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1. Not all mosquitoes are created equal: A synthesis of vector competence experiments reinforces virus associations of Australian mosquitoes

   https://doi.org/10.1371/journal.pntd.0010768  

   Kain, Morgan P. ; Skinner, Eloise B. ; Athni, Tejas S. ; Ramirez, Ana L. ; Mordecai, Erin A. ; van den Hurk, Andrew F. ( October 2022 , PLOS Neglected Tropical Diseases)

   Brackney, Doug E. (Ed.)

   The globalization of mosquito-borne arboviral diseases has placed more than half of the human population at risk. Understanding arbovirus ecology, including the role individual mosquito species play in virus transmission cycles, is critical for limiting disease. Canonical virus-vector groupings, such as Aedes - or Culex -associated flaviviruses, have historically been defined using virus detection in field-collected mosquitoes, mosquito feeding patterns, and vector competence, which quantifies the intrinsic ability of a mosquito to become infected with and transmit a virus during a subsequent blood feed. Herein, we quantitatively synthesize data from 68 laboratory-based vector competence studies of 111 mosquito-virus pairings of Australian mosquito species and viruses of public health concern to further substantiate existing canonical vector-virus groupings and quantify variation within these groupings. Our synthesis reinforces current canonical vector-virus groupings but reveals substantial variation within them. While Aedes species were generally the most competent vectors of canonical “ Aedes -associated flaviviruses” (such as dengue, Zika, and yellow fever viruses), there are some notable exceptions; for example, Aedes notoscriptus is an incompetent vector of dengue viruses. Culex spp. were the most competent vectors of many traditionally Culex -associated flaviviruses including West Nile, Japanese encephalitis and Murray Valley encephalitis viruses, although some Aedes spp. are also moderately competent vectors of these viruses. Conversely, many different mosquito genera were associated with the transmission of the arthritogenic alphaviruses, Ross River, Barmah Forest, and chikungunya viruses. We also confirm that vector competence is impacted by multiple barriers to infection and transmission within the mesenteron and salivary glands of the mosquito. Although these barriers represent important bottlenecks, species that were susceptible to infection with a virus were often likely to transmit it. Importantly, this synthesis provides essential information on what species need to be targeted in mosquito control programs. 

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2. Transcriptional response of individual Hawaiian Culex quinquefasciatus mosquitoes to the avian malaria parasite Plasmodium relictum

   https://doi.org/10.1186/s12936-022-04271-x  

   Ferreira, Francisco C. ; Videvall, Elin ; Seidl, Christa M. ; Wagner, Nicole E. ; Kilpatrick, A. Marm ; Fleischer, Robert C. ; Fonseca, Dina M. ( August 2022 , Malaria Journal)

   Plasmodiumparasites that cause bird malaria occur in all continents except Antarctica and are primarily transmitted by mosquitoes in the genusCulex.Culex quinquefasciatus, the mosquito vector of avian malaria in Hawaiʻi, became established in the islands in the 1820s. While the deadly effects of malaria on endemic bird species have been documented for many decades, vector-parasite interactions in avian malaria systems are relatively understudied.

   To evaluate the gene expression response of mosquitoes exposed to aPlasmodiuminfection intensity known to occur naturally in Hawaiʻi, offspring of wild-collected HawaiianCx. quinquefasciatuswere fed on a domestic canary infected with a fresh isolate ofPlasmodium relictumGRW4 from a wild-caught Hawaiian honeycreeper. Control mosquitoes were fed on an uninfected canary. Transcriptomes of five infected and three uninfected individual mosquitoes were sequenced at each of three stages of the parasite life cycle: 24 h post feeding (hpf) during ookinete invasion; 5 days post feeding (dpf) when oocysts are developing; 10 dpf when sporozoites are released and invade the salivary glands.

   Differential gene expression analyses showed that during ookinete invasion (24 hpf), genes related to oxidoreductase activity and galactose catabolism had lower expression levels in infected mosquitoes compared to controls. Oocyst development (5 dpf) was associated with reduced expression of a gene with a predicted innate immune function. At 10 dpf, infected mosquitoes had reduced expression levels of a serine protease inhibitor, and further studies should assess its role as aPlasmodiumagonist inC. quinquefasciatus. Overall, the differential gene expression response of HawaiianCulexexposed to aPlasmodiuminfection intensity known to occur naturally in Hawaiʻi was low, but more pronounced during ookinete invasion.

   This is the first analysis of the transcriptional responses of vectors to malaria parasites in non-mammalian systems. Interestingly, few similarities were found between the response ofCulexinfected with a birdPlasmodiumand those reported inAnophelesinfected with humanPlasmodium. The relatively small transcriptional changes observed in mosquito genes related to immune response and nutrient metabolism support conclusions of low fitness costs often documented in experimental challenges ofCulexwith avianPlasmodium.

    

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3. The midgut epithelium of mosquitoes adjusts cell proliferation and endoreplication to respond to physiological challenges

   https://doi.org/10.1186/s12915-023-01769-x  

   Taracena-Agarwal, M. L. ; Hixson, B. ; Nandakumar, S. ; Girard-Mejia, A. P. ; Chen, R. Y. ; Huot, L. ; Padilla, N. ; Buchon, N. ( January 2024 , BMC Biology)

   Hematophagous mosquitoes transmit many pathogens that cause human diseases. Pathogen acquisition and transmission occur when female mosquitoes blood feed to acquire nutrients for reproduction. The midgut epithelium of mosquitoes serves as the point of entry for transmissible viruses and parasites.

   We studied midgut epithelial dynamics in five major mosquito vector species by quantifying PH3-positive cells (indicative of mitotic proliferation), the incorporation of nucleotide analogs (indicative of DNA synthesis accompanying proliferation and/or endoreplication), and the ploidy (by flow cytometry) of cell populations in the posterior midgut epithelium of adult females. Our results show that the epithelial dynamics of post-emergence maturation and of mature sugar-fed guts were similar in members of theAedes,Culex, andAnophelesgenera. In the first three days post-emergence, ~ 20% of cells in the posterior midgut region of interest incorporated nucleotide analogs, concurrent with both proliferative activity and a broad shift toward higher ploidy. In mature mosquitoes maintained on sugar, an average of 3.5% of cells in the posterior midgut region of interest incorporated nucleotide analogs from five to eight days post-emergence, with a consistent presence of mitotic cells indicating constant cell turnover. Oral bacterial infection triggered a sharp increase in mitosis and nucleotide analog incorporation, suggesting that the mosquito midgut undergoes accelerated cellular turnover in response to damage. Finally, blood feeding resulted in an increase in cell proliferation, but the nature and intensity of the response varied by mosquito species and by blood source (human, bovine, avian or artificial). InAn. gambiae, enterocytes appeared to reenter the cell cycle to increase ploidy after consuming blood from all sources except avian.

   We saw that epithelial proliferation, differentiation, and endoreplication reshape the blood-fed gut to increase ploidy, possibly to facilitate increased metabolic activity. Our results highlight the plasticity of the midgut epithelium in mosquitoes’ physiological responses to distinct challenges.

    

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4. Mixed transmission modes promote persistence of an emerging tick‐borne pathogen

   https://doi.org/10.1002/ecs2.3171  

   Sambado, Samantha ; Salomon, Jordan ; Crews, Arielle ; Swei, Andrea ( June 2020 , Ecosphere)

   Pathogens utilize different modes of transmission to maximize transmission success. In vector‐borne disease systems, both vertical and horizontal modes of transmission are common, but the relative contribution of these modes is not well understood but may be determined by host genetics, physiology, or environmental conditions. This study focuses on an emerging tick‐borne relapsing fever pathogen,Borrelia miyamotoi, that can be transmitted both vertically and horizontally. The enzootic cycle of this pathogen has not been described in the western USA where it was recently found in the tick species,Ixodes pacificus. Our field surveys found that all three life stages ofI. pacificuscarry the pathogen, and therefore, all stages pose some level of disease risk to humans. The prevalence of infection increases with each life stage suggesting that horizontal transmission is important in the persistence of this pathogen in the enzootic cycle. In support of this finding, we found that small mammal hosts that are frequently parasitized by juvenile stages ofI. pacificuswere infected withB. miyamotoiand may therefore function as a source of horizontal transmission and enzootic maintenance of this disease. Our data show that in the western USAB. miyamotoiis maintained in natural populations by both transovarial transmission and transmission from blood meal hosts and that synchronous phenology of juvenile stages ofI. pacificusmay facilitate the transmission dynamics ofB. miyamotoiand other vertically transmitted, vector‐borne pathogens.

    

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5. Scoping review of Culex mosquito life history trait heterogeneity in response to temperature

   https://doi.org/10.1186/s13071-023-05792-3  

   Moser, S. Kane ; Barnard, Martha ; Frantz, Rachel M. ; Spencer, Julie A. ; Rodarte, Katie A. ; Crooker, Isabel K. ; Bartlow, Andrew W. ; Romero-Severson, Ethan ; Manore, Carrie A. ( June 2023 , Parasites & Vectors)

   Mosquitoes in the genusCulexare primary vectors in the US for West Nile virus (WNV) and other arboviruses. Climatic drivers such as temperature have differential effects on species-specific changes in mosquito range, distribution, and abundance, posing challenges for population modeling, disease forecasting, and subsequent public health decisions. Understanding these differences in underlying biological dynamics is crucial in the face of climate change.

   We collected empirical data on thermal response for immature development rate, egg viability, oviposition, survival to adulthood, and adult lifespan forCulex pipiens, Cx. quinquefasciatus, Cx. tarsalis, andCx. restuansfrom existing literature according to the PRISMA scoping review guidelines.

   We observed linear relationships with temperature for development rate and lifespan, and nonlinear relationships for survival and egg viability, with underlying variation between species. Optimal ranges and critical minima and maxima also appeared varied. To illustrate how model output can change with experimental input data from individualCulexspecies, we applied a modified equation for temperature-dependent mosquito type reproduction number for endemic spread of WNV among mosquitoes and observed different effects.

   Current models often input theoretical parameters estimated from a single vector species; we show the need to implement the real-world heterogeneity in thermal response between species and present a useful data resource for researchers working toward that goal.

    

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