More than sperm and egg: male, female and environmental factors that influence reproduction of Aedes and Anopheles mosquitoes
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Reproduction is more than the union of the sperm and the egg, as the successful generation of progeny requires a series of interactions (behavioral, physical, and molecular) between males and females to ensure that a spermatozoon will ultimately fertilize an egg. Thus, reproduction is a complex process in which species- and sex-specific behavioral cues are required for the localization, recognition, and attraction of a sexual partner, and post-insemination interactions between male and female molecules mediate physiological and behavioral changes in females necessary for optimal reproductive output. In this review, we focus on the behavioral and physiological processes required for reproduction in Aedes and Anopheles vector mosquitoes. We highlight recent work that has elucidated the pre-mating behaviors of males and females that lead to a successful copulation, describe the post-mating behavioral and physiological changes observed in females, which primarily serve to facilitate the production of progeny, and discuss the role of sex-specific molecules in mediating the post-mating changes observed in mated Aedes and Anopheles females. Finally, we give an overview of how environmental factors (e.g., larval nutrition or the composition of the microbiome) can influence adult fertility.
ADERSLEY A.; CHAMPNEYS A.; HOMER M.; BODE N. W. F.; ROBERT D. 2017. Emergent acoustic order in arrays of mosquitoes. Curr. Biol. 27: R1208–R1210. https://doi.org/10.1016/j.cub.2017.09.055
ADERSLEY A.; CATOR L.J. 2019. Female resistance and harmonic convergence influence male mating success in Aedes aegypti. Sci. Rep. 9: 1–12. https://doi.org/10.1038/s41598-019-38599-3
ALFONSO-PARRA C.; AVILA F. W.; DEEWATTHANAWONG P.; SIROT L. K.; WOLFNER M. F.; HARRINGTON L. C. 2014. Synthesis, depletion and cell-type expression of a protein from the male accessory glands of the dengue vector mosquito Aedes aegypti. J. Insect Physiol. 70: 117–124. https://doi.org/10.1016/j.jinsphys.2014.07.004
ALFONSO-PARRA C.; AHMED-BRAIMAH Y. H.; DEGNER E. C.; AVILA F. W.; VILLARREAL S. M.; PLEISS J. A.; WOLFNER M. F.; HARRINGTON L. C. 2016. Mating-Induced Transcriptome Changes in the Reproductive Tract of Female Aedes aegypti. PLoS Negl. Trop. Dis. 10: e0004451. https://doi.org/10.1371/journal.pntd.0004451
ALIOTA M. T.; PEINADO S. A.; VELEZ I. D.; OSORIO J. E. 2016a. The wMel strain of Wolbachia Reduces Transmission of Zika virus by Aedes aegypti. Sci. Rep. 6: 1–7. https://doi.org/10.1038/srep28792
ALIOTA M. T.; WALKER E. C.; URIBE YEPES A.; VELEZ I. D.; CHRISTESSEN B. M.; OSORIO J. E. 2016b. The wMel Strain of Wolbachia Reduces Transmission of Chikungunya Virus in Aedes aegypti. PLoS Negl. Trop. Dis. 10: e0004677. https://doi.org/10.1371/journal.pntd.0004677
ALLEN A. K.; SPRADLING A. C. 2008. The Sf1-related nuclear hormone receptor Hr39 regulates Drosophila female reproductive tract development and function. Development 135: 311–321. https://doi.org/10.1242/dev.015156
AVILA F. W.; SIROT L. K.; LAFLAMME B. A.; RUBINSTEIN C. D.; WOLFNER M. F. 2011. Insect Seminal Fluid Proteins: Identification and Function. Annu. Rev. Entomol. 56: 21–40. https://doi.org/10.1146/annurev-ento-120709-144823
BALDINI F.; GABRIELI P.; SOUTH A.; VALIM C.; MANCINI F.; CATTERUCCIA F. 2013. The interaction between a sexually transferred steroid hormone and a female protein regulates oogenesis in the malaria mosquito Anopheles gambiae. PLoS Biol. 11: e1001695. https://doi.org/10.1371/journal.pbio.1001695
BASCUÑAN P.; GABRIELI P.; MAMELI E.; CATTERUCCIA F. 2020. Mating-regulated atrial proteases control reinsemination rates in Anopheles gambiae females. Sci. Rep. 10: 21974. https://doi.org/10.1038/s41598-020-78967-y
BASSENE H.; NIANG E. H. A.; FENOLLAR F.; DOUCOURE S.; FAYE O.; RAOULT D.; SOKHNA C.; MEDIANNIKOV O. 2020. Role of plants in the transmission of Asaia sp., which potentially inhibit the Plasmodium sporogenic cycle in Anopheles mosquitoes. Sci. Rep. 10: 7144. https://doi.org/10.1038/s41598-020-64163-5
BELTON P. 1994. Attraction of male mosquitos to sound. J. Am. Mosq. Control Assoc. 10: 297–301.
BIAN G.; XU Y.; LU P.; XIE Y.; XI Z. 2010. The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS Pathog. 6: e1000833. https://doi.org/10.1371/journal.ppat.1000833
BOES K. E.; RIBEIRO J. M. C.; WONG A.; HARRINGTON L.C.; WOLFNER M.F.; SIROT L.K. 2014. Identification and Characterization of Seminal Fluid Proteins in the Asian Tiger Mosquito, Aedes albopictus. PLoS Negl. Trop. Dis. 8: e2946. https://doi.org/10.1371/journal.pntd.0002946
BRIEGEL H.; TIMMERMANN S. E. 2001. Aedes albopictus (Diptera: Culicidae): physiological aspects of development and reproduction. J. Med. Entomol. 38: 566–571. https://doi.org/10.1603/0022-2585-38.4.566
CAMARGO C.; AHMED-BRAIMAH Y. H.; AMARO I. A.; HARRINGTON L. C.; WOLFNER M.F.; AVILA F. W. 2020. Mating and blood-feeding induce transcriptome changes in the spermathecae of the yellow fever mosquito Aedes aegypti. Sci. Rep. 10: 14899. https://doi.org/10.1038/s41598-020-71904-z
CARRINGTON L. B.; ARMIJOS M. V.; LAMBRECHTS L.; BARKER C. M.; SCOTT T. W. 2013. Effects of fluctuating daily temperatures at critical thermal extremes on Aedes aegypti life-history traits. PLoS One 8: e58824. https://doi.org/10.1371/journal.pone.0058824
CATOR L. J.; ARTHUR B. J.; HARRINGTON L. C.; HOY R. R. 2009. Harmonic convergence in the love songs of the dengue vector mosquito. Science. 323: 1077–1079. https://doi.org/10.1126/science.1166541
CATOR L. J.; ARTHUR B. J.; PONLAWAT A.; HARRINGTON L. C. 2011. Behavioral observations and sound recordings of free-flight mating swarms of Ae. Aegypti (Diptera: Culicidae) in Thailand. J. Med. Entomol. 48: 941–946. https://doi.org/10.1603/me11019
CATOR L. J.; WYER C. A. S.; HARRINGTON L. C. 2021. Mosquito Sexual Selection and Reproductive Control Programs. Trends Parasitol. 37: 330–339. https://doi.org/10.1016/j.pt.2020.11.009
CHAMBERS E. W.; HAPAIRAI L.; PEEL B. A.; BOSSIN H.; DOBSN S. L. 2011. Male mating competitiveness of a Wolbachia-introgressed Aedes polynesiensis strain under semi-field conditions. PLoS Negl. Trop. Dis. 5: e1271. https://doi.org/10.1371/journal.pntd.0001271
CHAPMAN T. 2008. The soup in my fly: evolution, form and function of seminal fluid proteins. PLoS Biol. 6: e179. https://doi.org/10.1371/journal.pbio.0060179
CLIFTON M. E.; CORREA S.; RIVERA-PEREZ C.; NOUZOVA M.; NORIEGO F. G. 2014. Male Aedes aegypti mosquitoes use JH III transferred during copulation to influence previtellogenic ovary physiology and affect the reproductive output of female mosquitoes. J. Insect Physiol. 64: 40–47. https://doi.org/10.1016/j.jinsphys.2014.03.006
COON K. L.; BROWN M. R.; STRAND M. R. 2016a. Gut bacteria differentially affect egg production in the anautogenous mosquito Aedes aegypti and facultatively autogenous mosquito Aedes atropalpus (Diptera: Culicidae). Parasit. Vectors 9: 375. https://doi.org/10.1186/s13071-016-1660-9
COON K. L.; BROWN M. R.; STRAND M. R. 2016b. Mosquitoes host communities of bacteria that are essential for development but vary greatly between local habitats. Mol. Ecol. 25: 5806–5826. https://doi.org/10.1111/mec.13877
COSTA E. A. P. A.; SANTOS E. M. M.; CORREIA J. C.; ALBUQUERQUE C. M. R. 2010. Impact of small variations in temperature and humidity on the reproductive activity and survival of Aedes aegypti (Diptera, Culicidae). Rev. Bras. Entomol. 54: 488–493.
CRAIG G. B. 1967. Mosquitoes: Female Monogamy Induced by Male Accessory Gland Substance. Science. 156: 1499–1501. https://doi.org/10.1126/science.156.3781.1499
DEGNER E. C.; HARRINGTON L. C. 2016a. A mosquito sperm’s journey from male ejaculate to egg: Mechanisms, molecules, and methods for exploration. Mol. Reprod. Dev. 83: 897–911. https://doi.org/10.1002/mrd.22653
DEGNER E. C.; HARRINGTON L. C. 2016b. Polyandry depends on postmating time interval in the dengue vector Aedes aegypti. Am. J. Trop. Med. Hyg. 94: 780–785. https://doi.org/10.4269/ajtmh.15-0893
DEGNER E. C.; AHMED-BRAIMAH Y. H.; BORZIAK K.; WOLFNER M. F.; HARRINGTON L. C.; DORUS S. 2018. Proteins, Transcripts, and Genetic Architecture of Seminal Fluid and Sperm in the Mosquito Aedes aegypti . Mol. Cell. Proteomics 18: S6–S22. https://doi.org/10.1074/mcp.ra118.001067
DELLATE H.; GIMONNEAU G.; TRIBOIRE A.; FONTENILLE D. 2009. Influence of temperature on immature development, survival, longevity, fecundity, and gonotrophic cycles of aedes albopictus, vector of chikungunya and dengue in the indian ocean. J. Med. Entomol. 46: 33–41. https://doi.org/10.1603/033.046.0105
DIABTÉ A.; YARO A. S.; DAO A.; DIALLO M.; HUESTIS D. L.; LEHMANN T. 2011. Spatial distribution and male mating success of Anopheles gambiae swarms. BMC Evol. Biol. 11: 184. https://doi.org/10.1186/1471-2148-11-184
DOTTORINI T.; NICOLAIDES L.; RANSON H.; ROGERS D. W.; CRISANTI A.; CATTERUCCIA F. 2007. A genome-wide analysis in Anopheles gambiae mosquitoes reveals 46 male accessory gland genes, possible modulators of female behavior. Proc. Natl. Acad. Sci. U. S. A. 104: 16215–16220. https://doi.org/10.1073/pnas.0703904104
DOTTORINI T.; PERSAMPIERI T.; PALLADINO P.; BAKER D. A.; SPACCAPELO R.; SENNIN N.; CRISANTI A. 2013. Regulation of Anopheles gambiae male accessory gland genes influences postmating response in female. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 27: 86–97. https://doi.org/10.1096/fj.12-219444
DUVALL L. B.; BASRUR N. S.; MOLINA H.; MCMENIMAN C. J.; VOSSHALL L. B. 2017. A Peptide Signaling System that Rapidly Enforces Paternity in the Aedes aegypti Mosquito. Curr. Biol. 27: 3734-3742.e5. https://doi.org/10.1016/j.cub.2017.10.074
EPOPA P. S.; MAIGA H.; HIEN D. F. S.; DABIRE R. K.; LEES R. S.; GILES J.; TRIPET F.; BALDET T.; DAMIENS D.; DIABATE A. 2018. Assessment of the developmental success of Anopheles coluzzii larvae under different nutrient regimes: effects of diet quality, food amount and larval density. Malar. J. 17: 377. https://doi.org/10.1186/s12936-018-2530-z
FEITOZA T. S.; FERREIRA-DE-LIMA V. H.; CAMARA D. C. P.; HONÓRIO N. A.; LOUNIBOS L. P.; LIMA-CAMARA T. N. 2020. Interspecific Mating Effects on Locomotor Activity Rhythms and Refractoriness of Aedes albopictus (Diptera: Culicidae) Females. Insects 11: 874. https://doi.org/10.3390/insects11120874
GABRIELI P.; KAKANI E. G.; MITCHELL S. N.; MAMELI E.; WANT E. J.; ANTON A. N.; SERRAO A.; BALDINI F.; CATTERUCCIA F. 2014. Sexual transfer of the steroid hormone 20E induces the postmating switch in Anopheles gambiae. Proc. Natl. Acad. Sci. 111: 16353–16358. https://doi.org/10.1073/pnas.1410488111
GAIO A. D. O.; GUSMAO D. S.; SANTOS A. V.; BERBERT-MOLINA M. A.; PIMENTA P. F. P.; LEMOS S. J. A. 2011. Contribution of midgut bacteria to blood digestion and egg production in aedes aegypti (diptera: Culicidae) (L.). Parasites and Vectors 4: 105. https://doi.org/10.1186/1756-3305-4-105
GENDRIN M.; RODEGRS F. H.; YERBANGA R. S.; OUEDRAOGO J. B.; BASÁÑEZ M. G.; COHUET A.; CHRISTOPHIDES G. K. 2015. Antibiotics in ingested human blood affect the mosquito microbiota and capacity to transmit malaria. Nat. Commun. 6: 5921. https://doi.org/10.1038/ncomms6921
GILLES J. R. L.; LEES R. S.; SOLIBAN S. M.; BENEDICT M. Q. 2011. Density-dependent effects in experimental larval populations of Anopheles arabiensis (Diptera: Culicidae) can be negative, neutral, or overcompensatory depending on density and diet levels. J. Med. Entomol. 48: 296–304. https://doi.org/10.1603/me09209
GIMONNEAU G.; TCHIOFFO M. T.; ABATE L.; BOISSIÈRE A.; AWONO-AMBÉNÉ P. H.; NSANGO S. E.; CHRISTEN R.; MORLAIS I. 2014. Composition of Anopheles coluzzii and Anopheles gambiae microbiota from larval to adult stages. Infect. Genet. Evol. J. Mol. Epidemiol. Evol. Genet. Infect. Dis. 28: 715–724. https://doi.org/10.1016/j.meegid.2014.09.029
HATALA A. J.; HARRINGTON L. C.; DEGNER E. C. 2018. Age and body size infuence sperm quantity in male Aedes albopictus (Diptera: Culicidae) mosquitoes. J. Med. Entomol. 55: 1051–1054. https://doi.org/10.1093/jme/tjy040
HELINSKI M. E. H.; HARRINGTON L. C. 2011. Male mating history and body size influence female fecundity and longevity of the dengue vector Aedes aegypti. J. Med. Entomol. 48: 202–11. https://doi.org/10.1603/ME10071
HELINSKI M. E. H., DEEWATTHANAWONG P.; SIROT L. K.; WOLFNER M. F.; HARRINGTON L. C. 2012. Duration and dose-dependency of female sexual receptivity responses to seminal fluid proteins in Aedes albopictus and Ae. aegypti mosquitoes. J. Insect Physiol. 58: 1307–1313. https://doi.org/10.1016/j.jinsphys.2012.07.003
HOFFMANN A. A.; MONTGOMERY B. L.; POPOVICI J.; ITURBE-ORMAETXE I.; JOHNSON P. H.; MUZZI F.; GREENFIELD M.; DURKAN M.; LEONG Y. S.; DONG Y.; COOK H.; AXFORD J.; CALLAHAN A. G.; KENNY N.; OMODEI C.; MCGRAW E. A.; RYAN P. A.; RITCHIE S. A. TURELLI M.; O'NEILL S. L. 2011. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476: 454–459. https://doi.org/10.1038/nature10356
HOPKINS B. R.; SEPIL I,; WIGBY S. 2017. Seminal Fluid. Curr Biol. 27: R404-R405. https://doi.org/10.1016/j.club.2017.03.063
HOPKINS B. R.; AVILA F. W.; WOLFNER M. F. 2018. Insect Male Reproductive Glands and Their Products, pp. 137–144 in Encyclopedia of Reproduction, Elsevier.
HOWELL P. I.; KNOLS B. G. J. 2009. Male mating biology. Malar. J. 8 Suppl 2: S8. https://doi.org/10.1186/1475-2875-8-S2-S8
ISHIMOTO H.; KITAMOTO T. 2011. Beyong molting--roles of the steroid molting hormone ecdysone in the regulation of memory and sleep in adult Drosophila. Fly. 5: 215-20. https://doi.org/10.4161/fly.5.3.15477
DE JESUS C. E.; REISKIND M. H. 2016. The importance of male body size on sperm uptake and usage, and female fecundity in Aedes aegypti and Aedes albopictus. Parasit. Vectors 9: 447. https://doi.org/10.1186/s13071-016-1734-8
JOHNSON B. J.; RITCHIE S. A. 2016. The Siren’s Song: Exploitation of Female Flight Tones to Passively Capture Male Aedes aegypti (Diptera: Culicidae). J. Med. Entomol. 53: 245–248. https://doi.org/10.1093/jme/tjv165
KAMBHAMPATI S.; RAI K. S.; BURGUN S. J. 1993. UNIDIRECTIONAL CYTOPLASMIC INCOMPATIBILITY IN THE MOSQUITO, AEDES ALBOPICTUS. Evolution 47: 673–677. https://doi.org/10.1111/j.1558-5646.1993.tb02121.x
KREMER N.; HUIGENS M. E. 2011. Vertical and horizontal transmission drive bacterial invasion. Mol. Ecol. 20: 3496–3498. https://doi.org/10.1111/j.1365-294X.2011.05194.x
LAU M. J.; ROSS P. A.; HOFFMANN A. A. 2021. Infertility and fecundity loss of Wolbachia-infected Aedes aegypti hatched from quiescent eggs is expected to alter invasion dynamics, (J. J. Gillespie, Ed.). PLoS Negl. Trop. Dis. 15: e0009179. https://doi.org/10.1371/journal.pntd.0009179
LEAGUE G. P.; BAXTER L. L.; WOLFNER M. F.; HARRINGTON L. C. 2019. M.ale accessory gland molecules inhibit harmonic convergence in the mosquito Aedes aegypti. Curr. Biol. 29: R196–R197.
LEAHY M. G.; CRAIG G. B. 1965. Male accessory gland as a stimulant for oviposition in Aedes aegypti and A. albopictus. Mosq. News 25: 448–452.
MARCENAC P.; SHAW W. R.; KAKANI E. G.; MITCHELL S. N.; SOUTH A.; WERLING K.; MARROGI E.; ABERNATHY D. G.; YERBANGA Y. S.; DABIRE R. K.; DIABATE A.; LEFEVRE T.; CATTERUCCIA F. 2020. A mating-induced reproductive gene promotes Anopheles tolerance to Plasmodium falciparum infection. PLoS Pathog. 16: e1008908. https://doi.org/10.1371/journal.ppat.1008908
MATTEI A. L.; RICCIO M. L.; AVILA F. W.; WOLFNER M. F. 2015. Integrated 3D view of postmating responses by the Drosophila melanogaster female reproductive tract, obtained by micro-computed tomography scanning . Proc. Natl. Acad. Sci. 112: 8475–8480. https://doi.org/10.1073/pnas.1505797112
MCMENIMAN C. J.; LANE R. V.; CASS B. N.; FONG A. W. C.; SIDHU M.; WONG Y. F.; O'NEILL S. L. 2009. Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 323: 141–144. https://doi.org/10.1126/science.1165326
MEUTI M.; SHORT S. 2019. Physiological and Environmental Factors Affecting the Composition of the Ejaculate in Mosquitoes and Other Insects. Insects 10: 74. https://doi.org/10.3390/insects10030074
MITCHELL S. N.; KAKANI E. G.; SOUTH A.; HOWELL P. I.; WATERHOUSE R. M.; CATTERUCCIA F. 2015. Mosquito biology. Evolution of sexual traits influencing vectorial capacity in anopheline mosquitoes. Science 347: 985–988. https://doi.org/10.1126/science.1259435
MONTOYA J. P.; PANTOJA-SÁNCHEZ H.; GOMEZ S.; AVILA F. W.; ALFONSO-PARRA C. 2021. Flight tone characterisation of the South American malaria vector Anopheles darlingi (Diptera: Culicidae). Mem. Inst. Oswaldo Cruz 116: e200497. https://doi.org/10.1590/0074-02760200497
NACCARATI C.; AUDSLEY N.; KEEN J. N.; KIM J. H.; HOWELL G. J.; KIM Y. J.; ISAAC R. E. 2012. The host-seeking inhibitory peptide, Aea-HP-1, is made in the male accessory gland and transferred to the female during copulation. Peptides 34: 150–157. https://doi.org/10.1016/j.peptides.2011.10.027
NOBLE J. M.; DEGNER E. C.; HARRINGTON L. C.; KOURKOUTIS L. F. 2019. Cryo-Electron Microscopy Reveals That Sperm Modification Coincides with Female Fertility in the Mosquito Aedes aegypti. Sci. Rep. 9: 18537. https://doi.org/10.1038/s41598-019-54920-6
OLIVA C. F.; DAMIENS D.; BENEDICT M. Q. 2014 .Male reproductive biology of Aedes mosquitoes. Acta Trop. 132 Suppl: S12-9. https://doi.org/10.1016/j.actatropica.2013.11.021
PANTOJA-SÁNCHEZ H.; GOMEZ S.; VELEZ V.; AVILA F. W.; ALFONSO-PARRA C. 2019. Precopulatory acoustic interactions of the New World malaria vector Anopheles albimanus (Diptera: Culicidae). Parasites and Vectors 12: 386. https://doi.org/10.1186/s13071-019-3648-8
PASCINI T. V.; RAMALHO-ORTIGAO M.; RIBEIRO J. M.; JACOBS-LORENA M.; MARTINS G. F. 2020. Transcriptional profiling and physiological roles of Aedes aegypti spermathecal-related genes. BMC Genomics 21: 143. https://doi.org/10.1186/s12864-020-6543-y
PEIRCE M. J.; MITCHELL S. N.; KAKANI E. G.; SCARPELLI P.; SOUTH A.; SHAW W. R.; WERLING K. L; GABRIELI P.; MARCENAC P.; BORDONI M.; TALESA V.; CATTERUCCIA F. 2020. JNK signaling regulates oviposition in the malaria vector Anopheles gambiae. Sci. Rep. 10: 14344. https://doi.org/10.1038/s41598-020-71291-5
PENNETIER C.; WARREN B.; DABIRE K. R.; RUSSELL I. J.; GIBSON G. 2010. “Singing on the wing” as a mechanism for species recognition in the malarial mosquito Anopheles gambiae. Curr. Biol. 20: 131–136. https://doi.org/10.1016/j.cub.2009.11.040
PONLAWAT A.; HARRINGTON L. C. 2007. Age and body size influence male sperm capacity of the dengue vector Aedes aegypti (Diptera: Culicidae). J. Med. Entomol. 44: 422–6.
PONLAWAT A.; HARRINGTON L. C. 2009. Factors associated with male mating success of the dengue vector mosquito, Aedes aegypti. Am. J. Trop. Med. Hyg. 80: 395–400. https://doi.org/10.4269/ajtmh.2009.80.395
PROKUPEK A. M.; KACHMAN S. D.; LADUNGA I.; HARSHMAN L. G. 2009. Transcriptional profiling of the sperm storage organs of Drosophila melanogaster. Insect Mol. Biol. 18: 465–475. https://doi.org/10.1111/j.1365-2583.2009.00887.x
QSIM M.; ASHFAQ U. A.; YOUSAF M. Z.; MASOUD M. S.; RASUL I.; NOOR N.; HUSSAIN A. 2017. Genetically Modified Aedes aegypti to Control Dengue: A Review. Crit. Rev. Eukaryot. Gene Expr. 27: 331–340. https://doi.org/10.1615/CritRevEukaryotGeneExpr.2017019937
RAMÍREZ-SÁNCHEZ L. F.; CAMARGO C.; AVILA F. W. 2020. Male sexual history influences female fertility and re-mating incidence in the mosquito vector Aedes aegypti (Diptera: Culicidae). J. Insect Physiol. 121: 104019. https://doi.org/10.1016/j.jinsphys.2020.104019
ROGERS D. W.; WHITTEN M. M. A.; THAILAYIL J.; SOICHOT J.; LEVASHINA E. A.; CATTERUCCIA F. 2008. Molecular and cellular components of the mating machinery in Anopheles gambiae females. Proc. Natl. Acad. Sci. 105: 19390–19395. https://doi.org/10.1073/pnas.0809723105
ROGERS D. W.; BALDINI F.; BATTAGLIA F.; PANICO M.; DELL A.; MORRIS H. R.; CATTERUCCIA F. 2009. Transglutaminase-mediated semen coagulation controls sperm storage in the malaria mosquito. PLoS Biol. 7: e1000272. https://doi.org/10.1371/journal.pbio.1000272
ROMOLI O.; SCHÖNBECK J. C.; HAPFELMEIER S.; GENDRIN M. 2021. Production of germ-free mosquitoes via transient colonisation allows stage-specific investigation of host-microbiota interactions. Nat. Commun. 12: 942. https://doi.org/10.1038/s41467-021-21195-3
ROSS P. A.; HOFFMANN A. A. 2021. Vector control: Discovery of Wolbachia in malaria vectors. Curr. Biol. 31: R738–R740. https://doi.org/10.1016/j.cub.2021.04.038
ROTH L. M. 1948. A Study of Mosquito Behavior. An Experimental Laboratory Study of the Sexual Behavior of Aedes aegypti (Linnaeus). Am. Midl. Nat. 40: 265. https://doi.org/10.2307/2421604
RUBINSTEIN C. D.; WOLFNER M. F. 2013. Drosophila seminal protein ovulin mediates ovulation through female octopamine neuronal signaling. Proc. Natl. Acad. Sci. 110: 17420–17425. https://doi.org/10.1073/pnas.1220018110
SCHNAKENBERG S. L.; MATIAS W. R.; SIEGAL M. L. 2011. Sperm-storage defects and live birth in drosophila females lacking spermathecal secretory cells. PLoS Biol. 9: e1001192. https://doi.org/10.1371/journal.pbio.1001192
SCHWENKE R. A.; LAZZARO B. P.; WOLFNER M. F. 2016. Reproduction-Immunity Trade-Offs in Insects. Annu. Rev. Entomol. 61: 239–256. https://doi.org/10.1146/annurev-ento-010715-023924
SEGOLI M.; HOFFMANN A. A.; LLOYD J.; OMODEI G. J.; RITCHIE S. A. 2014. The effect of virus-blocking Wolbachia on male competitiveness of the dengue vector mosquito, Aedes aegypti. PLoS Negl. Trop. Dis. 8: e3294. https://doi.org/10.1371/journal.pntd.0003294
SHAW W. R.; TEODORI E.; MITCHELL S. N.; BALDINI F.; GABRIELI P.; ROGERS D. W.; CATTERUCCIA F. 2014. Mating activates the heme peroxidase HPX15 in the sperm storage organ to ensure fertility in Anopheles gambiae. Proc. Natl. Acad. Sci. 111: 5854–5859. https://doi.org/10.1073/pnas.1401715111
SHISHIK A D.; MANOUKIS N. C.; BUTAIL S.; PALEY D. A. 2014. Male motion coordination in anopheline mating swarms. Sci. Rep. 4: 6318. https://doi.org/10.1038/srep06318
SIMÕES P.; INGHAM R.; GIBSON G.; RUSSELL I. 2016. A role for acoustic distortion in novel rapid frequency modulation behaviour in free-flying male mosquitoes. Exp. Biol. 219: 2039–2047.
SIMÕES P. M. V.; GIBSON G.; RUSSELL I. J. 2017 Pre-copula acoustic behaviour of males in the malarial mosquitoes Anopheles coluzzii and Anopheles gambiae s.s. does not contribute to reproductive isolation. J. Exp. Biol. 220: 379–385. https://doi.org/10.1242/jeb.149757
STRAND M. R. 2018. Composition and functional roles of the gut microbiota in mosquitoes. Curr. Opin. insect Sci. 28: 59–65. https://doi.org/10.1016/j.cois.2018.05.008
SUN J.; SPRADLING A. C. 2013. Ovulation in Drosophila is sontrolled by secretory cells of the female
reproductive tract. eLife. 2: e00415. https://doi.org/0.7554/eLife.00415
TAKKEN W.; SMALLEGANGE R. C.; VIGNEAU A. J.; JOHNSTON V.; BROWN M.; MORDUE-LUNTZ A. J.; BILLINGSLEY P. F. 2013. Larval nutrition differentially affects adult fitness and Plasmodium development in the malaria vectors Anopheles gambiae and Anopheles stephensi. Parasit. Vectors 6: 345. https://doi.org/10.1186/1756-3305-6-345
TEVATIYA S.; KUMARI S.; SHARMA P.; RANI J.; CHAUHAN C.; DAS DE T.; PANDEY K. C.; PANDE V.; DIXIT R. 2020. Molecular and Functional Characterization of Trehalase in the Mosquito Anopheles stephensi. Front. Physiol. 11: 575718. https://doi.org/10.3389/fphys.2020.575718
THAILAYIL J.; MAGNUSSON K.; GODFRAY H. C. J.; CRISANTI A.; CATTERUCCIA F. 2011. Spermless males elicit large-scale female responses to mating in the malaria mosquito Anopheles gambiae. Proc. Natl. Acad. Sci. U. S. A. 108: 13677–13681. https://doi.org/10.1073/pnas.1104738108
TSUNODA T.; FUKUCHI A.; NANBARA S.; TAKAGI M. 2010. Effect of body size and sugar meals on oviposition of the yellow fever mosquito, Aedes aegypti (Diptera: Culicidae). J. Vector Ecol. 35: 56–60. https://doi.org/10.1111/j.1948-7134.2010.00028.x
VANTAUX A.; LEFÈVRE T.; COHUET A.; DABIRÉ K. R.; ROCHE B.; ROUX O. 2016. Larval nutritional stress affects vector life history traits and human malaria transmission. Sci. Rep. 6: 36778. https://doi.org/10.1038/srep36778
VILLARREAL S. M.; PITCHER S.; HELINSKI M. E. H.; JOHNSON L.; WOLFNER M. F.; HARRINGTON L. C. 2018. Male contributions during mating increase female survival in the disease vector mosquito Aedes aegypti. J. Insect Physiol. 108: 1–9. https://doi.org/10.1016/j.jinsphys.2018.05.001
WARREN B.; GIBSON G.; RUSSELL I. J. 2009. Sex Recognition through midflight mating duets in Culex mosquitoes is mediated by acoustic distortion. Curr. Biol. 19: 485–491. https://doi.org/10.1016/j.cub.2009.01.059
WEINERT L. A.; ARAUJO-JNR E. V.; AHMED M. Z.; WELCH J. J. 2015. The incidence of bacterial endosymbionts in terrestrial arthropods. Proceedings. Biol. Sci. 282: 20150249. https://doi.org/10.1098/rspb.2015.0249
WERREN J. H.; BALDO L.; CLARK M. E. 2008. Wolbachia: master manipulators of invertebrate biology. Nat. Rev. Microbiol. 6: 741–751. https://doi.org/10.1038/nrmicro1969
WINSKILL P.; CARVALHO D. O.; CAPURRO M. L.; ALPHEY L.; DONNELLY C. A.; MCKEMEY A. R. 2015. Dispersal of Engineered Male Aedes aegypti Mosquitoes. PLoS Negl. Trop. Dis. 9: e0004156. https://doi.org/10.1371/journal.pntd.0004156
YAMANAKA N.; REWITZ K. F.; O'CONNOR M. B. 2013. Ecdysone control of developmental transitions: lessons from Drosophila research. Ann. Rev. Entomol. 58: 497-516. https://doi.org/10.1146/annurev-ento-120811-153608
YAN J.; KIBECH R.; STONE C. M. 2021. Differential effects of larval and adult nutrition on female survival, fecundity, and size of the yellow fever mosquito, Aedes aegypti. Front. Zool. 18: 10. https://doi.org/10.1186/s12983-021-00395-z
YUVAL B. 2005. Mating Systems of Blood-Feeding Flies. Annu. Rev. Entomol. 51: 413–440. https://doi.org/10.1146/annurev.ento.51.110104.151058
ZELLER M.; KOELLA J. C. 2016. Effects of food variability on growth and reproduction of Aedes aegypti. Ecol. Evol. 6: 552–559. https://doi.org/10.1002/ece3.1888
Accepted 2022-04-21
Published 2022-07-07
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