Plant-mediated effects on mosquito capacity to transmit human malaria

The ecological context in which mosquitoes and malaria parasites interact has received little attention, compared to the genetic and molecular aspects of malaria transmission. Plant nectar and fruits are important for the nutritional ecology of malaria vectors, but how the natural diversity of plant-derived sugar sources affects mosquito competence for malaria parasites is unclear. To test this, we infected Anopheles coluzzi, an important African malaria vector, with sympatric field isolates of Plasmodium falciparum, using direct membrane feeding assays. Through a series of experiments, we then examined the effects of sugar meals from Thevetia neriifolia and Barleria lupilina cuttings that included flowers, and fruit from Lannea microcarpa and Mangifera indica on parasite and mosquito traits that are key for determining the intensity of malaria transmission. We found that the source of plant sugar meal differentially affected infection prevalence and intensity, the development duration of the parasites, as well as the survival and fecundity of the vector. These effects are likely the result of complex interactions between toxic secondary metabolites and the nutritional quality of the plant sugar source, as well as of host resource availability and parasite growth. Using an epidemiological model, we show that plant sugar source can be a significant driver of malaria transmission dynamics, with some plant species exhibiting either transmission-reducing or -enhancing activities

Data from: Plant-mediated effects on mosquito capacity to transmit human malaria

The ecological context in which mosquitoes and malaria parasites interact has received little attention, compared to the genetic and molecular aspects of malaria transmission. Plant nectar and fruits are important for the nutritional ecology of malaria vectors, but how the natural diversity of plant-derived sugar sources affects mosquito competence for malaria parasites is unclear. To test this, we infected Anopheles coluzzi, an important African malaria vector, with sympatric field isolates of Plasmodium falciparum, using direct membrane feeding assays. Through a series of experiments, we then examined the effects of sugar meals from Thevetia neriifolia and Barleria lupilina cuttings that included flowers, and fruit from Lannea microcarpa and Mangifera indica on parasite and mosquito traits that are key for determining the intensity of malaria transmission. We found that the source of plant sugar meal differentially affected infection prevalence and intensity, the development duration of the parasites, as well as the survival and fecundity of the vector. These effects are likely the result of complex interactions between toxic secondary metabolites and the nutritional quality of the plant sugar source, as well as of host resource availability and parasite growth. Using an epidemiological model, we show that plant sugar source can be a significant driver of malaria transmission dynamics, with some plant species exhibiting either transmission-reducing or -enhancing activities

Mosquito aging modulates the development, virulence and transmission potential of pathogens

<p>Host age variation is a striking source of heterogeneity that can shape the evolution and transmission dynamic of pathogens. Compared to vertebrate systems, our understanding of the impact of host age on invertebrate-pathogen interactions remains limited. We examined the influence of mosquito age on key life-history traits driving human malaria transmission. Females of <em>Anopheles coluzzii</em>, a major malaria vector, belonging to three age classes (4, 8, and 12 day-old), were experimentally infected with <em>Plasmodium falciparum</em> field isolates. Our findings revealed reduced competence in 12-day-old mosquitoes, characterized by lower oocyst/sporozoite rates and intensities compared to younger mosquitoes. Despite shorter median longevities in older age classes, infected 12-day-old mosquitoes exhibited improved survival, suggesting that the infection might act as a fountain of youth for older mosquitoes specifically. The timing of sporozoite appearance in the salivary glands remained consistent across mosquito age classes, with an extrinsic incubation period of approximately 13 days. Integrating these results into an epidemiological model revealed a lower vectorial capacity for older mosquitoes compared to younger ones, albeit still substantial due to extended longevity in the presence of infection. Considering age heterogeneity provides valuable insights for ecological and epidemiological studies, informing targeted control strategies to mitigate pathogen transmission.</p><p>Funding provided by: Agence Nationale de la Recherche<br>Crossref Funder Registry ID: https://ror.org/00rbzpz17<br>Award Number: grant no.11-PDOC-006-01</p><p>Funding provided by: Agence Nationale de la Recherche<br>Crossref Funder Registry ID: https://ror.org/00rbzpz17<br>Award Number: grant no.16-CE35-0007</p&gt

Field evidence for manipulation of mosquito host selection by the human malaria parasite, Plasmodium falciparum

International audienceWhether the malaria parasite Plasmodium falciparum can manipulate mosquito host choice in ways that enhance parasite transmission toward humans is unknown. We assessed the influence of P. falciparum on the blood-feeding behaviour of three of its major vectors (Anopheles coluzzii, An. gambiae and An. arabiensis) in Burkina Faso. Host preference assays using odour-baited traps revealed no effect of infection on mosquito long-range anthropophily. However, the identification of the blood meal origin of mosquitoes showed that females carrying sporozoites, the mature transmissible stage of the parasite, displayed a 24% increase in anthropophagy compared to both females harbouring oocysts, the parasite immature stage, and uninfected individuals. Using a mathematical model, we further showed that this increased anthropophagy in infectious females resulted in a 250% increase in parasite transmission potential, everything else being equal. This important epidemiological consequence highlights the importance of vector control tools targeting infectious females

Effect of sugar treatment on the early development of <i>P</i>. <i>falciparum</i>, and on the survival and fecundity of malaria-exposed <i>Anopheles coluzzii</i>.

<p>(a) Infection rate (± 95% CI), expressed as the proportion of mosquitoes exposed to an infectious blood meal and harboring at least one oocyst in their midgut, over 4 replicates and using a total of 7 gametocyte carriers. Numbers in brackets indicate the total number of mosquitoes dissected 7 days post infection (dpi) for each sugar treatment. Different letters above the bars denote statistically significant differences based on multiple pair-wise post-hoc tests. (b) Infection intensity (± se), expressed as the mean number of developing oocysts in the guts of infected females, over 4 replicates and using a total of 7 gametocyte carriers. Numbers in brackets indicate the total number of infected mosquitoes for each sugar treatment. Different letters above the bars denote statistically significant differences based on multiple pair-wise post-hoc tests. (c) Survivorship of malaria-exposed mosquitoes for each sugar treatment over 4 replicates and using a total of 7 gametocyte carriers. Survival was recorded twice a day from 1 to 7 dpi. (d) Egg incidence (± 95% CI) of malaria-exposed mosquitoes, expressed as the proportion of mosquito females carrying fully matured eggs inside their ovaries on 7 dpi for each sugar treatment and infection status.</p

Effect of sugar treatment on the sporozoite index and EIP.

<p>(a) Sporozoite index (± 95% CI), expressed as the proportion of mosquitoes exposed to an infectious blood meal and having disseminated sporozoites in their head/thoraces, over 2 replicates and using a total of 4 gametocyte carriers. Numbers in brackets indicate, for each sugar treatment, the total number of mosquitoes analyzed with PCR on 14 days post infection (dpi). Different letters above the bars denote statistically significant differences based on multiple pair-wise post-hoc tests. (b) Survivorship of malaria-exposed mosquitoes for each sugar treatment over 2 replicates, and using a total of 4 gametocyte carriers. Survival was recorded twice a day from 1 to 14 dpi. (c) Sporozoite index (± 95% CI) over time and using a total of 2 gametocyte carriers. *p<0.05; **p < 0.01, NS: non-significant difference between sugar treatment</p