The neurobiology of gustation in insect disease vectors: progress and potential

Clements, 1992 Ready, 2013, Biology of phlebotomine sand flies as vectors of disease agents, Annu Rev Entomol, 58, 227, 10.1146/annurev-ento-120811-153557 Rodhain, 2015, Insects as vectors: systematics and biology, Rev Sci Tech, 34, 83 Barrozo, 2016, An inside look at the sensory biology of triatomines, J Insect Physiol Lehane, 2005 Dethier, 1976 Mullins, 2015, Physiology of environmental adaptations and resource acquisition in cockroaches, Annu Rev Entomol, 60, 473, 10.1146/annurev-ento-011613-162036 Raoult, 1999, The body louse as a vector of reemerging human diseases, Clin Infect Dis, 29, 888, 10.1086/520454 Takken, 2013, Host preferences of blood-feeding mosquitoes, Annu Rev Entomol, 58, 433, 10.1146/annurev-ento-120811-153618 McBride, 2016, Genes and odors underlying the recent evolution of mosquito preference for humans, Curr Biol, 26, R41, 10.1016/j.cub.2015.11.032 Reisenman, 2016, Neuroethology of olfactory-guided behavior and its potential application in the control of harmful insects, Front Physiol, 7, 271, 10.3389/fphys.2016.00271 Freeman, 2015, Molecular neurobiology of Drosophila taste, Curr Opin Neurobiol, 34, 140, 10.1016/j.conb.2015.06.001 Pontes, 2014, Bitter stimuli modulate the feeding decision of a blood-sucking insect via two sensory inputs, J Exp Biol, 217, 3708 Ledue, 2015, Pharyngeal sense organs drive robust sugar consumption in Drosophila, Nat Commun, 6, 10.1038/ncomms7667 Kessler, 2013, The sugar meal of the African malaria mosquito Anopheles gambiae and how deterrent compounds interfere with it: a behavioural and neurophysiological study, J Exp Biol, 216, 1292 Kessler, 2015, Sugar-sensitive neurone responses and sugar feeding preferences influence lifespan and biting behaviours of the Afrotropical malaria mosquito, Anopheles gambiae, J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 201, 317, 10.1007/s00359-015-0978-7 Fujii, 2015, Drosophila sugar receptors in sweet taste perception, olfaction, and internal nutrient sensing, Curr Biol, 25, 621, 10.1016/j.cub.2014.12.058 Sparks, 2016, Bitter-sensitive gustatory receptor neuron responds to chemically diverse insect repellents in the common malaria mosquito Anopheles quadrimaculatus, Naturwissenschaften, 103, 39, 10.1007/s00114-016-1367-y Sparks, 2016, Electrophysiological responses of gustatory receptor neurons on the labella of the common malaria mosquito, Anopheles quadrimaculatus (Diptera: Culicidae), J Med Entomol, 53, 1148, 10.1093/jme/tjw073 Kessler, 2014, Quinine and artesunate inhibit feeding in the African malaria mosquito Anopheles gambiae: the role of gustatory organs within the mouthparts, Physiol Entomol, 39, 172, 10.1111/phen.12061 Asparch, 2016, Kissing bugs can generalize and discriminate between different bitter compounds, J Physiol Paris, S0928-4257 Verhulst, 2010, Chemical ecology of interactions between human skin microbiota and mosquitoes, Fems Microbiol Ecol, 74, 1, 10.1111/j.1574-6941.2010.00908.x Choumet, 2012, Visualizing non infectious and infectious Anopheles gambiae blood feedings in naive and saliva-immunized mice, PLoS One, 7, e50464, 10.1371/journal.pone.0050464 Galun, 1963, Feeding response in Aedes Aegypti—stimulation by adenosine triphosphate, Science, 142, 1674-+, 10.1126/science.142.3600.1674 Dekker, 2002, l-lactic acid: a human-signifying host cue for the anthropophilic mosquito Anopheles gambiae, Med Vet Entomol, 16, 91, 10.1046/j.0269-283x.2002.00345.x Raad, 2016, Functional gustatory role of chemoreceptors in Drosophila wings, Cell Rep, 15, 1442, 10.1016/j.celrep.2016.04.040 Yanagawa, 2014, Hygienic grooming is induced by contact chemicals in Drosophila melanogaster, Front Behav Neurosci, 8 van Lenteren, 2007, Structure and electrophysiological responses of gustatory organs on the ovipositor of the parasitoid Leptopilina heterotoma, Arthropod Struct Dev, 36, 271, 10.1016/j.asd.2007.02.001 Jeong, 2013, An odorant-binding protein required for suppression of sweet taste by bitter chemicals, Neuron, 79, 725, 10.1016/j.neuron.2013.06.025 Kent, 2008, The Gr family of candidate gustatory and olfactory receptors in the yellow-fever mosquito Aedes aegypti, Chem Sens, 33, 79, 10.1093/chemse/bjm067 Hill, 2002, G protein-coupled receptors in Anopheles gambiae, Science, 298, 176, 10.1126/science.1076196 Zhou, 2014, De novo transcriptome of the Hemimetabolous German cockroach (Blattella germanica), PLoS One, 9, e106932, 10.1371/journal.pone.0106932 Neafsey, 2015, Mosquito genomics. Highly evolvable malaria vectors: the genomes of 16 Anopheles mosquitoes, Science, 347, 1258522, 10.1126/science.1258522 Mesquita, 2015, Genome of Rhodnius prolixus, an insect vector of Chagas disease, reveals unique adaptations to hematophagy and parasite infection, Proc Natl Acad Sci U S A, 112, 14936, 10.1073/pnas.1506226112 International Glossina Genome Initiative, 2014, Genome sequence of the tsetse fly (Glossina morsitans): vector of African trypanosomiasis, Science, 344, 380, 10.1126/science.1249656 Macharia, 2016, Genome-wide comparative analysis of chemosensory gene families in five tsetse fly species, PLoS Negl Trop Dis, 10 Andere, 2016, Genome sequence of Phormia regina Meigen (Diptera: Calliphoridae): implications for medical, veterinary and forensic research, BMC Genom, 17, 10.1186/s12864-016-3187-z Kent, 2009, Evolution of the sugar receptors in insects, BMC Evol Biol, 9, 41, 10.1186/1471-2148-9-41 Croset, 2010, Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction, PLoS Genet, 6, e1001064, 10.1371/journal.pgen.1001064 Sparks, 2013, Gustatory receptor expression in the labella and tarsi of Aedes aegypti, Insect Biochem Mol Biol, 43, 1161, 10.1016/j.ibmb.2013.10.005 Sparks, 2014, The genetics of chemoreception in the labella and tarsi of Aedes aegypti, Insect Biochem Mol Biol, 48, 8, 10.1016/j.ibmb.2014.02.004 Matthews, 2016, The neurotranscriptome of the Aedes aegypti mosquito, BMC Genom, 17, 32, 10.1186/s12864-015-2239-0 Pitts, 2011, Transcriptome profiling of chemosensory appendages in the malaria vector Anopheles gambiae reveals tissue- and sex-specific signatures of odor coding, BMC Genom, 12, 271, 10.1186/1471-2164-12-271 Carey, 2010, Odorant reception in the malaria mosquito Anopheles gambiae, Nature, 464, 66, 10.1038/nature08834 Wang, 2010, Molecular basis of odor coding in the malaria vector mosquito Anopheles gambiae, Proc Natl Acad Sci U S A Miyamoto, 2012, A fructose receptor functions as a nutrient sensor in the Drosophila brain, Cell, 151, 1113, 10.1016/j.cell.2012.10.024 Freeman, 2014, Detection of sweet tastants by a conserved group of insect gustatory receptors, Proc Natl Acad Sci U S A, 111, 1598, 10.1073/pnas.1311724111 Amrein, 2014, An expression system for gustatory receptors—and why it failed, Fly (Austin), 8, 232, 10.1080/19336934.2015.1039756 Wyatt, 2003 Vosshall, 2007, Molecular architecture of smell and taste in Drosophila, Annu Rev Neurosci, 30, 505, 10.1146/annurev.neuro.30.051606.094306 Rytz, 2013, Ionotropic receptors (IRs): chemosensory ionotropic glutamate receptors in Drosophila and beyond, Insect Biochem Mol Biol, 43, 888, 10.1016/j.ibmb.2013.02.007 Dippel, 2016, Morphological and transcriptomic analysis of a beetle chemosensory system reveals a gnathal olfactory center, BMC Biol, 14, 90, 10.1186/s12915-016-0304-z Kwon, 2006, Olfactory responses in a gustatory organ of the malaria vector mosquito Anopheles gambiae, Proc Natl Acad Sci U S A, 103, 13526, 10.1073/pnas.0601107103 Pitts, 2004, A highly conserved candidate chemoreceptor expressed in both olfactory and gustatory tissues in the malaria vector Anopheles gambiae, Proc Natl Acad Sci U S A, 101, 5058, 10.1073/pnas.0308146101 Jung, 2015, A novel olfactory pathway is essential for fast and efficient blood-feeding in mosquitoes, Sci Rep, 5, 13444, 10.1038/srep13444 Choo, 2015, Multitasking roles of mosquito labrum in oviposition and blood feeding, Front Physiol, 6, 306, 10.3389/fphys.2015.00306 Riabinina, 2016, Organization of olfactory centres in the malaria mosquito Anopheles gambiae, Nat Commun, 7, 13010, 10.1038/ncomms13010 Klowden, 1979, Humoral inhibition of host-seeking in Aedes aegypti during oocyte maturation, J Insect Physiol, 25, 231, 10.1016/0022-1910(79)90048-9 Matsumoto, 1989, Isolation and primary structure of neuropeptides from the mosquito, Aedes Aegypti, immunoreactive to FMRFamide antiserum, Insect Biochem, 19, 277, 10.1016/0020-1790(89)90073-5 Predel, 2010, Neuropeptidomics of the mosquito Aedes aegypti, J Proteome Res, 9, 2006, 10.1021/pr901187p Liesch, 2013, Functional and genetic characterization of neuropeptide Y-like receptors in Aedes aegypti, PLoS Negl Trop Dis, 7, e2486, 10.1371/journal.pntd.0002486 Rinker, 2013, Blood meal-induced changes to antennal transcriptome profiles reveal shifts in odor sensitivities in Anopheles gambiae, Proc Natl Acad Sci U S A, 110, 8260, 10.1073/pnas.1302562110 Fox, 2001, Candidate odorant receptors from the malaria vector mosquito Anopheles gambiae and evidence of down-regulation in response to blood feeding, Proc Natl Acad Sci U S A, 98, 14693, 10.1073/pnas.261432998 Meireles, 2013, Circadian rhythms in insect disease vectors, Memorias Do Instituto Oswaldo Cruz, 108, 48, 10.1590/0074-0276130438 Bernáth, 2016, Anopheles gambiae females readily learn to associate complex visual cues with the quality of sugar sources, J Insect Physiol, 95, 8, 10.1016/j.jinsphys.2016.08.011 Alonso, 2006, The ‘ghosts’ that pester studies on learning in mosquitoes: guidelines to chase them off, Med Vet Entomol, 20, 157, 10.1111/j.1365-2915.2006.00623.x Siju, 2008, Immunocytochemical localization of serotonin in the central and peripheral chemosensory system of mosquitoes, Arthropod Struct Dev, 37, 248, 10.1016/j.asd.2007.12.001 Zandawala, 2013, Post-feeding physiology in Rhodnius prolixus: the possible role of FGLamide-related allatostatins, Gen Comp Endocrinol, 194, 311, 10.1016/j.ygcen.2013.10.005 Kwon, 2016, Leucokinin mimetic elicits aversive behavior in mosquito Aedes aegypti (L.) and inhibits the sugar taste neuron, Proc Natl Acad Sci U S A, 113, 6880, 10.1073/pnas.1520404113 Rogers, 2007, Leishmania manipulation of sand fly feeding behavior results in enhanced transmission, PLoS Pathog, 3, e91, 10.1371/journal.ppat.0030091 Cator, 2012, Do malaria parasites manipulate mosquitoes?, Trends Parasitol, 28, 466, 10.1016/j.pt.2012.08.004 Lalubin, 2014, Natural malaria infection reduces starvation resistance of nutritionally stressed mosquitoes, J Anim Ecol, 83, 850, 10.1111/1365-2656.12190 Cator, 2013, ‘Manipulation’ without the parasite: altered feeding behaviour of mosquitoes is not dependent on infection with malaria parasites, Proc R Soc B-Biol Sci, 280 Cator, 2015, Immune response and insulin signalling alter mosquito feeding behaviour to enhance malaria transmission potential, Sci Rep, 5, 10.1038/srep11947 Ohm, 2016, Fitness consequences of altered feeding behavior in immune-challenged mosquitoes, Parasites Vectors, 9, 10.1186/s13071-016-1392-x Arguello, 2016, Extensive local adaptation within the chemosensory system following Drosophila melanogaster’s global expansion, Nat Commun, 7, 10.1038/ncomms11855 McBride, 2014, Evolution of mosquito preference for humans linked to an odorant receptor, Nature, 515, 222, 10.1038/nature13964 Logan, 2008, Identification of human-derived volatile chemicals that interfere with attraction of Aedes aegypti mosquitoes, J Chem Ecol, 34, 308, 10.1007/s10886-008-9436-0 Wada-Katsumata, 2013, Changes in taste neurons support the emergence of an adaptive behavior in cockroaches, Science, 340, 972, 10.1126/science.1234854 Wada-Katsumata, 2011, Differential inputs from chemosensory appendages mediate feeding responses to glucose in wild-type and glucose-averse German cockroaches, Blattella germanica, Chem Sens, 36, 589, 10.1093/chemse/bjr023 Jensen, 2015, Suboptimal nutrient balancing despite dietary choice in glucose-averse German cockroaches, Blattella germanica, J Insect Physiol, 81, 42, 10.1016/j.jinsphys.2015.07.001 Shik, 2014, Diet specialization in an extreme omnivore: nutritional regulation in glucose-averse German cockroaches, J Evol Biol, 27, 2096, 10.1111/jeb.12458 Faraji, 2016, The eye of the tiger, the thrill of the fight: effective larval and adult control measures against the Asian Tiger mosquito, Aedes albopictus (Diptera: Culicidae), in North America, J Med Entomol, 53, 1029, 10.1093/jme/tjw096 Leal, 2014, The enigmatic reception of DEET—the gold standard of insect repellents, Curr Opin Insect Sci, 6, 93, 10.1016/j.cois.2014.10.007 DeGennaro, 2015, The mysterious multi-modal repellency of DEET, Fly (Austin), 9, 45, 10.1080/19336934.2015.1079360 Silbering, 2016, Ir40a neurons are not DEET detectors, Nature, 534, E5, 10.1038/nature18321 Xu, 2014, Mosquito odorant receptor for DEET and methyl jasmonate, Proc Natl Acad Sci U S A, 111, 16592, 10.1073/pnas.1417244111 Syed, 2008, Mosquitoes smell and avoid the insect repellent DEET, Proc Natl Acad Sci U S A, 105, 13598, 10.1073/pnas.0805312105 Bar-Zeev, 1959, Action of a repellent as indicated by a radioactive tracer, J Econ Entomol, 52, 268, 10.1093/jee/52.2.268 Klun, 2006, Repellent and deterrent effects of SS220, Picaridin, and Deet suppress human blood feeding by Aedes aegypti, Anopheles stephensi, and Phlebotomus papatasi, J Med Entomol, 43, 34 Lee, 2010, Avoiding DEET through insect gustatory receptors, Neuron, 67, 555, 10.1016/j.neuron.2010.07.006 Sanford, 2013, Gustatory receptor neuron responds to DEET and other insect repellents in the yellow-fever mosquito, Aedes aegypti, Naturwissenschaften, 100, 269, 10.1007/s00114-013-1021-x Decourtye, 2010, Ecotoxicity of neonicotinoid insecticides to bees, Adv Exp Med Biol, 683, 85, 10.1007/978-1-4419-6445-8_8 Kessler, 2015, Bees prefer foods containing neonicotinoid pesticides, Nature, 521, 74, 10.1038/nature14414 Vaníčková, 2016, Sexual chemoecology of mosquitoes (Diptera, Culicidae): current knowledge and implications for vector control programs, Parasitol Int, S1383-5769, 30057 Auer, 2016, Sexual circuitry in Drosophila, Curr Opin Neurobiol, 38, 18, 10.1016/j.conb.2016.01.004 Suh, 2016, Suboptimal larval habitats modulate oviposition of the malaria vector mosquito Anopheles coluzzii, PLoS One, 11 Afify, 2015, Chemosensory cues for mosquito oviposition site selection, J Med Entomol, 52, 120, 10.1093/jme/tju024