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 ◽  
...  

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.

2020 ◽  
Author(s):  
Perrine Marcenac ◽  
W. Robert Shaw ◽  
Evdoxia G. Kakani ◽  
Sara N. Mitchell ◽  
Adam South ◽  
...  

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.


Author(s):  
A. Djènontin ◽  
B. Zogo ◽  
J. Ahlonsou ◽  
A. Bouraima ◽  
M. Ibikounle ◽  
...  

Lagoon areas maintain ideal water conditions for mosquito breeding habitats and are thus environments with high risk of malaria transmission. In Benin, several administrative units, among which the Sô-Ava District, are located in lagoon areas. We conducted entomological surveys in this lagoon district from July 2014 to June 2015, in order to update existing information on biodiversity of mosquitoes, Plasmodium falciparum infection, and insecticide resistance status in malaria vectors. Our survey found that Culex quinquefasciatus and Mansonia africana were the most abundant species, and that Anopheles coluzzii represented the main malaria vector in this area, followed by Anopheles melas. Only Anopheles coluzzii was positive to Plasmudium falcimarum circum sporozoitic protein (4.2 %). An. gambiae s.l. were susceptible to chlorpyrifos-methyl and bendiocarb but resistant to all pyrethroids tested and to pyrimiphos-methyl. The average of kdr allelic frequency from July 2014 to June 2015 was 77.4% and that of ace1 gene was less than 1%. We conclude that Anopheles coluzzii is the main malaria vector in the lagoon area we studied, somewhat contrary to our expectations. However, this malaria vector was resistant to insecticides used for bed net impregnation, even if the resistance level was lower than observed in other parts of Benin.


2022 ◽  
Vol 12 (1) ◽  
Author(s):  
Iliyas Rashid ◽  
Melina Campos ◽  
Travis Collier ◽  
Marc Crepeau ◽  
Allison Weakley ◽  
...  

AbstractUsing high-depth whole genome sequencing of F0 mating pairs and multiple individual F1 offspring, we estimated the nuclear mutation rate per generation in the malaria vectors Anopheles coluzzii and Anopheles stephensi by detecting de novo genetic mutations. A purpose-built computer program was employed to filter actual mutations from a deep background of superficially similar artifacts resulting from read misalignment. Performance of filtering parameters was determined using software-simulated mutations, and the resulting estimate of false negative rate was used to correct final mutation rate estimates. Spontaneous mutation rates by base substitution were estimated at 1.00 × 10−9 (95% confidence interval, 2.06 × 10−10—2.91 × 10−9) and 1.36 × 10−9 (95% confidence interval, 4.42 × 10−10—3.18 × 10−9) per site per generation in A. coluzzii and A. stephensi respectively. Although similar studies have been performed on other insect species including dipterans, this is the first study to empirically measure mutation rates in the important genus Anopheles, and thus provides an estimate of µ that will be of utility for comparative evolutionary genomics, as well as for population genetic analysis of malaria vector mosquito species.


1993 ◽  
Vol 76 (1) ◽  
pp. 32-38 ◽  
Author(s):  
J. Li ◽  
R.A. Wirtz ◽  
I. Schneider ◽  
O.V. Muratova ◽  
T.F. Mccutchan ◽  
...  

2013 ◽  
Vol 12 (1) ◽  
pp. 2 ◽  
Author(s):  
Ibrahim Sangare ◽  
Yannis Michalakis ◽  
Bienvenue Yameogo ◽  
Roch Dabire ◽  
Isabelle Morlais ◽  
...  

Parasitology ◽  
1990 ◽  
Vol 101 (2) ◽  
pp. 193-200 ◽  
Author(s):  
A. M. Feldmann ◽  
P. F. Billingsley ◽  
E. Savelkoul

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.


2013 ◽  
Vol 81 (6) ◽  
pp. 2206-2216 ◽  
Author(s):  
Abbasali Raz ◽  
Navid Dinparast Djadid ◽  
Sedigheh Zakeri

ABSTRACTMalaria is one of the most important infectious diseases in the world, and it has many economic and social impacts on populations, especially in poor countries. Transmission-blocking vaccines (TBVs) are valuable tools for malaria eradication. A study onAnopheles gambiaerevealed that polyclonal antibodies to carboxypeptidase B1 ofA. gambiaecan block sexual parasite development in the mosquito midgut. Hence, it was introduced as a TBV target in regions whereA. gambiaeis the main malaria vector. However, in Iran and neighboring countries as far as China, the main malaria vector isAnopheles stephensi. Also, the genome of this organism has not been sequenced yet. Therefore, in this study, carboxypeptidase B1 ofA. stephensiwas characterized by genomic and proteomic approaches. Furthermore, its expression pattern after ingestion ofPlasmodium falciparumgametocytes and the effect of anti-CPBAs1 antibodies on sexual parasite development were evaluated. Our results revealed that thecpbAs1expression level was increased after ingestion of the mature gametocytes ofP. falciparumand that anti-CPBAs1 directed antibodies could significantly reduce the mosquito infection rate in the test group compared with the control group. Therefore, according to our findings and with respect to the high similarity of carboxypeptidase enzymes between the two main malaria vectors in Africa (A. gambiae) and Asia (A. stephensi) and the presence of other sympatric vectors, CPBAs1 could be introduced as a TBV candidate in regions whereA. stephensiis the main malaria vector, and this will broaden the scope for the potential wider application of CPBAs1 antigen homologs/orthologs.


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