalo,et al.  The Drosophila insulin receptor is required for normal growth. , 1996, Endocrinology.

[137]  J. Vanfleteren,et al.  The gerontogenes age‐1 and daf‐2 determine metabolic rate potential in aging Caenorhabditis elegans , 1995, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[138]  M. Frasch,et al.  The Drosophila insulin receptor homolog: a gene essential for embryonic development encodes two receptor isoforms with different signaling potential. , 1995, The EMBO journal.

[139]  G. Ruvkun,et al.  daf-2, daf-16 and daf-23: genetically interacting genes controlling Dauer formation in Caenorhabditis elegans. , 1994, Genetics.

[140]  D. Denlinger Relationship between Cold Hardiness and Diapause , 1991 .

[141]  W. J. Bell,et al.  Seasonal adaptations of insects. , 1987 .

[142]  D. Denlinger Dormancy in tropical insects. , 1986, Annual review of entomology.

[143]  A. D. Lees,et al.  The identification of an aphid juvenile hormone, and its titre in relation to photoperiod , 1985 .

[144]  D L Riddle,et al.  The Caenorhabditis elegans dauer larva: developmental effects of pheromone, food, and temperature. , 1984, Developmental biology.

[145]  D. Riddle,et al.  A pheromone influences larval development in the nematode Caenorhabditis elegans. , 1982, Science.

[146]  William S. Herman,et al.  STUDIES ON THE ADULT REPRODUCTIVE DIAPAUSE OF THE MONARCH BUTTERFLY, DANAUS PLEXIPPUS , 1981 .

[147]  P. J. Randle Fat Cells , 1972, Nature.