Special Issue "Integrative Mosquito Biology: From Molecules to Ecosystems"

A special issue of Insects (ISSN 2075-4450).

Deadline for manuscript submissions: closed (31 January 2019)

Special Issue Editors

Guest Editor
Prof. Dr. Peter Piermarini

Department of Entomology, Ohio Agricultural Research and Development Center, The Ohio State University, 1680 Madison Ave., Wooster, OH 44691, USA
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Interests: physiology; toxicology; molecular biology
Guest Editor
Dr. Chloe Lahondere

Department of Biochemistry, Virginia Tech, 340 West Campus Drive, Blacskburg, VA 24061, USA
Website | E-Mail
Interests: behavior; ecology; physiology; disease vector insects; vector-host-pathogens interactions
Guest Editor
Dr. Clement Vinauger

Department of Biochemistry, Virginia Tech, 340 West Campus Drive, Blacksburg, VA 24061, USA
Website | E-Mail
Interests: disease vector insects; medical entomology; olfaction; neurobiology; behavior; learning and memory; chemical ecology

Special Issue Information

Dear Colleagues,

Mosquitoes captivate the attention of scientists and the public because they are the most dangerous animals on the planet, transmiting several debilitating and deadly diseases to humans, including malaria, dengue fever, lymphatic filariasis, and Zika. Underlying the danger they present to humans is a fascinating and complex biology on all levels, from molecules to ecosystems, which has been the subject of investigation for over a century. This special issue will report recent discoveries and review key subject areas in the field of mosquito biology, as well as the utilization of this biological knowledge to develop new solutions for controlling mosquitoes and the diseases they transmit.

Prof. Dr. Peter Piermarini
Dr. Chloe Lahondere
Dr. Clement Vinauger
Guest Editor

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All papers will be peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Insects is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 1000 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Please note that for papers submitted after 1 July 2018 an APC of 1000 CHF applies.

Keywords

  • mosquitoes

  • Physiology

  • molecular biology

  • toxicology

  • behavior

  • chemical biology

  • ecology

  • pathogens

Published Papers (25 papers)

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Open AccessArticle
Gamma Radiation Sterilization Dose of Adult Males in Asian Tiger Mosquito Pupae
Insects 2019, 10(4), 101; https://doi.org/10.3390/insects10040101
Received: 3 January 2019 / Revised: 20 March 2019 / Accepted: 22 March 2019 / Published: 8 April 2019
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Abstract
The pathogen-carrying tiger mosquito, Aedes albopictus, has spread from the Western Pacific and Southeast Asia to Europe, Africa, the Middle East, North and South America, and the Caribbean. This species of mosquito transmits arboviral infections, such as yellow fever, chikungunya, dengue, zika, [...] Read more.
The pathogen-carrying tiger mosquito, Aedes albopictus, has spread from the Western Pacific and Southeast Asia to Europe, Africa, the Middle East, North and South America, and the Caribbean. This species of mosquito transmits arboviral infections, such as yellow fever, chikungunya, dengue, zika, and several encephalitides. The objective of this research was to provide a radiation dose inducing sterilization in adult male Ae. albopictus in the pupal stage. A cobalt-60 source of gamma radiation at a dose rate of 381 Gy/h was used. The pupae were irradiated with doses of 0 (control), 20, 30, 40, 50, and 60 Gy. Each treatment had a total of five replications using 60 pupae. After irradiation, the different phases of Ae. albopictus development (egg, larva, pupa, and adult) in the F1 generation were observed daily. Parameters such as viability, fertility, longevity, and mortality were recorded. The results from these studies showed that a dose of 60 Gy was necessary to sterilize 100% of the male Ae. albopictus pupae. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessArticle
Heterologous Expression of Aedes aegypti Cation Chloride Cotransporter 2 (aeCCC2) in Xenopus laevis Oocytes Induces an Enigmatic Na+/Li+ Conductance
Received: 17 February 2019 / Revised: 6 March 2019 / Accepted: 9 March 2019 / Published: 14 March 2019
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Abstract
The yellow fever mosquito Aedes aegypti possesses three genes encoding putative Na+-coupled cation chloride cotransporters (CCCs): aeNKCC1, aeCCC2, and aeCCC3. To date, none of the aeCCCs have been functionally characterized. Here we expressed aeCCC2 heterologously in Xenopus oocytes and measured the [...] Read more.
The yellow fever mosquito Aedes aegypti possesses three genes encoding putative Na+-coupled cation chloride cotransporters (CCCs): aeNKCC1, aeCCC2, and aeCCC3. To date, none of the aeCCCs have been functionally characterized. Here we expressed aeCCC2 heterologously in Xenopus oocytes and measured the uptake of Li+ (a tracer for Na+) and Rb+ (a tracer for K+). Compared to control (H2O-injected) oocytes, the aeCCC2-expressing oocytes exhibited significantly greater uptake of Li+, but not Rb+. However, the uptake of Li+ was neither Cl-dependent nor inhibited by thiazide, loop diuretics, or amiloride, suggesting unconventional CCC activity. To determine if the Li+-uptake was mediated by a conductive pathway, we performed two-electrode voltage clamping (TEVC) on the oocytes. The aeCCC2 oocytes were characterized by an enhanced conductance for Li+ and Na+, but not K+, compared to control oocytes. It remains to be determined whether aeCCC2 directly mediates the Na+/Li+ conductance or whether heterologous expression of aeCCC2 stimulates an endogenous cation channel in the oocyte plasma membrane. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessCommunication
Insecticide Exposure Triggers a Modulated Expression of ABC Transporter Genes in Larvae of Anopheles gambiae s.s.
Received: 22 January 2019 / Revised: 21 February 2019 / Accepted: 28 February 2019 / Published: 5 March 2019
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Abstract
Insecticides remain a main tool for the control of arthropod vectors. The urgency to prevent the insurgence of insecticide resistance and the perspective to find new target sites, for the development of novel molecules, are fuelling the study of the molecular mechanisms involved [...] Read more.
Insecticides remain a main tool for the control of arthropod vectors. The urgency to prevent the insurgence of insecticide resistance and the perspective to find new target sites, for the development of novel molecules, are fuelling the study of the molecular mechanisms involved in insect defence against xenobiotic compounds. In this study, we have investigated if ATP-binding cassette (ABC) transporters, a major component of the defensome machinery, are involved in defence against the insecticide permethrin, in susceptible larvae of the malaria vector Anopheles gambiae sensu stricto. Bioassays were performed with permethrin alone, or in combination with an ABC transporter inhibitor. Then we have investigated the expression profiles of five ABC transporter genes at different time points following permethrin exposure, to assess their expression patterns across time. The inhibition of ABC transporters increased the larval mortality by about 15-fold. Likewise, three genes were up-regulated after exposure to permethrin, showing different patterns of expression across the 48 h. Our results provide the first evidences of ABC transporters involvement in defence against a toxic in larvae of An. gambiae s.s. and show that the gene expression response is modulated across time, being continuous, but stronger at the earliest and latest times after exposure. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessArticle
Pyriproxyfen-Treated Polypropylene Sheets and Resting Boxes for Controlling Mosquitoes in Livestock Operations
Received: 21 January 2019 / Revised: 13 February 2019 / Accepted: 14 February 2019 / Published: 18 February 2019
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Abstract
Many insect vector species of medical and veterinary importance are found abundantly in areas where animals are held. In these areas, they often rest for a period of time on objects around the animals both before and after blood feeding. However, the use [...] Read more.
Many insect vector species of medical and veterinary importance are found abundantly in areas where animals are held. In these areas, they often rest for a period of time on objects around the animals both before and after blood feeding. However, the use of neurotoxic insecticides for vector control is not advised for use in such shelters as these chemicals can pose hazards to animals. The present study evaluated the efficacy of pyriproxyfen (PPF), an insect growth regulator, applied to polypropylene sheets and resting boxes on the reproductivity of mosquitoes found in animal shelters in Chiang Mai, Thailand. The sheets sprayed with 666 mg PPF/m2 were set on the inner wall of a cowshed and kept in place for 3 h (6.00 to 9.00 pm). During this time, fully blood-fed female mosquitoes that landed and remained continuously on the sheets for 5, 10, and 20 min were collected. The results, involving Anopheles subpictus, An. vagus, Culex gelidus, Cx. tritaeniorhynchus, and Cx. vishnui, revealed significant reductions in oviposition rates, egg hatchability, pupation, and adult emergence in the PPF-treated groups compared to the control groups. Adult emergence rates were reduced to 85.6–94.9% and 95.5–100% in those exposed for 10 and 20 min, respectively. The sheets retained their effectiveness for three months. The PPF-treated (666 mg/m2) resting boxes (35 × 35 × 55 cm) were placed overnight at a chicken farm where Cx. quinquefasciatus predominated. Blood-fed mosquitoes were collected in the morning and reared in the laboratory. Oviposition rates were reduced by 71.7% and adult emergence was reduced by 97.8% compared to the controls. PPF residual spray on surface materials in animal sheds is a potential method for controlling mosquitoes. Further studies are needed to evaluate the impact of PPF-treated materials on wild populations. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessArticle
Green, Yellow, and Red Fluorescent Proteins as Markers for Bacterial Isolates from Mosquito Midguts
Received: 14 December 2018 / Revised: 29 January 2019 / Accepted: 31 January 2019 / Published: 3 February 2019
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Abstract
The growing awareness that microbial symbionts residing in mosquito midguts can interrupt transmission of vector-borne diseases has stimulated interest in understanding their potential role in mosquito biology. Fluorescent proteins are powerful molecular markers that provide for detailed analysis of the function and behavior [...] Read more.
The growing awareness that microbial symbionts residing in mosquito midguts can interrupt transmission of vector-borne diseases has stimulated interest in understanding their potential role in mosquito biology. Fluorescent proteins are powerful molecular markers that provide for detailed analysis of the function and behavior of specific midgut bacterial isolates without disturbing the normal gut microbiota. The aim of this study was to label bacterial isolates from the midgut of Ochlerotatus triseriatus, the primary vector of La Crosse virus, with green, yellow, and red fluorescent proteins (GFP, YFP, RFP) via electroporation. We also assessed the stability of GFP-, YFP-, and RFP-bearing plasmids and their effect on bacterial growth. Seven of eleven bacterial species could not be labeled despite several attempts. Labeling of Escherichia coli and Enterobacter cloacae was successfully achieved with all three fluorescent proteins. In contrast, labeling of Aerococcus viridans was achieved with GFP only and labeling of Aeromonas hydrophila was achieved with GFP and YFP only. The stability of GFP plasmid varied among bacterial species with A. hydrophila followed by E. cloacae having the most stable GFP label. In contrast, YFP and RFP plasmids were very stable in all bacterial species possessing these labels. GFP plasmid reduced the growth of labeled strains relative to wild type but this effect was not evident in YFP and RFP plasmids. These findings suggest that some mosquito midgut bacterial isolates can effectively be labeled with GFP, YFP and RFP plasmids allowing non-destructive studies on their functions within the vector. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessArticle
Attraction of Female Aedes aegypti (L.) to Aphid Honeydew
Received: 4 January 2019 / Revised: 19 January 2019 / Accepted: 22 January 2019 / Published: 1 February 2019
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Abstract
Plant sugar is an essential dietary constituent for mosquitoes, and hemipteran honeydew is one of the many forms of plant sugar that is important to mosquitoes. Many insects rely on volatile honeydew semiochemicals to locate aphids or honeydew itself. Mosquitoes exploit volatile semiochemicals [...] Read more.
Plant sugar is an essential dietary constituent for mosquitoes, and hemipteran honeydew is one of the many forms of plant sugar that is important to mosquitoes. Many insects rely on volatile honeydew semiochemicals to locate aphids or honeydew itself. Mosquitoes exploit volatile semiochemicals to locate sources of plant sugar but their attraction to honeydew has not previously been investigated. Here, we report the attraction of female yellow fever mosquitoes, Aedes aegypti, to honeydew odorants from the green peach aphid, Myzus persicae, and the pea aphid, Acyrthosiphon pisum, feeding on fava bean, Vicia faba. We used solid phase micro-extraction and gas chromatography-mass spectrometry to collect and analyze headspace odorants from the honeydew of A. pisum feeding on V. faba. An eight-component synthetic blend of these odorants and synthetic odorant blends of crude and sterile honeydew that we prepared according to literature data all attracted female A. aegypti. The synthetic blend containing microbial odor constituents proved more effective than the blend without these constituents. Our study provides the first evidence for anemotactic attraction of mosquitoes to honeydew and demonstrates a role for microbe-derived odorants in the attraction of mosquitoes to essential plant sugar resources. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessArticle
Landscape and Environmental Factors Influencing Stage Persistence and Abundance of the Bamboo Mosquito, Tripteroides bambusa (Diptera: Culicidae), across an Altitudinal Gradient
Received: 24 December 2018 / Revised: 11 January 2019 / Accepted: 12 January 2019 / Published: 1 February 2019
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Abstract
The bamboo mosquito, Tripteroides bambusa (Yamada) (Diptera: Culicidae), is a common insect across East Asia. Several studies have looked at the ecology of Tr. bambusa developmental stages separately, but little is known about the factors associated with the persistence (how often) and [...] Read more.
The bamboo mosquito, Tripteroides bambusa (Yamada) (Diptera: Culicidae), is a common insect across East Asia. Several studies have looked at the ecology of Tr. bambusa developmental stages separately, but little is known about the factors associated with the persistence (how often) and abundance (how many individuals) of Tr. bambusa stages simultaneously studied across a heterogeneous landscape. Here, we ask what environmental and landscape factors are associated with the persistence and abundance of Tr. bambusa stages across the altitudinal gradient of Mt. Konpira, Nagasaki City, Japan. During a season-long study we counted 8065 (7297 4th instar larvae, 670 pupae and 98 adults) Tr. bambusa mosquitoes. We found that persistence and abundance patterns were not associated among stages, with the exception of large (4th instar) and small (1st to 3rd instars) larvae persistence, which were positively correlated. We also found that relative humidity was associated with the persistence of Tr. bambusa aquatic stages, being positively associated with large and small larvae, but negatively with pupae. Similarly, landscape aspect changed from positive to negative the sign of its association with Tr. bambusa pupae and adults, highlighting that environmental associations change with life stage. Meanwhile, Tr. bambusa abundance patterns were negatively impacted by more variable microenvironments, as measured by the negative impacts of kurtosis and standard deviation (SD) of environmental variables, indicating Tr. bambusa thrives in stable environments, suggesting this mosquito species has a finely grained response to environmental changes. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessArticle
Population Dynamics of Anopheles albimanus (Diptera: Culicidae) at Ipetí-Guna, a Village in a Region Targeted for Malaria Elimination in Panamá
Received: 22 May 2018 / Revised: 16 July 2018 / Accepted: 17 July 2018 / Published: 16 November 2018
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Abstract
Anopheles albimanus Wiedemann is a major malaria vector in Mesoamerica and the Caribbean whose population dynamics, in response to changing environments, has been relatively poorly studied. Here, we present monthly adult and larvae data collected from May 2016 to December 2017 in Ipetí-Guna, [...] Read more.
Anopheles albimanus Wiedemann is a major malaria vector in Mesoamerica and the Caribbean whose population dynamics, in response to changing environments, has been relatively poorly studied. Here, we present monthly adult and larvae data collected from May 2016 to December 2017 in Ipetí-Guna, a village within an area targeted for malaria elimination in the República de Panamá. During the study period we collected a total of 1678 Anopheles spp. mosquitoes (1602 adults and 76 larvae). Over 95% of the collected Anopheles spp. mosquitoes were An. albimanus. Using time series analysis techniques, we found that population dynamics of larvae and adults were not significantly correlated with each other at any time lag, though correlations were highest at one month lag between larvae and adults and four months lag between adults and larvae. Larvae population dynamics had cycles of three months and were sensitive to changes in temperature with 5 months lag, while adult abundance was correlated with itself (1 month lag) and with the normalized difference vegetation index (NDVI) with three months lag. A key observation from our study is the absence of both larvae and adults of An. albimanus between January and April from environments associated with Guna population’s daily activities, which suggests this time window could be the best time to implement elimination campaigns aimed at clearing Plasmodium spp. parasites from Guna populations using, for example, mass drug administration. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessCommunication
Pharmacological Inhibition of Inward Rectifier Potassium Channels Induces Lethality in Larval Aedes aegypti
Received: 15 October 2018 / Revised: 7 November 2018 / Accepted: 12 November 2018 / Published: 15 November 2018
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Abstract
The inward rectifier potassium (Kir) channels play key roles in the physiology of mosquitoes and other insects. Our group, among others, previously demonstrated that small molecule inhibitors of Kir channels are promising lead molecules for developing new insecticides to control adult female mosquitoes. [...] Read more.
The inward rectifier potassium (Kir) channels play key roles in the physiology of mosquitoes and other insects. Our group, among others, previously demonstrated that small molecule inhibitors of Kir channels are promising lead molecules for developing new insecticides to control adult female mosquitoes. However, the potential use of Kir channel inhibitors as larvicidal agents is unknown. Here we tested the hypothesis that pharmacological inhibition of Kir channels in the larvae of Aedes aegypti, the vector of several medically important arboviruses, induces lethality. We demonstrated that adding barium, a non-specific blocker of Kir channels, or VU041, a specific small-molecule inhibitor of mosquito Kir1 channels, to the rearing water (deionized H2O) of first instar larvae killed them within 48 h. We further showed that the toxic efficacy of VU041 within 24 h was significantly enhanced by increasing the osmolality of the rearing water to 100 mOsm/kg H2O with NaCl, KCl or mannitol; KCl provided the strongest enhancement compared to NaCl and mannitol. These data suggest: (1) the important role of Kir channels in the acclimation of larvae to elevated ambient osmolality and KCl concentrations; and (2) the disruption of osmoregulation as a potential mechanism of the toxic action of VU041. The present study provides the first evidence that inhibition of Kir channels is lethal to larval mosquitoes and broadens the potential applications of our existing arsenal of small molecule inhibitors of Kir channels, which have previously only been considered for developing adulticides. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessArticle
Fatty Acid and Related Potassium Kv2 Channel Blockers: Toxicity and Physiological Actions on Mosquitoes
Received: 27 September 2018 / Revised: 19 October 2018 / Accepted: 30 October 2018 / Published: 1 November 2018
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Abstract
Potassium channels constitute a very diverse group involved in neural signaling, neuronal activity, membrane potential maintenance, and action potential generation. Here, we tested the mammalian potassium channel blockers TRAM-34 and 5-hydroxydecanoate (5-HDC), as well as certain fatty acids (FA) that might fit in [...] Read more.
Potassium channels constitute a very diverse group involved in neural signaling, neuronal activity, membrane potential maintenance, and action potential generation. Here, we tested the mammalian potassium channel blockers TRAM-34 and 5-hydroxydecanoate (5-HDC), as well as certain fatty acids (FA) that might fit in the lumen of the pore and block channel activity by obstructing K+ ion passage. Kv channel blockers could be leads for a novel pesticide type. Insecticidal activity was assessed by topical application to Anopheles gambiae adult mosquitoes, paralysis in a headless larval assay, at the cellular level with patch-clamp recordings of engineered HEK cells expressing AgKv2.1 channels, as well as central nervous system recordings from larval Drosophila melanogaster. With only one hydroxyl group difference, decanoic acid had a consistently greater effect than 5-HDC in blocking Kv channels, paralyzing larvae, and killing mosquitoes. The 11-dansylamino undecanoic acid (DAUDA) blockage of eukaryotic Kv channels is demonstrated for the first time, but it failed to kill adult mosquitoes. We synthesized alkyl esters from DAUDA and decanoic acid in an effort to improve cuticular penetration, but it had little impact upon adult toxicity. TRAM-34 and rolipram did not show activity on Kv channels nor potent insecticidal effect on adult mosquitoes. Furthermore, co-application of test compounds with permethrin did not increase mortality in adults. In conclusion, the compounds tested had modest insecticidal and synergistic activity. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessFeature PaperArticle
Odor-Specific Daily Rhythms in the Olfactory Sensitivity and Behavior of Aedes aegypti Mosquitoes
Received: 29 September 2018 / Revised: 18 October 2018 / Accepted: 19 October 2018 / Published: 23 October 2018
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Abstract
Many biological processes and behaviors in mosquitoes display rhythmic patterns, allowing for fine tuning to cyclic environmental conditions. In mosquitoes, vector-host interactions are primarily mediated by olfactory signals. Previous studies have established that, in the malaria vector Anopheles gambiae, rhythmic expression of [...] Read more.
Many biological processes and behaviors in mosquitoes display rhythmic patterns, allowing for fine tuning to cyclic environmental conditions. In mosquitoes, vector-host interactions are primarily mediated by olfactory signals. Previous studies have established that, in the malaria vector Anopheles gambiae, rhythmic expression of odorant binding proteins and takeout proteins in the antenna resulted in a corresponding rhythm in olfactory sensitivity to relevant host odors. However, it remained unclear how rhythms observed in olfactory sensitivity affect or explain rhythms in behavioral output, which ultimately impacts disease transmission. In order to address this knowledge gap, we quantified and compared patterns in locomotor activity, olfactory sensitivity, and olfactory behaviors in adult female Aedes aegypti mosquitoes. Here, we demonstrate an odorant-specific modulation of olfactory sensitivity in Ae. aegypti, decoupled from rhythms in olfactory behavior. Additionally, behavioral assays performed herein represent the first evidence of a time-dependence of the olfactory activation of behavior in Ae. aegypti mosquitoes. Results suggest that olfactory behavior of Aedes mosquitoes is modulated at both the peripheral (antenna) and central levels. As such, this work serves as a foundation for future studies aimed at further understanding the neural and molecular mechanisms underlying behavioral plasticity. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessArticle
Characterizing Permethrin and Etofenprox Resistance in Two Common Laboratory Strains of Anopheles gambiae (Diptera: Culicidae)
Received: 27 September 2018 / Revised: 14 October 2018 / Accepted: 14 October 2018 / Published: 22 October 2018
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Abstract
Anopheles gambiae Giles (Diptera: Culicidae) is the most prolific malaria vector in sub-Saharan Africa, where widespread insecticide resistance has been reported. An. gambiae laboratory strains are commonly used to study the basic biology of this important mosquito vector, and also in new insecticide [...] Read more.
Anopheles gambiae Giles (Diptera: Culicidae) is the most prolific malaria vector in sub-Saharan Africa, where widespread insecticide resistance has been reported. An. gambiae laboratory strains are commonly used to study the basic biology of this important mosquito vector, and also in new insecticide discovery programs, where insecticide-susceptible and -resistant strains are often used to screen new molecules for potency and cross-resistance, respectively. This study investigated the toxicity of permethrin, a Type-I pyrethroid insecticide, and etofenprox, a non-ester containing pyrethroid insecticide, against An. gambiae at three life stages. This characterization was performed with susceptible (G3; MRA-112) and resistant (Akdr; MRA-1280) An. gambiae strains; the Akdr strain is known to contain the L1014F mutation in the voltage-sensitive sodium channel. Surprisingly, etofenprox displays a lower level of resistance than permethrin against all stages of mosquitoes, except in a headless larval paralysis assay designed to minimize penetration factors. In first-instar An. gambiae larvae, permethrin had significant resistance, determined by the resistance ratio (RR50 = 5), but etofenprox was not significantly different (RR50 = 3.4) from the wild-type strain. Fourth-instar larvae displayed the highest level of resistance for permethrin (RR50 = 108) and etofenprox (RR50 = 35). Permethrin (PC50 = 2 ppb) and etofenprox (PC50 = 9 ppb) resulted in headless larval paralysis (5-h), but resistance, albeit lower, was still present for permethrin (RR50 = 5) and etofenprox (RR50 = 6.9). In adult female mosquitoes, permethrin displayed higher resistance (RR50 = 14) compared to etofenprox (RR50 = 4.3). The level of etofenprox resistance was different from that previously reported for a similar Akron An. gambiae laboratory strain (MRA-913). The chemical synergists piperonyl butoxide (PBO) and diethyl maleate (DEM) were able to synergize permethrin, but not etofenprox in the resistant strain (Akdr). In conclusion, multiple mechanisms are likely involved in pyrethroid resistance, but resistance profiles are dependent upon selection. Etofenprox is an effective insecticide against An. gambiae in the lab but will likely suffer from resistance in the field. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
Open AccessArticle
Effects of Alternative Blood Sources on Wolbachia Infected Aedes aegypti Females within and across Generations
Received: 11 September 2018 / Revised: 6 October 2018 / Accepted: 9 October 2018 / Published: 11 October 2018
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Abstract
Wolbachia bacteria have been identified as a tool for reducing the transmission of arboviruses transmitted by Aedes aegypti. Research groups around the world are now mass rearing Wolbachia-infected Ae. aegypti for deliberate release. We investigated the fitness impact of a crucial [...] Read more.
Wolbachia bacteria have been identified as a tool for reducing the transmission of arboviruses transmitted by Aedes aegypti. Research groups around the world are now mass rearing Wolbachia-infected Ae. aegypti for deliberate release. We investigated the fitness impact of a crucial element of mass rearing: the blood meal required by female Ae. aegypti to lay eggs. Although Ae. aegypti almost exclusively feed on human blood, it is often difficult to use human blood in disease-endemic settings. When females were fed on sheep or pig blood rather than human blood, egg hatch rates decreased in all three lines tested (uninfected, or infected by wMel, or wAlbB Wolbachia). This finding was particularly pronounced when fed on sheep blood, although fecundity was not affected. Some of these effects persisted after an additional generation on human blood. Attempts to keep populations on sheep and pig blood sources only partly succeeded, suggesting that strong adaptation is required to develop a stably infected line on an alternative blood source. There was a decrease in Wolbachia density when Ae. aegypti were fed on non-human blood sources. Density increased in lines kept for multiple generations on the alternate sources but was still reduced relative to lines kept on human blood. These findings suggest that sheep and pig blood will entail a cost when used for maintaining Wolbachia-infected Ae. aegypti. These costs should be taken into account when planning mass release programs. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessArticle
Plant Essential Oils Enhance Diverse Pyrethroids against Multiple Strains of Mosquitoes and Inhibit Detoxification Enzyme Processes
Received: 14 August 2018 / Revised: 21 September 2018 / Accepted: 21 September 2018 / Published: 4 October 2018
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Abstract
Mosquito-borne diseases account for the deaths of approximately 700,000 people annually throughout the world, with many more succumbing to the debilitating side effects associated with these etiologic disease agents. This is exacerbated in many countries where the lack of mosquito control and resources [...] Read more.
Mosquito-borne diseases account for the deaths of approximately 700,000 people annually throughout the world, with many more succumbing to the debilitating side effects associated with these etiologic disease agents. This is exacerbated in many countries where the lack of mosquito control and resources to prevent and treat mosquito-borne disease coincide. As populations of mosquito species grow more resistant to currently utilized control chemistries, the need for new and effective chemical means for vector control is more important than ever. Previous work revealed that plant essential oils enhance the toxicity of permethrin against multiple mosquito species that are of particular importance to public health. In this study, we screened permethrin and deltamethrin in combination with plant essential oils against a pyrethroid-susceptible and a pyrethroid-resistant strain of both Aedes aegypti and Anopheles gambiae. A number of plant essential oils significantly enhanced the toxicity of pyrethroids equal to or better than piperonyl butoxide, a commonly used synthetic synergist, in all strains tested. Significant synergism of pyrethroids was also observed for specific combinations of plant essential oils and pyrethroids. Moreover, plant essential oils significantly inhibited both cytochrome P450 and glutathione S-transferase activities, suggesting that the inhibition of detoxification contributes to the enhancement or synergism of plant essential oils for pyrethroids. This study highlights the potential of using diverse plant oils as insecticide additives to augment the efficacy of insecticidal formulations. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessArticle
Attraction of Culex pipiens to House Sparrows Is Influenced by Host Age but Not Uropygial Gland Secretions
Received: 27 August 2018 / Revised: 21 September 2018 / Accepted: 22 September 2018 / Published: 25 September 2018
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Abstract
Culex pipiens serves as the endemic vector of West Nile virus (WNV) in eastern North America, where house sparrows (HOSP, Passer domesticus) serve as a reservoir host. We tested the hypotheses that: (1) Attraction of Cx. pipiens to HOSP is influenced by [...] Read more.
Culex pipiens serves as the endemic vector of West Nile virus (WNV) in eastern North America, where house sparrows (HOSP, Passer domesticus) serve as a reservoir host. We tested the hypotheses that: (1) Attraction of Cx. pipiens to HOSP is influenced by bird age and (2) that age-specific variation in chemical profiles of bird uropygial gland secretions informs this choice. We conducted mosquito choice trials in an olfactometer and found that Cx. pipiens were more often attracted to adult sparrows over nestlings, however, they demonstrated no preference for adults over fledglings. Using gas chromatography-mass spectrometry we observed age-specific differences in the semi-volatile chemical profiles of house sparrow uropygial gland secretions. Contrary to our hypothesis, we found no significant difference in mosquito feeding preference between the secretions of adults and those of either nestlings or fledglings. We suggest that other chemical cues influence the feeding preference of Cx. pipiens, either independently of uropygial gland secretions, or synergistically with them. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessArticle
Nutritional Quality during Development Alters Insulin-Like Peptides’ Expression and Physiology of the Adult Yellow Fever Mosquito, Aedes aegypti
Received: 5 June 2018 / Revised: 30 July 2018 / Accepted: 22 August 2018 / Published: 30 August 2018
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Abstract
Mosquitoes have distinct developmental and adult life history, and the vectorial capacity of females has been shown to be affected by the larval nutritional environment. However, little is known about the effect of developmental nutrition on insulin-signaling and nutrient storage. In this study, [...] Read more.
Mosquitoes have distinct developmental and adult life history, and the vectorial capacity of females has been shown to be affected by the larval nutritional environment. However, little is known about the effect of developmental nutrition on insulin-signaling and nutrient storage. In this study, we used Aedes aegypti, the yellow fever mosquito, to determine whether larval nutrition affects insulin gene expression. We also determined the traits regulated by insulin signaling, such as stored-nutrient levels and fecundity. We raised mosquito larvae on two different diets, containing either high protein or high carbohydrates. Development on a high-carbohydrate diet resulted in several life-history phenotypes indicative of suboptimal conditions, including increased developmental time and decreased fecundity. Additionally, our data showed that insulin transcript levels are affected by a high-carbohydrate diet during development. Females, not males, reared on high-carbohydrate diets had much higher transcript levels of insulin-like peptide 3 (ILP3), a mosquito equivalent of human insulin, and these females more readily converted sugar meals into lipids. We also found that AaILP4, not AaILP3, transcript levels were much higher in the males after a sugar meal, suggesting sex-specific differences in the insulin-signaling pathway. Our findings suggest a conserved mechanism of carbohydrate-mediated hyperinsulinemia in animals. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessArticle
Evaluation of Eosin-Methylene Blue as a Photosensitizer for Larval Control of Aedes aegypti by a Photodynamic Process
Received: 7 June 2018 / Revised: 13 August 2018 / Accepted: 22 August 2018 / Published: 30 August 2018
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Abstract
Aedes aegypti (Ae. aegypti) is a competent vector for transmitting important viral diseases such as yellow fever, dengue, chikungunya, and Zika. Several strategies have been applied to avoid Ae. aegypti proliferation by using environmental management, biological, and chemical approaches. However, the [...] Read more.
Aedes aegypti (Ae. aegypti) is a competent vector for transmitting important viral diseases such as yellow fever, dengue, chikungunya, and Zika. Several strategies have been applied to avoid Ae. aegypti proliferation by using environmental management, biological, and chemical approaches. However, the development of new methods for effective control of the insect vector population is still needed. Photodynamic control is an alternative way to control the vector population by using a physical approach based on the larval phototoxicity of a photosensitizer. In this context, the present study evaluated the use of eosin-methylene blue (EMB) as a new photosensitizer for photodynamic control of Ae. aegypti larval populations. The photodynamic assays were performed submitting Ae. aegypti third-instar larvae to different EMB concentrations (0.0, 0.5, 1.0, 5.0, 10.0, 50.0, and 100.0 µg mL−1) in combination of three different light doses (24.3, 48.6, and 97.2 J cm−2) under either white-light radiation from RGB LEDs or sunlight. The results demonstrated that EMB presented a rapid internalization into the larvae and was phototoxic. The photodynamic action induced 100% of larval mortality after about 40 min of sunlight irradiation even using low EMB concentration (0.5 µg mL−1). The findings reveal EMB as an effective photoactive compound to control larval populations of Ae. aegypti by photodynamic process induced by either sunlight or white-light from RGB LEDs. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessArticle
Oviplate: A Convenient and Space-Saving Method to Perform Individual Oviposition Assays in Aedes aegypti
Received: 3 July 2018 / Revised: 31 July 2018 / Accepted: 9 August 2018 / Published: 15 August 2018
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Abstract
Aedes aegypti is the principal vector of the urban arboviruses and the blood ingestion is important to produce the eggs in this species. To analyze the egg production in Ae. aegypti, researchers frequently use small cages or Drosophila vials to collect eggs [...] Read more.
Aedes aegypti is the principal vector of the urban arboviruses and the blood ingestion is important to produce the eggs in this species. To analyze the egg production in Ae. aegypti, researchers frequently use small cages or Drosophila vials to collect eggs from gravid females. Although it is affordable, the setup is time- and space-consuming, mainly when many mosquitoes need to be individually analyzed. This study presents an easy, cheap, and space-saving method to perform individual oviposition assays in Ae. aegypti using cell culture plates. This new method to access fecundity rate was named “oviplate”. The oviplates are setup with 12- or 24-well plates, distilled water and filter paper and they are 78 to 88% cheaper than the traditional Drosophila vial assay, respectively. Furthermore, to allocate 72 vitellogenic females in an insectary using Drosophila vial is necessary 4100 cm3 against 1400 cm3 and 700 cm3 when using 12- and 24-well plates, respectively. No statistical differences were found between the number of eggs laid in Drosophila vials and the oviplates, validating the method. The oviplate method is an affordable, and time- and space-efficient device, and it is simpler to perform individual fecundity analyses in Ae. aegypti. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessArticle
Increased Adult Aedes aegypti and Culex quinquefasciatus (Diptera: Culicidae) Abundance in a Dengue Transmission Hotspot, Compared to a Coldspot, within Kaohsiung City, Taiwan
Received: 20 June 2018 / Revised: 30 July 2018 / Accepted: 10 August 2018 / Published: 13 August 2018
Cited by 4 | PDF Full-text (4283 KB) | HTML Full-text | XML Full-text | Supplementary Files
Abstract
The assumption that vector abundance differences might drive spatial and temporal heterogeneities in vector-borne disease transmission is common, though data supporting it is scarce. Here, we present data from two common mosquito species Aedes aegypti (Linnaeus) and Culex quinquefasciatus Say, biweekly sampled as [...] Read more.
The assumption that vector abundance differences might drive spatial and temporal heterogeneities in vector-borne disease transmission is common, though data supporting it is scarce. Here, we present data from two common mosquito species Aedes aegypti (Linnaeus) and Culex quinquefasciatus Say, biweekly sampled as adults, from March 2016 through December 2017, with BG-sentinel traps in two neighboring districts of Kaohsiung City (KC), Taiwan. One district has historically been a dengue transmission hotspot (Sanmin), and the other a coldspot (Nanzih). We collected a total 41,027 mosquitoes, and we found that average mosquito abundance (mean ± S.D.) was higher in Sanmin (Ae. aegypti: 9.03 ± 1.46; Cx. quinquefasciatus: 142.57 ± 14.38) than Nanzih (Ae. aegypti: 6.21 ± 0.47; Cx. quinquefasciatus: 63.37 ± 8.71) during the study period. In both districts, Ae. aegypti and Cx. quinquefasciatus population dynamics were sensitive to changes in temperature, the most platykurtic environmental variable at KC during the study period, a pattern predicted by Schmalhausen’s law, which states that organisms are more sensitive to small changes in environmental variables whose average value is more uncertain than its extremes. Our results also suggest that differences in Ae. aegypti abundance might be responsible for spatial differences in dengue transmission at KC. Our comparative approach, where we also observed a significant increment in the abundance of Cx. quinquefasciatus in the dengue transmission hotspot, suggests this area might be more likely to experience outbreaks of other vector borne diseases and should become a primary focus for vector surveillance and control. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessArticle
Alterations and Interchange of Morphometric Characters in Different Life Cycle Stages with Reference to Genomic Variations of Anopheles subpictus (Diptera; Culicidae) Sibling Species Complex in Sri Lanka
Received: 21 May 2018 / Revised: 10 July 2018 / Accepted: 19 July 2018 / Published: 24 July 2018
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Abstract
The species complex of the mosquito Anopheles subpictus is designated by the sibling species A–D, depending on morphological characters of life cycle stages and variations in polytene chromosomes. However, morphological aberrations in the life cycle stages make the identification of sibling species uncertain [...] Read more.
The species complex of the mosquito Anopheles subpictus is designated by the sibling species A–D, depending on morphological characters of life cycle stages and variations in polytene chromosomes. However, morphological aberrations in the life cycle stages make the identification of sibling species uncertain and imprecise. The objective of the present study is to determine the suitability of morphological variations of sibling species and their genomic variations to identify the sibling species status of an An. subpictus population in Sri Lanka. Life cycle stages of larvae, pupal exuviae, and adults were examined for previously reported distinctive morphological features. Five nuclear and mitochondrial genome regions, including the Internal transcribed spacer 2 (ITS2) region, D3 region, white gene, cytochrome c oxidase I (COI), and Cytochrome b (Cyt-b), were sequenced and analyzed for variations. The eggs changed their distinct sibling morphological characters during metamorphosis (89.33%). The larvae, pupal exuviae, and adult stages showed deviation from their sibling characters by 26.10%, 19.71%, and 15.87%, respectively. However, all the species from the analysis shared two distinct sequence types for all regions, regardless of the morphological variations. In conclusion, the An. subpictus sibling species complex in Sri Lanka is not identifiable using morphological characters due to variations, and the genomic variations are independent from the morphological variations. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessArticle
Oviposition Deterrent and Larvicidal and Pupaecidal Activity of Seven Essential Oils and their Major Components against Culex quinquefasciatus Say (Diptera: Culicidae): Synergism–antagonism Effects
Received: 6 January 2018 / Revised: 9 February 2018 / Accepted: 12 February 2018 / Published: 14 February 2018
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Abstract
The larvicidal activity of essential oils cinnamon (Cinnamomum verum J. Presl), Mexican lime (Citrus aurantifolia Swingle) cumin (Cuminum cyminum Linnaeus), clove (Syzygium aromaticum (L.) Merr. & L.M.Perry), laurel (Laurus nobilis Linnaeus), Mexican oregano (Lippia berlandieri Schauer) and [...] Read more.
The larvicidal activity of essential oils cinnamon (Cinnamomum verum J. Presl), Mexican lime (Citrus aurantifolia Swingle) cumin (Cuminum cyminum Linnaeus), clove (Syzygium aromaticum (L.) Merr. & L.M.Perry), laurel (Laurus nobilis Linnaeus), Mexican oregano (Lippia berlandieri Schauer) and anise (Pimpinella anisum Linnaeus)) and their major components are tested against larvae and pupae of Culex quinquefasciatus Say. Third instar larvae and pupae are used for determination of lethality and mortality. Essential oils with more than 90% mortality after a 30-min treatment are evaluated at different time intervals. Of the essential oils tested, anise and Mexican oregano are effective against larvae, with a median lethal concentration (LC50) of 4.7 and 6.5 µg/mL, respectively. Anise essential oil and t-anethole are effective against pupae, with LC50 values of 102 and 48.7 µg/mL, respectively. Oregano essential oil and carvacrol also have relevant activities. A kinetic analysis of the larvicidal activity, the oviposition deterrent effect and assays of the effects of the binary mixtures of chemical components are undertaken. Results show that anethole has synergistic effects with other constituents. This same effect is observed for carvacrol and thymol. Limonene shows antagonistic effect with β-pinene. The high larvicidal and pupaecidal activities of essential oils and its components demonstrate that they can be potential substitutes for chemical compounds used in mosquitoes control programs. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Review

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Open AccessReview
Physiological and Environmental Factors Affecting the Composition of the Ejaculate in Mosquitoes and Other Insects
Received: 23 January 2019 / Revised: 5 March 2019 / Accepted: 8 March 2019 / Published: 15 March 2019
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Abstract
In addition to transferring sperm, male mosquitoes deliver several proteins, hormones and other factors to females in their seminal fluid that inhibit remating, alter host-seeking behaviors and stimulate oviposition. Recently, bioinformatics, transcriptomics and proteomics have been used to characterize the genes transcribed in [...] Read more.
In addition to transferring sperm, male mosquitoes deliver several proteins, hormones and other factors to females in their seminal fluid that inhibit remating, alter host-seeking behaviors and stimulate oviposition. Recently, bioinformatics, transcriptomics and proteomics have been used to characterize the genes transcribed in male reproductive tissues and the individual proteins that are delivered to females. Thanks to these foundational studies, we now understand the complexity of the ejaculate in several mosquito species. Building on this work, researchers have begun to identify the functions of various proteins and hormones in the male ejaculate, and how they mediate their effects on female mosquitoes. Here, we present an overview of these studies, followed by a discussion of an under-studied aspect of male reproductive physiology: the effects of biotic and abiotic factors on the composition of the ejaculate. We argue that future research in this area would improve our understanding of male reproductive biology from a physiological and ecological perspective, and that researchers may be able to leverage this information to study key components of the ejaculate. Furthermore, this work has the potential to improve mosquito control by allowing us to account for relevant factors when implementing vector control strategies involving male reproductive biology. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessReview
Effects of the Environmental Temperature on Aedes aegypti and Aedes albopictus Mosquitoes: A Review
Received: 30 September 2018 / Revised: 25 October 2018 / Accepted: 31 October 2018 / Published: 6 November 2018
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Abstract
The temperature of the environment is one of the most important abiotic factors affecting the life of insects. As poikilotherms, their body temperature is not constant, and they rely on various strategies to minimize the risk of thermal stress. They have been thus [...] Read more.
The temperature of the environment is one of the most important abiotic factors affecting the life of insects. As poikilotherms, their body temperature is not constant, and they rely on various strategies to minimize the risk of thermal stress. They have been thus able to colonize a large spectrum of habitats. Mosquitoes, such as Ae. aegypti and Ae. albopictus, vector many pathogens, including dengue, chikungunya, and Zika viruses. The spread of these diseases has become a major global health concern, and it is predicted that climate change will affect the mosquitoes’ distribution, which will allow these insects to bring new pathogens to naïve populations. We synthesize here the current knowledge on the impact of temperature on the mosquito flight activity and host-seeking behavior (1); ecology and dispersion (2); as well as its potential effect on the pathogens themselves and how climate can affect the transmission of some of these pathogens (3). Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Open AccessReview
Mosquito Innate Immunity
Received: 28 April 2018 / Revised: 17 June 2018 / Accepted: 18 June 2018 / Published: 8 August 2018
Cited by 2 | PDF Full-text (3476 KB) | HTML Full-text | XML Full-text | Supplementary Files
Abstract
Mosquitoes live under the endless threat of infections from different kinds of pathogens such as bacteria, parasites, and viruses. The mosquito defends itself by employing both physical and physiological barriers that resist the entry of the pathogen and the subsequent establishment of the [...] Read more.
Mosquitoes live under the endless threat of infections from different kinds of pathogens such as bacteria, parasites, and viruses. The mosquito defends itself by employing both physical and physiological barriers that resist the entry of the pathogen and the subsequent establishment of the pathogen within the mosquito. However, if the pathogen does gain entry into the insect, the insect mounts a vigorous innate cellular and humoral immune response against the pathogen, thereby limiting the pathogen’s propagation to nonpathogenic levels. This happens through three major mechanisms: phagocytosis, melanization, and lysis. During these processes, various signaling pathways that engage intense mosquito–pathogen interactions are activated. A critical overview of the mosquito immune system and latest information about the interaction between mosquitoes and pathogens are provided in this review. The conserved, innate immune pathways and specific anti-pathogenic strategies in mosquito midgut, hemolymph, salivary gland, and neural tissues for the control of pathogen propagation are discussed in detail. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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Other

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Open AccessTechnical Note
The Development of Cytogenetic Maps for Malaria Mosquitoes
Received: 15 August 2018 / Revised: 13 September 2018 / Accepted: 13 September 2018 / Published: 17 September 2018
Cited by 1 | PDF Full-text (3290 KB) | HTML Full-text | XML Full-text
Abstract
Anopheline mosquitoes are important vectors of human malaria. Next-generation sequencing opens new opportunities for studies of mosquito genomes to uncover the genetic basis of a Plasmodium transmission. Physical mapping of genome sequences to polytene chromosomes significantly improves reference assemblies. High-resolution cytogenetic maps are [...] Read more.
Anopheline mosquitoes are important vectors of human malaria. Next-generation sequencing opens new opportunities for studies of mosquito genomes to uncover the genetic basis of a Plasmodium transmission. Physical mapping of genome sequences to polytene chromosomes significantly improves reference assemblies. High-resolution cytogenetic maps are essential for anchoring genome sequences to chromosomes as well as for studying breakpoints of chromosome rearrangements and chromatin protein localization. Here we describe a detailed pipeline for the development of high-resolution cytogenetic maps using polytene chromosomes of malaria mosquitoes. We apply this workflow to the refinement of the cytogenetic map developed for Anopheles beklemishevi. Full article
(This article belongs to the Special Issue Integrative Mosquito Biology: From Molecules to Ecosystems)
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