scholarly journals A mating-induced reproductive gene promotes Anopheles tolerance to Plasmodium falciparum infection

2020 ◽  
Author(s):  
Perrine Marcenac ◽  
W. Robert Shaw ◽  
Evdoxia G. Kakani ◽  
Sara N. Mitchell ◽  
Adam South ◽  
...  
Keyword(s):  
Plasmodium Falciparum ◽  
Anopheles Gambiae ◽  
Anopheles Stephensi ◽  
Steroid Hormone ◽  
Parasite Development ◽  
Anopheles Coluzzii ◽  
Reproductive Costs ◽  
Fitness Costs ◽  
Mating Status ◽  
Human Malaria

AbstractAnopheles mosquitoes have transmitted Plasmodium parasites for millions of years, yet it remains unclear whether they suffer fitness costs to infection. Here we report that the fecundity of virgin and mated females of two important vectors—Anopheles gambiae and Anopheles stephensi—is not affected by infection with Plasmodium falciparum, demonstrating that these human malaria parasites do not inflict reproductive costs to their natural mosquito hosts. Additionally, parasite development is not impacted by mating status. However, in field studies using different P. falciparum isolates in Anopheles coluzzii, we find that Mating-Induced Stimulator of Oogenesis (MISO), a female reproductive gene strongly induced after mating by the sexual transfer of the steroid hormone 20-hydroxyecdysone (20E), protects females from incurring fecundity costs to infection. MISO-silenced females produce fewer eggs as they become increasingly infected with P. falciparum, while parasite development is not impacted by this gene silencing. Interestingly, previous work had shown that sexual transfer of 20E has specifically evolved in Cellia species of the Anopheles genus, driving the co-adaptation of MISO. Our data therefore suggest that evolution of male-female sexual interactions may have promoted Anopheles tolerance to P. falciparum infection in the Cellia subgenus, which comprises the most important malaria vectors.Author summaryPlasmodium falciparum, the deadliest form of human malaria, is transmitted when female Anopheles mosquitoes bite people and take a blood meal in order to develop eggs. To date, it is still poorly understood whether Anopheles mosquitoes that get infected with P. falciparum suffer fitness costs. Here, we find that the number of eggs produced by Anopheles gambiae and Anopheles stephensi females is not affected by P. falciparum infection, and that the mating status of the mosquitoes does not impact the parasite. However, in field experiments infecting a related species, Anopheles coluzzii, with P. falciparum using blood from donors in Burkina Faso, we find that interfering with the expression of a gene normally triggered by the sexual transfer of the steroid hormone 20-hydroxyecdysone induces increasing costs to egg development as females become more infected with P. falciparum, with no impacts on the parasite. The results of our study suggest that pathways triggered by mating may help Anopheles prevent reproductive costs associated with P. falciparum infection, providing new insights into evolutionary strategies adopted by anophelines in the face of a longstanding association with Plasmodium parasites.

scholarly journals A mating-induced reproductive gene promotes Anopheles tolerance to Plasmodium falciparum infection

2020 ◽  
Vol 16 (12) ◽  
pp. e1008908
Author(s):  
Perrine Marcenac ◽  
W. Robert Shaw ◽  
Evdoxia G. Kakani ◽  
Sara N. Mitchell ◽  
Adam South ◽  
...  
Keyword(s):  
Plasmodium Falciparum ◽  
Anopheles Stephensi ◽  
Steroid Hormone ◽  
Field Studies ◽  
Falciparum Infection ◽  
Malaria Vectors ◽  
Parasite Development ◽  
Anopheles Coluzzii ◽  
Fitness Costs ◽  
Mating Status

Anopheles mosquitoes have transmitted Plasmodium parasites for millions of years, yet it remains unclear whether they suffer fitness costs to infection. Here we report that the fecundity of virgin and mated females of two important vectors—Anopheles gambiae and Anopheles stephensi—is not affected by infection with Plasmodium falciparum, demonstrating that these human malaria parasites do not inflict this reproductive cost on their natural mosquito hosts. Additionally, parasite development is not impacted by mating status. However, in field studies using different P. falciparum isolates in Anopheles coluzzii, we find that Mating-Induced Stimulator of Oogenesis (MISO), a female reproductive gene strongly induced after mating by the sexual transfer of the steroid hormone 20-hydroxyecdysone (20E), protects females from incurring fecundity costs to infection. MISO-silenced females produce fewer eggs as they become increasingly infected with P. falciparum, while parasite development is not impacted by this gene silencing. Interestingly, previous work had shown that sexual transfer of 20E has specifically evolved in Cellia species of the Anopheles genus, driving the co-adaptation of MISO. Our data therefore suggest that evolution of male-female sexual interactions may have promoted Anopheles tolerance to P. falciparum infection in the Cellia subgenus, which comprises the most important malaria vectors.

scholarly journals Effect of naturally occurring Wolbachia in Anopheles gambiae s.l. mosquitoes from Mali on Plasmodium falciparum malaria transmission

2017 ◽  
Vol 114 (47) ◽  
pp. 12566-12571 ◽  
Author(s):  
Fabio M. Gomes ◽  
Bretta L. Hixson ◽  
Miles D. W. Tyner ◽  
Jose Luis Ramirez ◽  
Gaspar E. Canepa ◽  
...  
Keyword(s):  
Plasmodium Falciparum ◽  
Anopheles Gambiae ◽  
Malaria Transmission ◽  
Deleterious Effect ◽  
Plasmodium Falciparum Malaria ◽  
Anopheles Coluzzii ◽  
Naturally Occurring ◽  
Anopheles Gambiae S.L ◽  
Cat Fleas ◽  
Sporozoite Infection

A naturally occurring Wolbachia strain (wAnga-Mali) was identified in mosquitoes of the Anopheles gambiae complex collected in the Malian villages of Dangassa and Kenieroba. Phylogenetic analysis of the nucleotide sequence of two 16S rRNA regions showed that wAnga-Mali clusters with Wolbachia strains from supergroup A and has the highest homology to a Wolbachia strain isolated from cat fleas (Ctenocephalides). wAnga-Mali is different from two Wolbachia strains previously reported in A. gambiae from Burkina Faso (wAnga_VK5_STP and wAnga_VK5_3.1a). Quantitative analysis of Wolbachia and Plasmodium sporozoite infection in field-collected mosquitoes indicates that the prevalence and intensity of Plasmodium falciparum sporozoite infection is significantly lower in Wolbachia-infected females. The presence of Wolbachia in females from a laboratory Anopheles coluzzii (A. gambiae, M form) colony experimentally infected with P. falciparum (NF54 strain) gametocyte cultures slightly enhanced oocyst infection. However, Wolbachia infection significantly reduced the prevalence and intensity of sporozoite infection, as observed in the field. This indicates that wAnga-Mali infection does not limit early stages of Plasmodium infection in the mosquito, but it has a strong deleterious effect on sporozoites and reduces malaria transmission.

scholarly journals Contrasting effects of the alkaloid ricinine on the capacity of Anopheles gambiae s.l. to transmit Plasmodium falciparum

2021 ◽  
Author(s):  
Domonbabele François de Sales Hien ◽  
Prisca S. L. Paré ◽  
Amanda Cooper ◽  
Benjamin K. Koama ◽  
Edwige Guissou ◽  
...  
Keyword(s):  
Growth Rate ◽  
Plasmodium Falciparum ◽  
Anopheles Gambiae ◽  
Ricinus Communis ◽  
Control Agent ◽  
Phenotypic Traits ◽  
Anopheles Coluzzii ◽  
Vector Borne Diseases ◽  
Anopheles Gambiae S.L ◽  
The Impact

Abstract Background: Besides feeding on blood, females of the malaria vector Anopheles gambiae s.l. readily feed on natural sources of plant sugars. The impact of toxic secondary phytochemicals contained in plant-derived sugars on mosquito physiology and on the development of Plasmodium parasites remains elusive. The focus of this study was to explore the influence of the alkaloid ricinine, found in the nectar of the castorbean Ricinus communis, on the mosquito ability to transmit Plasmodium falciparum. Methods: Females of Anopheles gambiae and its sibling species Anopheles coluzzii were exposed to ricinine through sugar feeding assays to assess the effect of this phytochemical on mosquito survival, the level of P. falciparum infection, and the growth rate of the parasite. Results: Ricinine induced a significant reduction in the longevity of both Anopheles species. Ricinine caused acceleration in the parasite growth rate with an earlier invasion of the salivary glands in both species. At a concentration of 0.04 g l-1 in An. coluzzii, ricinine had no effect on mosquito infection, while 0.08 g l-1 ricinine-5% glucose solution induced a 14% increase in An. gambiae infection rate. Conclusions: Overall, our findings reveal that consumption of certain nectar phytochemicals can have unsuspected and contrasting effects on key phenotypic traits that govern the intensity of malaria transmission. Further studies will be required before concluding on the putative role of ricinine as a novel control agent, including the development of ricinine-based toxic and transmission-blocking sugar baits. Testing other secondary phytochemicals in plant nectar will provide a broader understanding of the impact, which plants can have on the transmission of vector-borne diseases.

Quantitation of Plasmodium falciparum Sporozoites Transmitted in Vitro by Experimentally Infected Anopheles gambiae and Anopheles stephensi

1991 ◽  
Vol 44 (5) ◽  
pp. 564-570 ◽  
Author(s):  
John C. Beier ◽  
Jefferson A. Vaughan ◽  
Jonathan R. Davis ◽  
Magda S. Beier ◽  
Bruce H. Noden
Keyword(s):  
Plasmodium Falciparum ◽  
Anopheles Gambiae ◽  
Anopheles Stephensi

Plasmodium falciparum: Stage-Specific Ribosomal RNA as a Potential Target for Monitoring Parasite Development in Anopheles stephensi

1993 ◽  
Vol 76 (1) ◽  
pp. 32-38 ◽  
Author(s):  
J. Li ◽  
R.A. Wirtz ◽  
I. Schneider ◽  
O.V. Muratova ◽  
T.F. Mccutchan ◽  
...  
Keyword(s):  
Plasmodium Falciparum ◽  
Ribosomal Rna ◽  
Anopheles Stephensi ◽  
Parasite Development ◽  
Potential Target

Bloodmeal digestion by strains of Anopheles stephensi Liston (Diptera: Culicidae) of differing susceptibility to Plasmodium falciparum

Parasitology ◽  
1990 ◽  
Vol 101 (2) ◽  
pp. 193-200 ◽  
Author(s):  
A. M. Feldmann ◽  
P. F. Billingsley ◽  
E. Savelkoul
Keyword(s):  
Plasmodium Falciparum ◽  
Anopheles Stephensi ◽  
Feeding Activity ◽  
Parasite Development ◽  
Aminopeptidase Activity ◽  
Total Protein Content ◽  
Trypsin Activity ◽  
Blood Digestion ◽  
Susceptibility To Infection ◽  
Post Feeding

Blood digestion was studied in strains of Anopheles stephensi which had been genetically selected for either refractoriness or susceptibility to infection by Plasmodium falciparum. Females of the refractory Pb3—9a strain ingested more blood than selected (Sda-500) and unselected (Punjab) susceptible females and began to degrade the haemoglobin soon after feeding. In susceptible females, haemoglobin degradation started only after a significant post-feeding lag period. Total protein content of the midgut after the bloodmeal was correspondingly higher for refractory than for susceptible females, but absolute and relative rates of protein degradation were not significantly different between the different mosquito strains. Bloodmeal induction of midgut trypsin activity and the maximal trypsin activity were the same for the different strains. The residual aminopeptidase activity and its relative post-feeding activity (enzyme units per midgut) were significantly higher in refractory females. However, when converting to specific aminopeptidase activity, no differences between strains were evident. The results indicate that both the early initiation of haemoglobin degradation and higher aminopeptidase activity in the Pb3—9a refractory strain are important in the limitation of parasite development within the mosquito midgut, whereas trypsin plays no role in this process.

scholarly journals Exploring the lower thermal limits for transmission of human malaria, Plasmodium falciparum

2019 ◽  
Author(s):  
Jessica L. Waite ◽  
Eunho Suh ◽  
Penelope A. Lynch ◽  
Matthew B. Thomas
Keyword(s):  
Plasmodium Falciparum ◽  
Anopheles Stephensi ◽  
Parasite Development ◽  
Temperature Dependent ◽  
Single Degree ◽  
Complete Development ◽  
Thermal Limits ◽  
Degree Day ◽  
Extrinsic Incubation Period ◽  
Impacts Of Climate Change

AbstractThe rate of malaria transmission is strongly determined by parasite development time in the mosquito, known as the extrinsic incubation period (EIP), since the quicker parasites develop, the greater the chance that the vector will survive long enough for the parasite to complete development and be transmitted. EIP is known to be temperature dependent but this relationship is surprisingly poorly characterized. There is a single degree-day model for EIP of Plasmodium falciparum that derives from a limited number of poorly controlled studies conducted almost a century ago. Here, we show that the established degree-day model greatly underestimates the rate of development of P. falciparum in both Anopheles stephensi and An. gambiae mosquitoes at temperatures in the range of 17-20°C. We also show that realistic daily temperature fluctuation further speeds parasite development. These novel results challenge one of the longest standing models in malaria biology and have potentially important implications for understanding the impacts of climate change.

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