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.
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Potential for urban warming to postpone overwintering dormancy of temperate mosquitoes
Cities are generally hotter than surrounding rural areas due to the Urban Heat Island (UHI) effect. These increases in temperature advance plant and animal phenology, development, and reproduction in the spring. However, research determining how increased temperatures affect the seasonal physiology of animals in the fall has been limited. The Northern house mosquito, Culex pipiens, is abundant in cities and transmits several pathogens including West Nile virus. Females of this species enter a state of developmental arrest, or reproductive diapause, in response to short days and low temperatures during autumn. Diapausing females halt reproduction and blood-feeding, and instead accumulate fat and seek sheltered overwintering sites. We found that exposure to increased temperatures in the lab that mimic the UHI effect induced ovarian development and blood-feeding, and that females exposed to these temperatures were as fecund as non-diapausing mosquitoes. We also found that females exposed to higher temperatures had lower survival rates in winter-like conditions, despite having accumulated equivalent lipid reserves relative to their diapausing congeners. These data suggest that urban warming may inhibit diapause initiation in the autumn, thereby extending the active biting season of temperate mosquitoes.
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- Award ID(s):
- 1944324
- PAR ID:
- 10521084
- Publisher / Repository:
- Journal of Thermal Biology
- Date Published:
- Journal Name:
- Journal of Thermal Biology
- Volume:
- 115
- Issue:
- C
- ISSN:
- 0306-4565
- Page Range / eLocation ID:
- 103594
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Consuming royal jelly alters several phenotypes associated with overwintering dormancy in mosquitoesmore » « less
Introduction 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 pipiens Major 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. pipiens is 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 of
Cx. pipiens with 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 against
CpMRJPI significantly 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 of
Cx. pipiens and that these responses are likely mediated in part by CpMRJP1. -
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Abstract In temperate regions of the United States, female Anopheles mosquitoes respond to low temperatures and short photoperiods by entering an overwintering dormancy or diapause. Diapause in Anopheles results in reduced frequency of blood-feeding and reproductive arrest, indicating a period when pathogen transmission by these mosquitoes is unlikely. However, it is unclear precisely how late into the fall and how early in the spring these mosquitoes are biting, reproducing, and potentially transmitting pathogens. This is further complicated by the lack of clear markers of diapause in Anopheles (e.g., changes in egg follicle length). Our goal was to characterize the seasonal reproductive activity of female Anopheles in central Ohio, United States and evaluate egg follicle length as an indicator of Anopheles diapause. We used traditional mosquito traps and aspirators to collect Anopheles from urban woodlots and culverts, respectively, from late September 2021 through mid-May 2022 in central Ohio. By measuring their egg follicle length, reproductive status, and blood-feeding status, we found that egg follicle length is not a reliable indicator of Anopheles diapause. We also found that a small proportion of An. punctipennis (Say), An. perplexens (Ludlow), and An. quadrimaculatus (Say) continued to bite and reproduce into early November 2021 and that females of these species terminated reproductive dormancy and began biting by mid-March 2022. This period of reproductive activity extends beyond current mosquito surveillance and control in Ohio. Our findings suggest that within temperate regions of North America, Anopheles have the capacity to transmit pathogens throughout the spring, summer, and fall.
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Abstract Background Culex mosquitoes 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 femaleCulex mosquitoes 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.
Culex mosquitoes 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% of
Culex pipiens collected in culverts were in diapause and 98% ofCx. erraticus were in diapause. Furthermore, gravid and blood-fedCulex salinarius ,Cx. pipiens , andCx. restuans were collected in late November in 2019 and 2021 in standard mosquito traps. In the winter of 2021, the proportions of non-diapausingCulex decreased within culverts. The last non-diapausingCx. erraticus was collected in late December 2021 while the final non-diapausingCx. pipiens was collected in mid-January 2022, both in culverts. Roughly 50% ofCx. pipiens terminated 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. territans were collected by the 1st week of May in 2022, indicating that multiple species ofCulex produced a second generation that reached adulthood by this time.Conclusions We collected blood-fed and gravid
Culex females 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. pipiens andCx. erraticus throughout December has important implications for the winter survival of WNV vectors and our overall understanding of diapause. Finally, determining whenCulex terminate 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 -
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Abstract In diapausing mosquitoes, cold tolerance and prolonged lifespan are important features that are crucial for overwintering success. In the mosquito Culex pipiens, we suggest that PDZ domain-containing protein (PDZ) (post synaptic density protein [PSD95], drosophila disc large tumor suppressor [Dlg1], and zonula occludens-1 protein [zo-1]) domain-containing protein is involved with these diapause features for overwintering survival in Culex mosquitoes. The expression level of pdz was significantly higher in diapausing adult females in the early stage in comparison to their nondiapausing counterparts. Suppression of the gene that encodes PDZ by RNA interference significantly decreased actin accumulation in the midgut of early-stage adult diapausing females. Inhibition of pdz also significantly reduced the survivability of diapausing females which indicates that this protein could play a key role in preserving the midgut tissues during early diapause.
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1016/j.jtherbio.2023.103594
