Title: Characterizing seasonal changes in the reproductive activity of Culex mosquitoes throughout the fall, winter, and spring in Ohio
AbstractBackground
Culexmosquitoes are the primary vectors of West Nile virus (WNV) across the USA. Understanding when these vectors are active indicates times when WNV transmission can occur. This study determined the proportion of femaleCulexmosquitoes that were in diapause during the fall and winter and when they terminated diapause and began blood feeding in the spring.
Methods
Mosquitoes were collected from parks using various traps and/or aspirated from culverts in Franklin County, Ohio, from October to mid-May from 2019 to 2022.Culexmosquitoes were morphologically identified to species, and the ovaries of females were dissected to determine their diapause and parity statuses.
Results
By early October 2021, roughly 95% ofCulex pipienscollected in culverts were in diapause and 98% ofCx. erraticuswere in diapause. Furthermore, gravid and blood-fedCulex salinarius,Cx. pipiens, andCx. restuanswere collected in late November in 2019 and 2021 in standard mosquito traps. In the winter of 2021, the proportions of non-diapausingCulexdecreased within culverts. The last non-diapausingCx. erraticuswas collected in late December 2021 while the final non-diapausingCx. pipienswas collected in mid-January 2022, both in culverts. Roughly 50% ofCx. pipiensterminated diapause by mid-March 2022, further supported by our collections of gravid females in late March in all 3 years of mosquito collection. In fact, male mosquitoes ofCx. pipiens,Cx. restuans, andCx. territanswere collected by the 1st week of May in 2022, indicating that multiple species ofCulexproduced a second generation that reached adulthood by this time.
Conclusions
We collected blood-fed and gravidCulexfemales into late November in 2 of the 3 years of our collections, indicating that it might be possible for WNV transmission to occur in late fall in temperate climates like Ohio. The persistence of non-diapausingCx. pipiensandCx. erraticusthroughout December has important implications for the winter survival of WNV vectors and our overall understanding of diapause. Finally, determining whenCulexterminate diapause in the spring may allow us to optimize mosquito management programs and reduce the spread of WNV before it is transmitted to humans.
Females of the Northern house mosquito,Culex pipiens, enter an overwintering dormancy, or diapause, in response to short day lengths and low environmental temperatures that is characterized by small egg follicles and high starvation resistance. During diapause,Culex pipiensMajor Royal Jelly Protein 1 ortholog (CpMRJP1) is upregulated in females ofCx. pipiens. This protein is highly abundant in royal jelly, a substance produced by honey bees (Apis mellifera), that is fed to future queens throughout larval development and induces the queen phenotype (e.g., high reproductive activity and longer lifespan). However, the role of CpMRJP1 inCx. pipiensis unknown.
Methods
We first conducted a phylogenetic analysis to determine how the sequence of CpMRJP1 compares with other species. We then investigated how supplementing the diets of both diapausing and nondiapausing females ofCx. pipienswith royal jelly affects egg follicle length, fat content, protein content, starvation resistance, and metabolic profile.
Results
We found that feeding royal jelly to females reared in long-day, diapause-averting conditions significantly reduced the egg follicle lengths and switched their metabolic profiles to be similar to diapausing females. In contrast, feeding royal jelly to females reared in short-day, diapause-inducing conditions significantly reduced lifespan and switched their metabolic profile to be similar nondiapausing mosquitoes. Moreover, RNAi directed againstCpMRJPIsignificantly increased egg follicle length of short-day reared females, suggesting that these females averted diapause.
Discussion
Taken together, our data show that consuming royal jelly reverses several key seasonal phenotypes ofCx. pipiensand that these responses are likely mediated in part by CpMRJP1.
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.(
, Parasites & Vectors)
AbstractBackground
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.
Methods
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.
Results
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.
Conclusions
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.
Females of the Northern house mosquito, Culex pipiens, enter an overwintering dormancy, or diapause, in response to short day lengths and low environmental temperatures. Diapausing female mosquitoes feed exclusively on sugar-rich products rather than human or animal blood, thereby reducing disease transmission. During diapause, Major Royal Jelly Protein 1 (MRJP1) is upregulated in females of Cx. pipiens. This protein is highly abundant in royal jelly, a substance produced by honey bees (Apis mellifera), that is fed to future queens throughout larval development and stimulates longevity and fecundity. However, the role of MRJP1 in Cx. pipiens is unknown. We investigated how supplementing the diets of both diapausing and nondiapausing females of Cx. pipiens with royal jelly affects gene expression, egg follicle length, fat content, protein content, longevity, and metabolic profile. We found that feeding royal jelly to long day-reared females significantly reduced the egg follicle lengths of females and switched their metabolic profiles to be similar to diapausing females. In contrast, feeding royal jelly to short day-reared females significantly reduced lifespan and switched their metabolic profile to be similar nondiapausing mosquitoes. Moreover, RNAi directed against MRJPI significantly increased egg follicle length of short day-reared females, suggesting that these females averted diapause, although RNAi against MRJP1 also extended the lifespan of short day-reared females. Taken together, our data show that consuming royal jelly reverses the seasonal responses of Cx. pipiens and that these responses are likely mediated in part by MRJP1.
Culex pipiens, the northern house mosquito, is a major vector of West Nile virus. To survive the severe winter, adult mosquitoes enter a diapause programme. Extended lifespan and an increase in lipid storage are key indicators of diapause. Post‐translational modifications to histone proteins impact the expression of genes and have been linked to the lifespan and energy utilisation of numerous insects. Here, we investigated the potential contribution of epigenetic alterations in initiating diapause in this mosquito species. Multiple sequence alignment of H3 sequences from other insect species demonstrates a high conservation of the H3 histone inCx. pipiensthroughout evolution. We then compared the levels of histone methylation in the ovaries and fat body tissues of diapausing and non‐diapausingCx. pipiensusing western blots. Our data indicate that histone methylation levels in the ovaries ofCx. pipiensdo not change during diapause. In contrast, H3K27me2 levels decrease more than twofold in the fat body of diapausing mosquitoes relative to non‐diapausing counterparts. H3K27 methylation plays a crucial role in chromosome activation and inactivation during development in many insect species. This is predominantly governed by polycomb repressor complex 2. Intriguingly, a previous ChIP‐seq study demonstrated that the transcription factor FOXO (Forkhead box O) targets the genes that comprise this complex. In addition, H3K27me2 exhibits dynamic abundance throughout the diapause programme inCx. pipiens, suggesting its potential role in the initial activation of the diapause programme. This study expands our understanding of the relationship between alterations in epigenetic regulation and diapause.
Uelmen, Jr., Johnny A.; Lamcyzk, Bennett; Irwin, Patrick; Bartlett, Dan; Stone, Chris; Mackay, Andrew; Arsenault-Benoit, Arielle; Ryan, Sadie J.; Mutebi, John-Paul; Hamer, Gabriel L.; et al(
, Parasites & Vectors)
AbstractBackground
West Nile virus (WNV), primarily vectored by mosquitoes of the genusCulex, is the most important mosquito-borne pathogen in North America, having infected thousands of humans and countless wildlife since its arrival in the USA in 1999. In locations with dedicated mosquito control programs, surveillance methods often rely on frequent testing of mosquitoes collected in a network of gravid traps (GTs) and CO2-baited light traps (LTs). Traps specifically targeting oviposition-seeking (e.g. GTs) and host-seeking (e.g. LTs) mosquitoes are vulnerable to trap bias, and captured specimens are often damaged, making morphological identification difficult.
Methods
This study leverages an alternative mosquito collection method, the human landing catch (HLC), as a means to compare sampling of potential WNV vectors to traditional trapping methods. Human collectors exposed one limb for 15 min at crepuscular periods (5:00–8:30 am and 6:00–9:30 pm daily, the time whenCulexspecies are most actively host-seeking) at each of 55 study sites in suburban Chicago, Illinois, for two summers (2018 and 2019).
Results
A total of 223 human-seeking mosquitoes were caught by HLC, of which 46 (20.6%) were mosquitoes of genusCulex. Of these 46 collectedCulexspecimens, 34 (73.9%) wereCx. salinarius, a potential WNV vector species not thought to be highly abundant in upper Midwest USA. Per trapping effort, GTs and LTs collected > 7.5-fold the number of individualCulexspecimens than HLC efforts.
Conclusions
The less commonly used HLC method provides important insight into the complement of human-biting mosquitoes in a region with consistent WNV epidemics. This study underscores the value of the HLC collection method as a complementary tool for surveillance to aid in WNV vector species characterization. However, given the added risk to the collector, novel mitigation methods or alternative approaches must be explored to incorporate HLC collections safely and strategically into control programs.
Siperstein, Alden, Pomeroy, Laura W., Robare, Sydney, Sarko, Lucas, Dehus, Hannah, Lowmiller, Taylor, Fyie, Lydia, and Meuti, Megan E. Characterizing seasonal changes in the reproductive activity of Culex mosquitoes throughout the fall, winter, and spring in Ohio. Parasites & Vectors 16.1 Web. doi:10.1186/s13071-023-05806-0.
Siperstein, Alden, Pomeroy, Laura W., Robare, Sydney, Sarko, Lucas, Dehus, Hannah, Lowmiller, Taylor, Fyie, Lydia, & Meuti, Megan E. Characterizing seasonal changes in the reproductive activity of Culex mosquitoes throughout the fall, winter, and spring in Ohio. Parasites & Vectors, 16 (1). https://doi.org/10.1186/s13071-023-05806-0
Siperstein, Alden, Pomeroy, Laura W., Robare, Sydney, Sarko, Lucas, Dehus, Hannah, Lowmiller, Taylor, Fyie, Lydia, and Meuti, Megan E.
"Characterizing seasonal changes in the reproductive activity of Culex mosquitoes throughout the fall, winter, and spring in Ohio". Parasites & Vectors 16 (1). Country unknown/Code not available: Springer Science + Business Media. https://doi.org/10.1186/s13071-023-05806-0.https://par.nsf.gov/biblio/10417541.
@article{osti_10417541,
place = {Country unknown/Code not available},
title = {Characterizing seasonal changes in the reproductive activity of Culex mosquitoes throughout the fall, winter, and spring in Ohio},
url = {https://par.nsf.gov/biblio/10417541},
DOI = {10.1186/s13071-023-05806-0},
abstractNote = {Abstract BackgroundCulexmosquitoes are the primary vectors of West Nile virus (WNV) across the USA. Understanding when these vectors are active indicates times when WNV transmission can occur. This study determined the proportion of femaleCulexmosquitoes that were in diapause during the fall and winter and when they terminated diapause and began blood feeding in the spring. MethodsMosquitoes were collected from parks using various traps and/or aspirated from culverts in Franklin County, Ohio, from October to mid-May from 2019 to 2022.Culexmosquitoes were morphologically identified to species, and the ovaries of females were dissected to determine their diapause and parity statuses. ResultsBy early October 2021, roughly 95% ofCulex pipienscollected in culverts were in diapause and 98% ofCx. erraticuswere in diapause. Furthermore, gravid and blood-fedCulex salinarius,Cx. pipiens, andCx. restuanswere collected in late November in 2019 and 2021 in standard mosquito traps. In the winter of 2021, the proportions of non-diapausingCulexdecreased within culverts. The last non-diapausingCx. erraticuswas collected in late December 2021 while the final non-diapausingCx. pipienswas collected in mid-January 2022, both in culverts. Roughly 50% ofCx. pipiensterminated diapause by mid-March 2022, further supported by our collections of gravid females in late March in all 3 years of mosquito collection. In fact, male mosquitoes ofCx. pipiens,Cx. restuans, andCx. territanswere collected by the 1st week of May in 2022, indicating that multiple species ofCulexproduced a second generation that reached adulthood by this time. ConclusionsWe collected blood-fed and gravidCulexfemales into late November in 2 of the 3 years of our collections, indicating that it might be possible for WNV transmission to occur in late fall in temperate climates like Ohio. The persistence of non-diapausingCx. pipiensandCx. erraticusthroughout December has important implications for the winter survival of WNV vectors and our overall understanding of diapause. Finally, determining whenCulexterminate diapause in the spring may allow us to optimize mosquito management programs and reduce the spread of WNV before it is transmitted to humans. Graphical Abstract},
journal = {Parasites & Vectors},
volume = {16},
number = {1},
publisher = {Springer Science + Business Media},
author = {Siperstein, Alden and Pomeroy, Laura W. and Robare, Sydney and Sarko, Lucas and Dehus, Hannah and Lowmiller, Taylor and Fyie, Lydia and Meuti, Megan E.},
}
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