Download:
Abstract
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.
571 506Catalina Alfonso-Parra, Instituto Colombiano de Medicina Tropical, Universidad CES
Dr. Catalina Alfonso-Parra is a member of both the Instituto Colombiano de Medicina Tropical (Universidad CES) and the Max Planck Tandem Group in Mosquito Reproductive Biology (Univerisdad de Antioquia).
- 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
How to Cite

This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
Copyright (c) 2022 Catalina Alfonso-Parra, Jéssica Osorio, Juliana Agudelo, Sebastián Díaz, Luis Ramírez-Sánchez, Frank Avila