Insect seminal fluid proteins: identification and function.

Seminal fluid proteins (SFPs) produced in reproductive tract tissues of male insects and transferred to females during mating induce numerous physiological and behavioral postmating changes in females. These changes include decreasing receptivity to remating; affecting sperm storage parameters; increasing egg production; and modulating sperm competition, feeding behaviors, and mating plug formation. In addition, SFPs also have antimicrobial functions and induce expression of antimicrobial peptides in at least some insects. Here, we review recent identification of insect SFPs and discuss the multiple roles these proteins play in the postmating processes of female insects.

[1]  J. Ribeiro,et al.  Towards a Semen Proteome of the Dengue Vector Mosquito: Protein Identification and Potential Functions , 2011, PLoS neglected tropical diseases.

[2]  S. Larsson,et al.  Urticating hairs in arthropods: their nature and medical significance. , 2011, Annual review of entomology.

[3]  D. Six,et al.  The role of phytopathogenicity in bark beetle-fungus symbioses: a challenge to the classic paradigm. , 2011, Annual review of entomology.

[4]  R. Eisen,et al.  Using Geographic Information Systems and Decision Support Systems for the Prediction , Prevention , and Control of Vector-Borne Diseases , 2010 .

[5]  M. Vreysen,et al.  Salivary gland hypertrophy viruses: a novel group of insect pathogenic viruses. , 2011, Annual review of entomology.

[6]  T. Pitts‐Singer,et al.  The alfalfa leafcutting bee, Megachile rotundata: the world's most intensively managed solitary bee. , 2011, Annual review of entomology.

[7]  M. Wolfner,et al.  Sex Peptide Is Required for the Efficient Release of Stored Sperm in Mated Drosophila Females , 2010, Genetics.

[8]  J. Walters,et al.  Combined EST and proteomic analysis identifies rapidly evolving seminal fluid proteins in Heliconius butterflies. , 2010, Molecular biology and evolution.

[9]  C. Grozinger,et al.  The effects of mating and instrumental insemination on queen honey bee flight behaviour and gene expression , 2010, Insect molecular biology.

[10]  J. Boomsma,et al.  Seminal Fluid Mediates Ejaculate Competition in Social Insects , 2010, Science.

[11]  F. Tripet,et al.  Male accessory gland proteins induce female monogamy in anopheline mosquitoes , 2010, Medical and veterinary entomology.

[12]  T. Chapman,et al.  Female nutritional status determines the magnitude and sign of responses to a male ejaculate signal in Drosophila melanogaster , 2010, Journal of evolutionary biology.

[13]  W. Swanson,et al.  Proteomics enhances evolutionary and functional analysis of reproductive proteins , 2010, BioEssays : news and reviews in molecular, cellular and developmental biology.

[14]  T. Chapman,et al.  A mating plug protein reduces early female remating in Drosophila melanogaster. , 2010, Journal of insect physiology.

[15]  R. Isaac,et al.  Drosophila male sex peptide inhibits siesta sleep and promotes locomotor activity in the post-mated female , 2010, Proceedings of the Royal Society B: Biological Sciences.

[16]  K. Reinhardt,et al.  Ejaculate components delay reproductive senescence while elevating female reproductive rate in an insect , 2009, Proceedings of the National Academy of Sciences.

[17]  J. Sivinski,et al.  Male and female condition influence mating performance and sexual receptivity in two tropical fruit flies (Diptera: Tephritidae) with contrasting life histories. , 2009, Journal of insect physiology.

[18]  D. W. Rogers,et al.  Transglutaminase-Mediated Semen Coagulation Controls Sperm Storage in the Malaria Mosquito , 2009, PLoS biology.

[19]  S. Aron,et al.  Prudent sperm use by leaf-cutter ant queens , 2009, Proceedings of the Royal Society B: Biological Sciences.

[20]  J. Perry,et al.  The conditional economics of sexual conflict , 2009, Biology Letters.

[21]  B. Rogina The Effect of Sex Peptide and Calorie Intake on Fecundity in Female Drosophila melanogaster , 2009, TheScientificWorldJournal.

[22]  K. Friesen,et al.  Salivary gland degeneration and vitellogenesis in the ixodid tick Amblyomma hebraeum: Surpassing a critical weight is the prerequisite and detachment from the host is the trigger. , 2009, Journal of insect physiology.

[23]  R. Roe,et al.  Male engorgement factor: Role in stimulating engorgement to repletion in the ixodid tick, Dermacentor variabilis. , 2009, Journal of insect physiology.

[24]  M. Wolfner,et al.  Acp36DE is required for uterine conformational changes in mated Drosophila females , 2009, Proceedings of the National Academy of Sciences.

[25]  M. Wolfner,et al.  A network of interactions among seminal proteins underlies the long-term postmating response in Drosophila , 2009, Proceedings of the National Academy of Sciences.

[26]  I. Ladunga,et al.  Transcriptional profiling of the sperm storage organs of Drosophila melanogaster , 2009, Insect molecular biology.

[27]  Z. Chen,et al.  Juvenile hormone regulation of male accessory gland activity in the red flour beetle, Tribolium castaneum , 2009, Mechanisms of Development.

[28]  K. Reinhardt,et al.  Bacteriolytic Activity in the Ejaculate of an Insect , 2009, The American Naturalist.

[29]  A. Millar,et al.  Insights into female sperm storage from the spermathecal fluid proteome of the honeybee Apis mellifera , 2009, Genome Biology.

[30]  J. Boomsma,et al.  Honey bee males and queens use glandular secretions to enhance sperm viability before and after storage. , 2009, Journal of insect physiology.

[31]  T. Chapman,et al.  Seminal Fluid Protein Allocation and Male Reproductive Success , 2009, Current Biology.

[32]  T. Chapman,et al.  Plastic responses of male Drosophila melanogaster to the level of sperm competition increase male reproductive fitness , 2009, Proceedings of the Royal Society B: Biological Sciences.

[33]  M. MacCoss,et al.  Proteomic discovery of previously unannotated, rapidly evolving seminal fluid genes in Drosophila. , 2009, Genome research.

[34]  T. Markow,et al.  Proteomic analysis of Drosophila mojavensis male accessory glands suggests novel classes of seminal fluid proteins. , 2009, Insect biochemistry and molecular biology.

[35]  P. Innocenti,et al.  Immunogenic males: a genome‐wide analysis of reproduction and the cost of mating in Drosophila melanogaster females , 2009, Journal of evolutionary biology.

[36]  Nobuaki Takemori,et al.  Proteome mapping of the Drosophila melanogaster male reproductive system , 2009, Proteomics.

[37]  A. Millar,et al.  The seminal fluid proteome of the honeybee Apis mellifera , 2009, Proteomics.

[38]  Barry J. Dickson,et al.  Sensory Neurons in the Drosophila Genital Tract Regulate Female Reproductive Behavior , 2009, Neuron.

[39]  Sebastian Rumpf,et al.  Control of the Postmating Behavioral Switch in Drosophila Females by Internal Sensory Neurons , 2009, Neuron.

[40]  L. Holman Drosophila melanogaster seminal fluid can protect the sperm of other males , 2009 .

[41]  R. DeSalle,et al.  Orthology, Function and Evolution of Accessory Gland Proteins in the Drosophila repleta Group , 2009, Genetics.

[42]  M. Wolfner,et al.  Molecular social interactions: Drosophila melanogaster seminal fluid proteins as a case study. , 2009, Advances in genetics.

[43]  A. Lange Neural mechanisms coordinating the female reproductive system in the locust. , 2009, Frontiers in bioscience.

[44]  K. Reinhardt,et al.  Detection of seminal fluid proteins in the bed bug, Cimex lectularius, using two-dimensional gel electrophoresis and mass spectrometry , 2008, Parasitology.

[45]  E. Pondeville,et al.  Anopheles gambiae males produce and transfer the vitellogenic steroid hormone 20-hydroxyecdysone to females during mating , 2008, Proceedings of the National Academy of Sciences.

[46]  D. W. Rogers,et al.  Molecular and cellular components of the mating machinery in Anopheles gambiae females , 2008, Proceedings of the National Academy of Sciences.

[47]  J. Walters,et al.  EST analysis of male accessory glands from Heliconius butterflies with divergent mating systems , 2008, BMC Genomics.

[48]  P. Rivlin,et al.  Tissue remodeling: a mating-induced differentiation program for the Drosophila oviduct , 2008, BMC Developmental Biology.

[49]  Y. Kimura,et al.  Female mating receptivity after injection of male-derived extracts in Callosobruchus maculatus. , 2008, Journal of insect physiology.

[50]  Y. Takami,et al.  Dual function of seminal substances for mate guarding in a ground beetle , 2008 .

[51]  A. Wong,et al.  A Role for Acp29AB, a Predicted Seminal Fluid Lectin, in Female Sperm Storage in Drosophila melanogaster , 2008, Genetics.

[52]  K. Gunsalus,et al.  Mating induces an immune response and developmental switch in the Drosophila oviduct , 2008, Proceedings of the National Academy of Sciences.

[53]  R. Harrison,et al.  Searching for candidate speciation genes using a proteomic approach: seminal proteins in field crickets , 2008, Proceedings of the Royal Society B: Biological Sciences.

[54]  J. Perry,et al.  Ingested spermatophores accelerate reproduction and increase mating resistance but are not a source of sexual conflict , 2008, Animal Behaviour.

[55]  M. MacCoss,et al.  Proteomics Reveals Novel Drosophila Seminal Fluid Proteins Transferred at Mating , 2008, PLoS biology.

[56]  A. Clark,et al.  Post-mating Gene Expression Profiles of Female Drosophila melanogaster in Response to Time and to Four Male Accessory Gland Proteins , 2008, Genetics.

[57]  Noam Pilpel,et al.  Erratum to “Mating increases trypsin in female Drosophila hemolymph” [Insect Biochem. Mol. Biol. 38 (2008) 320–330] , 2008 .

[58]  Sarah D. Kocher,et al.  Genomic analysis of post-mating changes in the honey bee queen (Apis mellifera) , 2008, BMC Genomics.

[59]  J. Perry,et al.  Neither Mating Rate Nor Spermatophore Feeding Influences Longevity in a Ladybird Beetle , 2008 .

[60]  L. Partridge,et al.  Feeding, fecundity and lifespan in female Drosophila melanogaster , 2008, Proceedings of the Royal Society B: Biological Sciences.

[61]  J. Sivinski,et al.  Reproductive trade-offs from mating with a successful male: the case of the tephritid fly Anastrepha obliqua , 2008, Behavioral Ecology and Sociobiology.

[62]  Noam Pilpel,et al.  Mating-increases trypsin in female Drosophila hemolymph. , 2008, Insect biochemistry and molecular biology.

[63]  Tracey Chapman,et al.  Targeted Gene Deletion and Phenotypic Analysis of the Drosophila melanogaster Seminal Fluid Protease Inhibitor Acp62F , 2008, Genetics.

[64]  Y. Kimura,et al.  Female mating receptivity inhibited by injection of male-derived extracts in Callosobruchus chinensis. , 2008, Journal of insect physiology.

[65]  M. Wolfner,et al.  Identity and transfer of male reproductive gland proteins of the dengue vector mosquito, Aedes aegypti: potential tools for control of female feeding and reproduction. , 2008, Insect biochemistry and molecular biology.

[66]  Preethi Radhakrishnan,et al.  Ability of male Queensland fruit flies to inhibit receptivity in multiple mates, and the associated recovery of accessory glands. , 2008, Journal of insect physiology.

[67]  T. Chapman,et al.  The effect of mating on immunity can be masked by experimental piercing in female Drosophila melanogaster. , 2008, Journal of insect physiology.

[68]  B. Dickson,et al.  A receptor that mediates the post-mating switch in Drosophila reproductive behaviour , 2008, Nature.

[69]  A. Spradling,et al.  The Sf1-related nuclear hormone receptor Hr39 regulates Drosophila female reproductive tract development and function , 2007, Development.

[70]  J. Fuente,et al.  The impact of RNA interference of the subolesin and voraxin genes in male Amblyomma hebraeum (Acari: Ixodidae) on female engorgement and oviposition , 2008, Experimental and Applied Acarology.

[71]  M. Wolfner,et al.  Sustained Post-Mating Response in Drosophila melanogaster Requires Multiple Seminal Fluid Proteins , 2007, PLoS genetics.

[72]  E. Kubli,et al.  The hydroxyproline motif of male sex peptide elicits the innate immune response in Drosophila females , 2007, The FEBS journal.

[73]  D. W. Rogers,et al.  A genome-wide analysis in Anopheles gambiae mosquitoes reveals 46 male accessory gland genes, possible modulators of female behavior , 2007, Proceedings of the National Academy of Sciences.

[74]  David R. Tarpy,et al.  Effects of Insemination Quantity on Honey Bee Queen Physiology , 2007, PloS one.

[75]  D. Begun,et al.  Adaptive Evolution of Recently Duplicated Accessory Gland Protein Genes in Desert Drosophila , 2007, Genetics.

[76]  M. Wolfner,et al.  Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction. , 2007, Integrative and comparative biology.

[77]  J. Fuente,et al.  Tick Vaccines and the Transmission of Tick-Borne Pathogens , 2007, Veterinary Research Communications.

[78]  Preethi Radhakrishnan,et al.  Seminal fluids mediate sexual inhibition and short copula duration in mated female Queensland fruit flies. , 2007, Journal of insect physiology.

[79]  J. Dow,et al.  Using FlyAtlas to identify better Drosophila melanogaster models of human disease , 2007, Nature Genetics.

[80]  D. Promislow,et al.  Post-mating disparity between potential and realized immune response in Drosophila melanogaster , 2007, Proceedings of the Royal Society B: Biological Sciences.

[81]  M. Wolfner,et al.  Seminal proteins but not sperm induce morphological changes in the Drosophila melanogaster female reproductive tract during sperm storage. , 2007, Journal of insect physiology.

[82]  A. Shelton,et al.  The diversity of Bt resistance genes in species of Lepidoptera. , 2007, Journal of invertebrate pathology.

[83]  S. Applebaum,et al.  Female sex pheromone suppression and the fate of sex-peptide-like peptides in mated moths of Helicoverpa armigera. , 2007, Archives of insect biochemistry and physiology.

[84]  M. F. Potter,et al.  Insecticide Resistance in the Bed Bug: A Factor in the Pest’s Sudden Resurgence? , 2007, Journal of medical entomology.

[85]  M. Wolfner,et al.  An Ectopic Expression Screen Reveals the Protective and Toxic Effects of Drosophila Seminal Fluid Proteins , 2007, Genetics.

[86]  N. Lamango,et al.  Angiotensin-converting enzyme as a target for the development of novel insect growth regulators , 2007, Peptides.

[87]  M. Wolfner,et al.  Predicted seminal astacin-like protease is required for processing of reproductive proteins in Drosophila melanogaster , 2006, Proceedings of the National Academy of Sciences.

[88]  U. Friberg,et al.  Male perception of female mating status: its effect on copulation duration, sperm defence and female fitness , 2006, Animal Behaviour.

[89]  T. Chapman,et al.  Identification of genes expressed in the accessory glands of male Mediterranean Fruit Flies (Ceratitis capitata). , 2006, Insect biochemistry and molecular biology.

[90]  C. Fox,et al.  Ejaculate size, second male size, and moderate polyandry increase female fecundity in a seed beetle , 2006 .

[91]  W. Swanson,et al.  Identification and comparative analysis of accessory gland proteins in Orthoptera. , 2006, Genome.

[92]  M. Zurita,et al.  Oviduct contraction in Drosophila is modulated by a neural network that is both, octopaminergic and glutamatergic , 2006, Journal of cellular physiology.

[93]  W. Garrett,et al.  Proteomic analyses of male contributions to honey bee sperm storage and mating , 2006, Insect molecular biology.

[94]  G. Arnqvist,et al.  The costs of mating and egg production in Callosobruchus seed beetles , 2006, Animal Behaviour.

[95]  W. Swanson,et al.  Molecular evolution of seminal proteins in field crickets. , 2006, Molecular biology and evolution.

[96]  Y. Heifetz,et al.  Mating-responsive genes in reproductive tissues of female Drosophila melanogaster , 2006, Proceedings of the National Academy of Sciences.

[97]  C. Elliott,et al.  Neuromuscular organization and aminergic modulation of contractions in the Drosophila ovary , 2006, BMC Biology.

[98]  Michael J. Walker,et al.  Proteomic identification of Drosophila melanogaster male accessory gland proteins, including a pro-cathepsin and a soluble γ-glutamyl transpeptidase , 2006, Proteome Science.

[99]  A. Poiani Complexity of seminal fluid: a review , 2006, Behavioral Ecology and Sociobiology.

[100]  David J. Anderson,et al.  Allocrine Modulation of Feeding Behavior by the Sex Peptide of Drosophila , 2006, Current Biology.

[101]  Aaron M. T. Harmer,et al.  Remating inhibition in female Queensland fruit flies: effects and correlates of sperm storage. , 2006, Journal of insect physiology.

[102]  Alisha K Holloway,et al.  Recently Evolved Genes Identified From Drosophila yakuba and D. erecta Accessory Gland Expressed Sequence Tags , 2005, Genetics.

[103]  D. Begun,et al.  Molecular Population Genetics of Accessory Gland Protein Genes and Testis-Expressed Genes in Drosophila mojavensis and D. arizonae , 2005, Genetics.

[104]  D. Begun,et al.  Rapid evolution of genomic Acp complement in the melanogaster subgroup of Drosophila. , 2005, Molecular biology and evolution.

[105]  E. Kubli,et al.  Drosophila Sex-Peptide Stimulates Female Innate Immune System after Mating via the Toll and Imd Pathways , 2005, Current Biology.

[106]  M. Wolfner,et al.  Fates and targets of male accessory gland proteins in mated female Drosophila melanogaster. , 2005, Insect biochemistry and molecular biology.

[107]  A. Clark,et al.  Cross-Species Comparison of Drosophila Male Accessory Gland Protein Genes , 2005, Genetics.

[108]  G. Gäde,et al.  Neuropeptides regulating development and reproduction in insects , 2005 .

[109]  T. Chapman,et al.  Sex Peptide Causes Mating Costs in Female Drosophila melanogaster , 2005, Current Biology.

[110]  T. Honegger,et al.  Gradual Release of Sperm Bound Sex-Peptide Controls Female Postmating Behavior in Drosophila , 2005, Current Biology.

[111]  Laura N. Vandenberg,et al.  Two cleavage products of the Drosophila accessory gland protein ovulin can independently induce ovulation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[112]  M. Molento,et al.  Tick control: an industry point of view , 2004, Parasitology.

[113]  K. Hartfelder,et al.  The initial stages of oogenesis and their relation to differential fertility in the honey bee (Apis mellifera) castes. , 2004, Arthropod structure & development.

[114]  D. Begun,et al.  A genome-wide analysis of courting and mating responses in Drosophila melanogaster females. , 2004, Genome.

[115]  M. Wolfner,et al.  Comparative structural modeling and inference of conserved protein classes in Drosophila seminal fluid. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[116]  A. Clark,et al.  Genes Regulated by Mating, Sperm, or Seminal Proteins in Mated Female Drosophila melanogaster , 2004, Current Biology.

[117]  M. Wolfner,et al.  Mating, seminal fluid components, and sperm cause changes in vesicle release in the Drosophila female reproductive tract. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[118]  B. Weiss,et al.  Two feeding-induced proteins from the male gonad trigger engorgement of the female tick Amblyomma hebraeum. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[119]  Y. Choffat,et al.  The presence of Drosophila melanogaster sex peptide-like immunoreactivity in the accessory glands of male Helicoverpa armigera. , 2004, Journal of insect physiology.

[120]  M. Monastirioti Distinct octopamine cell population residing in the CNS abdominal ganglion controls ovulation in Drosophila melanogaster. , 2003, Developmental biology.

[121]  Ronald L. Davis,et al.  Octopamine receptor OAMB is required for ovulation in Drosophila melanogaster. , 2003, Developmental biology.

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

[123]  Y. Choffat,et al.  The sex-peptide DUP99B is expressed in the male ejaculatory duct and in the cardia of both sexes. , 2003, European journal of biochemistry.

[124]  M. Wolfner,et al.  An early role for the Drosophila melanogaster male seminal protein Acp36DE in female sperm storage , 2003, Journal of Experimental Biology.

[125]  E. Kubli,et al.  Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[126]  L. Partridge,et al.  The sex peptide of Drosophila melanogaster: Female post-mating responses analyzed by using RNA interference , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[127]  B. Yuval,et al.  Regulation of sexual receptivity of female Mediterranean fruit flies: old hypotheses revisited and a new synthesis proposed. , 2003, Journal of insect physiology.

[128]  T. Pizzari,et al.  PERSPECTIVE: SEXUAL CONFLICT AND SEXUAL SELECTION: CHASING AWAY PARADIGM SHIFTS , 2003, Evolution; international journal of organic evolution.

[129]  Y. Choffat,et al.  Inhibition of pheromone biosynthesis in Helicoverpa armigera by pheromonostatic peptides. , 2003, Journal of insect physiology.

[130]  M. Wolfner,et al.  The developments between gametogenesis and fertilization: ovulation and female sperm storage in Drosophila melanogaster. , 2003, Developmental biology.

[131]  R. Isaac,et al.  ACE inhibitors reduce fecundity in the mosquito, Anopheles stephensi. , 2003, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[132]  G. Parker,et al.  Sperm competition, male prudence and sperm-limited females , 2002 .

[133]  B. Weiss,et al.  Identification and characterization of genes differentially expressed in the testis/vas deferens of the fed male tick, Amblyomma hebraeum. , 2002, Insect biochemistry and molecular biology.

[134]  A. Rafaeli Neuroendocrine control of pheromone biosynthesis in moths. , 2002, International review of cytology.

[135]  M. Wolfner,et al.  The Drosophila melanogaster seminal fluid protein Acp62F is a protease inhibitor that is toxic upon ectopic expression. , 2002, Genetics.

[136]  A. Clark,et al.  Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[137]  M. Wolfner,et al.  Drosophila males transfer antibacterial proteins from their accessory gland and ejaculatory duct to their mates. , 2001, Journal of insect physiology.

[138]  William E. Wagner,et al.  FEMALES RECEIVE A LIFE‐SPAN BENEFIT FROM MALE EJACULATES IN A FIELD CRICKET , 2001, Evolution; international journal of organic evolution.

[139]  M. Wolfner,et al.  Identification and characterization of the major Drosophila melanogaster mating plug protein. , 2001, Insect biochemistry and molecular biology.

[140]  Z. Jin,et al.  Male accessory gland derived factors can stimulate oogenesis and enhance oviposition in Helicoverpa armigera (Lepidoptera: Noctuidae). , 2001, Archives of insect biochemistry and physiology.

[141]  P. Schmid-Hempel,et al.  A nonspecific fatty acid within the bumblebee mating plug prevents females from remating , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[142]  L. L. Wolf,et al.  Function of the mating plug in Drosophila hibisci Bock , 2001, Behavioral Ecology and Sociobiology.

[143]  D. Tarpy,et al.  The curious promiscuity of queen honeybees (Apis mellifera): Evolutionary and behavioral mechanisms , 2001 .

[144]  Y. Choffat,et al.  Common functional elements of Drosophila melanogaster seminal peptides involved in reproduction of Drosophila melanogaster and Helicoverpa armigera females. , 2000, Insect biochemistry and molecular biology.

[145]  L. Partridge,et al.  The role of male accessory gland protein Acp36DE in sperm competition in Drosophila melanogaster , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[146]  M. Noll,et al.  Drosophila female sexual behavior induced by sterile males showing copulation complementation. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[147]  M. Wolfner,et al.  The Drosophila seminal fluid protein Acp26Aa stimulates release of oocytes by the ovary , 2000, Current Biology.

[148]  M. Wolfner,et al.  Drosophila seminal fluid proteins enter the circulatory system of the mated female fly by crossing the posterior vaginal wall. , 1999, Insect biochemistry and molecular biology.

[149]  L. Partridge,et al.  Mating-induced inhibition of remating in female Mediterranean fruit flies Ceratitis capitata. , 1999, Journal of insect physiology.

[150]  M. Wolfner,et al.  Mated Drosophila melanogaster females require a seminal fluid protein, Acp36DE, to store sperm efficiently. , 1999, Genetics.

[151]  M. Klowden The check is in the male: male mosquitoes affect female physiology and behavior. , 1999, Journal of the American Mosquito Control Association.

[152]  Y. Fan,et al.  Drosophila melanogaster sex peptide stimulates juvenile hormone synthesis and depresses sex pheromone production in Helicoverpa armigera. , 1999, Journal of insect physiology.

[153]  J. Barker,et al.  A mating plug and male mate choice inDrosophila hibisciBock , 1998, Animal Behaviour.

[154]  W. Eberhard Female control : sexual selection by cryptic female choice , 1996 .

[155]  L. Lomas,et al.  “Male factors” in ticks: their role in feeding and egg development , 1996 .

[156]  Juan D. López,et al.  Ovipositional Behavior of Newly Colonized Corn Earworm (Lepidoptera: Noctiiidae) Females and Evidence for an Oviposition Stimulating Factor of Male Origin , 1996 .

[157]  E. Jang Effects of mating and accessory gland injections on olfactory-mediated behavior in the female mediterranean fruit fly, Ceratitis capitata , 1995 .

[158]  L. Partridge,et al.  Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products , 1995, Nature.

[159]  T. Kingan,et al.  Mating‐induced loss of sex pheromone and sexual receptivity in insects with emphasis on Helicoverpa zea and Lymantria dispar , 1994 .

[160]  T. Kingan,et al.  MALE ACCESSORY GLAND FACTORS ELICIT CHANGE FROM 'VIRGIN' TO 'MATED' BEHAVIOUR IN THE FEMALE CORN EARWORM MOTH HELICOVERPA ZEA , 1993 .

[161]  A. Møller,et al.  Female control of paternity. , 1993, Trends in ecology & evolution.

[162]  L. Lomas,et al.  The influence of a factor from the male genital tract on salivary gland degeneration in the female ixodid tick, Amblyomma hebraeum , 1992 .

[163]  R. Wagner,et al.  Some pharmacological properties of the oviduct muscularis of the stable fly Stomoxys calcitrans. , 1992, Comparative biochemistry and physiology. C, Comparative pharmacology and toxicology.

[164]  R. Rutowski,et al.  The function of the sphragis in cressida cressida (Fab.) (lepidoptera, papilionidae): A visual deterrent to copulation attempts , 1991 .

[165]  M. Wolfner,et al.  Synthesis of two Drosophila male accessory gland proteins and their fate after transfer to the female during mating. , 1990, Developmental biology.

[166]  M. Mogi,et al.  Biology of mosquitoes. , 1987 .

[167]  I. Orchard,et al.  Evidence for octopaminergic modulation of an insect visceral muscle. , 1985, Journal of neurobiology.

[168]  T. Markow,et al.  Drosophila Males Contribute to Oogenesis in a Multiple Mating Species , 1984, Science.

[169]  R. Harris,et al.  NEURAL INVOLVEMENT IN THE CONTROL OF SALIVARY GLAND DEGENERATION IN THE IXODID TICK AMBLYOMMA HEBRAEUM , 1984 .

[170]  P. S. Chen THE FUNCTIONAL MORPHOLOGY AND BIOCHEMISTRY OF INSECT MALE ACCESSORY GLANDS AND THEIR SECRETIONS , 1984 .

[171]  S. Tobe,et al.  Prostaglandins: Their role in egg-laying of the cricket Teleogryllus commodus. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[172]  F. Hirata Effects of the Male Accessory Gland Secretion on Oviposition and Remating in Females of Drosophila melanogaster , 1981 .

[173]  A. Thomas Nervous control of egg progression into the common oviduct and genital chamber of the stick-insect Carausius morosus , 1979 .

[174]  R. Leopold The Role of Male Accessory Glands in Insect Reproduction , 1976 .

[175]  J. Bryan Biological sciences: Further Studies on Consecutive Matings in the Anopheles gambiae Complex , 1972, Nature.

[176]  Y. Balashov Bloodsucking ticks (Ixodoidea)-vectors of disease in man and animals. , 1972 .

[177]  G. Parker,et al.  SPERM COMPETITION AND ITS EVOLUTIONARY CONSEQUENCES IN THE INSECTS , 1970 .

[178]  J. Bryan,et al.  Results of Consecutive Matings of Female Anopheles gambiae Species B with Fertile and Sterile Males , 1968, Nature.

[179]  J. Patterson A New Type of Isolating Mechanism in Drosophila. , 1946, Proceedings of the National Academy of Sciences of the United States of America.