Mosquito – Arbovirus Interactions in Honor of Professor Walter J. Tabachnick

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

Deadline for manuscript submissions: closed (15 December 2018) | Viewed by 50324

Special Issue Editors


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Guest Editor
Florida Medical Entomology Laboratory, Department of Entomology and Nematology, University of Florida, 200 9th St. SE, Vero Beach, FL 32962, USA
Interests: gene expression and regulation; genetic basis of vector competence; mosquito vector – virus interactions; insecticide resistance mechanisms

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Guest Editor
Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI 53706, USA
Interests: mosquito physiology; host-parasite interactions; filarial worms; arboviruses

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Guest Editor
Department of Health Education and Promotion, Environmental Health Science Program, East Carolina University, Greenville, NC 27858, USA
Interests: vector biology; mosquito-virus interactions; vector competence; mosquito control; insecticide resistance

Special Issue Information

Dear Colleagues,

Mosquito vector competence is the ability of a mosquito to be infected with and transmit a pathogen through saliva during blood feeding. The vector competence phenotype is influenced by the environment under which the mosquito develops, microbiome, genetics and many other as yet little understood factors. Interactions between these factors contribute to vector competence. For a mosquito to be a competent vector, the infectious agent must infect the midgut epithelial cells, replicate and escape these barriers, followed by subsequent infection and escape of the salivary glands. Midgut and salivary gland infection and escape barriers can interfere with transmission ability and mosquitoes having these barriers are not efficient vectors. Both midgut and salivary gland barriers are often ascribed as a phenotype of a given mosquito population or species. However, within a cohort of mosquitoes there are usually individuals that are not infected. Additionally, although a mosquito species may be a known vector of an arbovirus, environmental conditions may enhance or suppress virus transmission. Such was the case in studies showing Aedes japonicus and Ae. albopictus capable of transmitting West Nile virus and Culex quinquefasciatus transmitting Zika virus. Thus, the variability seen in vector competence is complex and requires the integration of studies on arbovirus evolution, in the vertebrate hosts and arthropods, and assessment of genes in natural populations of mosquitoes that influence vector competence for arboviruses.

Walter J. Tabachnick is a Professor at the University of Florida’s Florida Medical Entomology Laboratory. Prof. Tabachnick is the (co-)author of 220 publications, including in international journals, with most of the publications cited over 10 times. Due to his expertise in the areas of population genetics and arbovirology, Prof. Tabachnick’s work has been cited over 4,000 times (h-index 35).

In honor of Professor Walter J. Tabachnick and his contribution to the field of arthropod population genetics and arbovirology this special issue ”Mosquito – Arbovirus interactions” welcomes submission of previously unpublished manuscripts from original work or reviews on “Understanding variation in arthropod virus transmission competence”.

Assoc. Prof. Chelsea T. Smartt


Assoc. Prof. Lyric Bartholomay
Assoc. Prof. Stephanie L. Richards
Guest Editors

Manuscript Submission Information

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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.

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Keywords

  • arbovirus
  • transmission
  • mosquito
  • vector competence

Published Papers (9 papers)

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Research

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12 pages, 2553 KiB  
Article
Detection of Yellow Fever Virus in Sylvatic Mosquitoes during Disease Outbreaks of 2017–2018 in Minas Gerais State, Brazil
by Guilherme Garcia Pinheiro, Marcele Neves Rocha, Maria Angélica de Oliveira, Luciano Andrade Moreira and José Dilermando Andrade Filho
Insects 2019, 10(5), 136; https://doi.org/10.3390/insects10050136 - 10 May 2019
Cited by 26 | Viewed by 4133
Abstract
Brazil has experienced several arbovirus outbreaks in recent years, among which yellow fever stands out. The state of Minas Gerais faced outbreaks of sylvatic yellow fever in 2017 and 2018, with 1002 confirmed cases and 340 deaths. This work presents the results of [...] Read more.
Brazil has experienced several arbovirus outbreaks in recent years, among which yellow fever stands out. The state of Minas Gerais faced outbreaks of sylvatic yellow fever in 2017 and 2018, with 1002 confirmed cases and 340 deaths. This work presents the results of survey efforts to detect the yellow fever virus in mosquitoes from two conservation areas in the metropolitan region of Belo Horizonte, Brazil. A total of 867 mosquitoes of 20 species were collected between September 2017 and May 2018, the most abundant being Psorophora (Janthinosoma) ferox (von Humboldt, 1819) (31.3%), Limatus durhamii Theobald, 1901 (19.1%) and Haemagogus (Haemagogus) janthinomys Dyar, 1921 (18.2%). Total RNA was extracted from the mosquitoes for real-time PCR analysis for yellow fever, chikungunya, mayaro, Zika and dengue viruses. The yellow fever infection rate was 8.2% for Hg. janthinomys (13 mosquitoes), which is the main vector of sylvatic yellow fever in Brazil. In addition to surveying the mosquito fauna of these conservation units, this work demonstrates the importance of monitoring the circulation of viruses near large urban centers. Full article
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17 pages, 761 KiB  
Article
Homologs of Human Dengue-Resistance Genes, FKBP1B and ATCAY, Confer Antiviral Resistance in Aedes aegypti Mosquitoes
by Seokyoung Kang, Dongyoung Shin, Derrick K. Mathias, Berlin Londono-Renteria, Mi Young Noh, Tonya M. Colpitts, Rhoel R. Dinglasan, Yeon Soo Han and Young S. Hong
Insects 2019, 10(2), 46; https://doi.org/10.3390/insects10020046 - 02 Feb 2019
Cited by 4 | Viewed by 3751
Abstract
Dengue virus (DENV) is transmitted by mosquitoes and is a major public health concern. The study of innate mosquito defense mechanisms against DENV have revealed crucial roles for the Toll, Imd, JAK-STAT, and RNAi pathways in mediating DENV in the mosquito. Often overlooked [...] Read more.
Dengue virus (DENV) is transmitted by mosquitoes and is a major public health concern. The study of innate mosquito defense mechanisms against DENV have revealed crucial roles for the Toll, Imd, JAK-STAT, and RNAi pathways in mediating DENV in the mosquito. Often overlooked in such studies is the role of intrinsic cellular defense mechanisms that we hypothesize to work in concert with the classical immune pathways to affect organismal defense. Our understanding of the molecular interaction of DENV with mosquito host cells is limited, and we propose to expand upon the recent results from a genome-scale, small interfering RNA (siRNA)-based study that identified mammalian host proteins associated with resistance to dengue/West Nile virus (DENV/WNV) infection. The study identified 22 human DENV/WNV resistance genes (DVR), and we hypothesized that a subset would be functionally conserved in Aedes aegypti mosquitoes, imparting cellular defense against flaviviruses in this species. We identified 12 homologs of 22 human DVR genes in the Ae. aegypti genome. To evaluate their possible role in cellular resistance/antiviral defense against DENV, we used siRNA silencing targeted against each of the 12 homologs in an Ae. aegypti cell line (Aag2) infected with DENV2 and identified that silencing of the two candidates, AeFKBP1 and AeATCAY, homologs of human FKBP1B and ATCAY, were associated with a viral increase. We then used dsRNA to silence each of the two genes in adult mosquitoes to validate the observed antiviral functions in vivo. Depletion of AeFKBP1 or AeATCAY increased viral dissemination through the mosquito at 14 days post-infection. Our results demonstrated that AeFKBP1 and AeATCAY mediate resistance to DENV akin to what has been described for their homologs in humans. AeFKBP1 and AeATCAY provide a rare opportunity to elucidate a DENV-resistance mechanism that may be evolutionarily conserved between humans and Ae. aegypti. Full article
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14 pages, 2712 KiB  
Article
Analysis of Salivary Glands and Saliva from Aedes albopictus and Aedes aegypti Infected with Chikungunya Viruses
by Irma Sanchez-Vargas, Laura C. Harrington, William C. Black IV and Ken E. Olson
Insects 2019, 10(2), 39; https://doi.org/10.3390/insects10020039 - 01 Feb 2019
Cited by 25 | Viewed by 4994
Abstract
Chikungunya virus (CHIKV) is a medically important mosquito-borne virus transmitted to humans by infected Aedes (Stegomyia) species. In 2013–2014, Ae. aegypti transmitted CHIKV to humans in the Caribbean and in 2005–2006, Ae. albopictus transmitted CHIKV on La Réunion Island (Indian Ocean [...] Read more.
Chikungunya virus (CHIKV) is a medically important mosquito-borne virus transmitted to humans by infected Aedes (Stegomyia) species. In 2013–2014, Ae. aegypti transmitted CHIKV to humans in the Caribbean and in 2005–2006, Ae. albopictus transmitted CHIKV on La Réunion Island (Indian Ocean basin). CHIKV LR2006 OPY1 from the La Réunion epidemic was associated with a mutation (E1:A226V) in the viral E1 glycoprotein that enhanced CHIKV transmission by Ae. albopictus. CHIKV R99659 from the Caribbean outbreak did not have the E1:A226V mutation. Here, we analyzed the salivary glands and saliva of Ae. albopictus strains from New Jersey, Florida, Louisiana and La Réunion after infection with each virus to determine their transmission potential. We infected the Ae. albopictus strains with blood meals containing 3–7 × 107 PFU/mL of each virus and analyzed the mosquitoes nine days later to maximize infection of their salivary glands. All four Ae. albopictus strains were highly susceptible to LR2006 OPY1 and R99659 viruses and their CHIKV disseminated infection rates (DIR) were statistically similar (p = 0.3916). The transmission efficiency rate (TER) was significantly lower for R99659 virus compared to LR2006 OPY1 virus in all Ae. albopictus strains and Ae. aegypti (Poza Rica) (p = 0.012) suggesting a salivary gland exit barrier to R99659 virus not seen with LR2006 OPY1 infections. If introduced, LR2006 OPY1 virus poses an increased risk of transmission by both Aedes species in the western hemisphere. Full article
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11 pages, 697 KiB  
Article
Genome-Wide Transcriptome Profiling Reveals Genes Associated with Meiotic Drive System of Aedes aegypti
by Dongyoung Shin, Susanta K. Behura and David W. Severson
Insects 2019, 10(1), 25; https://doi.org/10.3390/insects10010025 - 10 Jan 2019
Cited by 2 | Viewed by 3422
Abstract
Aedes aegypti is an important mosquito vector of several arboviruses, including dengue, yellow fever, Zika, and Chikungunya, which cause significant human morbidity and mortality globally. In certain populations of this mosquito, a native meiotic drive system causes abnormal spermatogenesis that results in highly [...] Read more.
Aedes aegypti is an important mosquito vector of several arboviruses, including dengue, yellow fever, Zika, and Chikungunya, which cause significant human morbidity and mortality globally. In certain populations of this mosquito, a native meiotic drive system causes abnormal spermatogenesis that results in highly male-biased progenies from some matings. Although the basic genetics and cytogenetics of the drive mechanism were elucidated, very little is known on a transcriptome level about how the meiotic drive phenotype is expressed in individual males. To address this question, we conducted a whole-genome microarray expression study of testes from a meiotic-drive-carrying strain (T37) in comparison with testes from a non-drive-carrying strain (RED). Based on bioinformatics analyses of the microarray data, we identified 209 genes associated with the meiotic drive phenotype that were significantly differentially expressed between the two strains. K-means cluster analysis revealed nine clusters, in which genes upregulated in T37 testes were assigned to five clusters and genes downregulated in T37 testes were assigned to four clusters. Our data further revealed that genes related to protein translation, phosphorylation, and binding, as well as to G-protein-coupled receptor (GPCR) and peptidase activities, are differentially upregulated in testes from males with the meiotic drive genotype. Based on pathway analysis of these differentially expressed genes, it was observed that the glycosylphosphatidylinositol (GPI)-anchor biosynthesis pathway may play a role in the meiotic drive system. Overall, this investigation enhances our understanding of whole-genome gene expression associated with the meiotic drive system in Ae. aegypti. Full article
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12 pages, 1767 KiB  
Article
Sequential Infection of Aedes aegypti Mosquitoes with Chikungunya Virus and Zika Virus Enhances Early Zika Virus Transmission
by Tereza Magalhaes, Alexis Robison, Michael C. Young, William C. Black, Brian D. Foy, Gregory D. Ebel and Claudia Rückert
Insects 2018, 9(4), 177; https://doi.org/10.3390/insects9040177 - 01 Dec 2018
Cited by 30 | Viewed by 5508
Abstract
In urban settings, chikungunya, Zika, and dengue viruses are transmitted by Aedes aegypti mosquitoes. Since these viruses co-circulate in several regions, coinfection in humans and vectors may occur, and human coinfections have been frequently reported. Yet, little is known about the molecular aspects [...] Read more.
In urban settings, chikungunya, Zika, and dengue viruses are transmitted by Aedes aegypti mosquitoes. Since these viruses co-circulate in several regions, coinfection in humans and vectors may occur, and human coinfections have been frequently reported. Yet, little is known about the molecular aspects of virus interactions within hosts and how they contribute to arbovirus transmission dynamics. We have previously shown that Aedes aegypti exposed to chikungunya and Zika viruses in the same blood meal can become coinfected and transmit both viruses simultaneously. However, mosquitoes may also become coinfected by multiple, sequential feeds on single infected hosts. Therefore, we tested whether sequential infection with chikungunya and Zika viruses impacts mosquito vector competence. We exposed Ae. aegypti mosquitoes first to one virus and 7 days later to the other virus and compared infection, dissemination, and transmission rates between sequentially and single infected groups. We found that coinfection rates were high after sequential exposure and that mosquitoes were able to co-transmit both viruses. Surprisingly, chikungunya virus coinfection enhanced Zika virus transmission 7 days after the second blood meal. Our data demonstrate heterologous arbovirus synergism within mosquitoes, by unknown mechanisms, leading to enhancement of transmission under certain conditions. Full article
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Review

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16 pages, 696 KiB  
Review
Vesicular Stomatitis Virus Transmission: A Comparison of Incriminated Vectors
by Paula Rozo-Lopez, Barbara S. Drolet and Berlin Londoño-Renteria
Insects 2018, 9(4), 190; https://doi.org/10.3390/insects9040190 - 11 Dec 2018
Cited by 47 | Viewed by 10336
Abstract
Vesicular stomatitis (VS) is a viral disease of veterinary importance, enzootic in tropical and subtropical regions of the Americas. In the U.S., VS produces devastating economic losses, particularly in the southwestern states where the outbreaks display an occurrence pattern of 10-year intervals. To [...] Read more.
Vesicular stomatitis (VS) is a viral disease of veterinary importance, enzootic in tropical and subtropical regions of the Americas. In the U.S., VS produces devastating economic losses, particularly in the southwestern states where the outbreaks display an occurrence pattern of 10-year intervals. To date, the mechanisms of the geographic spread and maintenance cycles during epizootics remain unclear. This is due, in part, to the fact that VS epidemiology has a complex of variables to consider, including a broad range of vertebrate hosts, multiple routes of transmission, and an extensive diversity of suspected vector species acting as both mechanical and biological vectors. Infection and viral progression within vector species are highly influenced by virus serotype, as well as environmental factors, including temperature and seasonality; however, the mechanisms of viral transmission, including non-conventional pathways, are yet to be fully studied. Here, we review VS epidemiology and transmission mechanisms, with comparisons of transmission evidence for the four most incriminated hematophagous dipteran taxa: Aedes mosquitoes, Lutzomyia sand flies, Simulium black flies, and Culicoides biting midges. Full article
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21 pages, 783 KiB  
Review
The Ecological Significance and Implications of Transovarial Transmission among the Vector-Borne Bunyaviruses: A Review
by Nicholas A. Bergren and Rebekah C. Kading
Insects 2018, 9(4), 173; https://doi.org/10.3390/insects9040173 - 27 Nov 2018
Cited by 21 | Viewed by 7565
Abstract
Transovarial transmission (TOT) is a widespread and efficient process through which pathogens can be passed between generations of arthropod vectors. Many species within the order Bunyavirales utilize TOT as a means of persisting within the environment when classical horizontal transmission is not possible [...] Read more.
Transovarial transmission (TOT) is a widespread and efficient process through which pathogens can be passed between generations of arthropod vectors. Many species within the order Bunyavirales utilize TOT as a means of persisting within the environment when classical horizontal transmission is not possible due to ecological constraints. The purpose of this review is to summarize previous findings regarding the ecological significance of TOT among viruses in the order Bunyavirales and identify the gaps in knowledge regarding this important mechanism of arboviral maintenance. Full article
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Other

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8 pages, 653 KiB  
Brief Report
Larval Exposure to the Bacterial Insecticide Bti Enhances Dengue Virus Susceptibility of Adult Aedes aegypti Mosquitoes
by Isabelle Moltini-Conclois, Renaud Stalinski, Guillaume Tetreau, Laurence Després and Louis Lambrechts
Insects 2018, 9(4), 193; https://doi.org/10.3390/insects9040193 - 14 Dec 2018
Cited by 22 | Viewed by 4000
Abstract
Understanding the interactions between pathogens sharing the same host can be complicated for holometabolous animals when larval and adult stages are exposed to distinct pathogens. In medically important insect vectors, the effect of pathogen exposure at the larval stage may influence susceptibility to [...] Read more.
Understanding the interactions between pathogens sharing the same host can be complicated for holometabolous animals when larval and adult stages are exposed to distinct pathogens. In medically important insect vectors, the effect of pathogen exposure at the larval stage may influence susceptibility to human pathogens at the adult stage. We addressed this hypothesis in the mosquito Aedes aegypti, a major vector of arthropod-borne viruses (arboviruses), such as the dengue virus (DENV) and the chikungunya virus (CHIKV). We experimentally assessed the consequences of sub-lethal exposure to the bacterial pathogen Bacillus thuringiensis subsp. israelensis (Bti), during larval development, on arbovirus susceptibility at the adult stage in three Ae. aegypti strains that differ in their genetic resistance to Bti. We found that larval exposure to Bti significantly increased DENV susceptibility, but not CHIKV susceptibility, in the Bti-resistant strains. However, there was no major difference in the baseline arbovirus susceptibility between the Bti-resistant strains and their Bti-susceptible parental strain. Although the generality of our results remains to be tested with additional arbovirus strains, this study supports the idea that the outcome of an infection by a pathogen depends on other pathogens sharing the same host even when they do not affect the same life stage of the host. Our findings may also have implications for Bti as a mosquito biocontrol agent, indicating that the sub-optimal Bti efficacy may have counter-productive effects by increasing vector competence, at least for some combinations of arbovirus and mosquito strains. Full article
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15 pages, 3388 KiB  
Concept Paper
Genetic Variation in Insect Vectors: Death of Typology?
by Jeffrey R. Powell
Insects 2018, 9(4), 139; https://doi.org/10.3390/insects9040139 - 11 Oct 2018
Cited by 20 | Viewed by 5562
Abstract
The issue of typological versus population thinking in biology is briefly introduced and defined. It is then emphasized how population thinking is most relevant and useful in vector biology. Three points are made: (1) Vectors, as they exist in nature, are genetically very [...] Read more.
The issue of typological versus population thinking in biology is briefly introduced and defined. It is then emphasized how population thinking is most relevant and useful in vector biology. Three points are made: (1) Vectors, as they exist in nature, are genetically very heterogeneous. (2) Four examples of how this is relevant in vector biology research are presented: Understanding variation in vector competence, GWAS, identifying the origin of new introductions of invasive species, and resistance to inbreeding. (3) The existence of high levels of vector genetic heterogeneity can lead to failure of some approaches to vector control, e.g., use of insecticides and release of sterile males (SIT). On the other hand, vector genetic heterogeneity can be harnessed in a vector control program based on selection for refractoriness. Full article
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