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Gene expression divergence between malaria vector sibling species Anopheles gambiae and An. coluzzii from rural and urban Yaounde Cameroon.

ABSTRACT: Divergent selection based on aquatic larval ecology is a likely factor in the recent isolation of two broadly sympatric and morphologically identical African mosquito species, the malaria vectors Anopheles gambiae and An. coluzzii. Population-based genome scans have revealed numerous candidate regions of recent positive selection, but have provided few clues as to the genetic mechanisms underlying behavioural and physiological divergence between the two species, phenotypes which themselves remain obscure. To uncover possible genetic mechanisms, we compared global transcriptional profiles of natural and experimental populations using gene-based microarrays. Larvae were sampled as second and fourth instars from natural populations in and around the city of Yaoundé, capital of Cameroon, where the two species segregate along a gradient of urbanization. Functional enrichment analysis of differentially expressed genes revealed that An. coluzzii--the species that breeds in more stable, biotically complex and potentially polluted urban water bodies--overexpresses genes implicated in detoxification and immunity relative to An. gambiae, which breeds in more ephemeral and relatively depauperate pools and puddles in suburbs and rural areas. Moreover, our data suggest that such overexpression by An. coluzzii is not a transient result of induction by xenobiotics in the larval habitat, but an inherent and presumably adaptive response to repeatedly encountered environmental stressors. Finally, we find no significant overlap between the differentially expressed loci and previously identified genomic regions of recent positive selection, suggesting that transcriptome divergence is regulated by trans-acting factors rather than cis-acting elements.

SUBMITTER: Cassone BJ

PROVIDER: S-EPMC4034741 | biostudies-literature | 2014 May

REPOSITORIES: biostudies-literature

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Gene expression divergence between malaria vector sibling species Anopheles gambiae and An. coluzzii from rural and urban Yaoundé Cameroon.

Cassone Bryan J BJ Kamdem Colince C Cheng Changde C Tan John C JC Hahn Matthew W MW Costantini Carlo C Besansky Nora J NJ

Molecular ecology 20140411 9

Divergent selection based on aquatic larval ecology is a likely factor in the recent isolation of two broadly sympatric and morphologically identical African mosquito species, the malaria vectors Anopheles gambiae and An. coluzzii. Population-based genome scans have revealed numerous candidate regions of recent positive selection, but have provided few clues as to the genetic mechanisms underlying behavioural and physiological divergence between the two species, phenotypes which themselves remai ...[more]

PMID: 24673723

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Project description:BACKGROUND:The rapid and unplanned urbanization of African cities is considered to increase the risk of urban malaria transmission. The present study objective was to assess factors influencing the spatio-temporal distribution of Anopheles gambiae s.l. larvae in the city of Yaoundé, Cameroon. METHODS:All water bodies were checked once every 2 months for the presence of mosquito larvae from March 2017 to May 2018 in 32 districts of Yaoundé. Physico-chemical characteristics including the size, depth, turbidity, pH, temperature, conductivity, sulfates, organophosphates, hydrogen peroxide (H2O2), conductivity, iron and calcium were recorded and analyzed according to anopheline larvae presence or absence. High resolution satellite images from landsat sentinel Enhanced Thematic Mapper were used for spatial mapping of both field and environmental variables. Bivariate and multivariate logistic regression models were used to identify variables closely associated with anopheline larvae distribution. RESULTS:A total of 18?696 aquatic habitats were checked and only 2942 sites (15.7%) contained anopheline larvae. A high number of sites with anopheline larvae (? 69%) presented late instar larvae (L3, L4 and pupae). Anopheline mosquito larvae were sampled from a variety of breeding sites including puddles (51.6%), tire prints (12.9%), wells (11.7%) and drains (11.3%). Bivariate logistic regression analyses associated anopheline larvae presence with the absence of predators, absence of algae, absence of vegetation and depth of less than 1?m. Conductivity, turbidity, organophosphates, H2O2 and temperature were significantly high in breeding sites with anopheline larvae than in breeding sites without these larvae (P?<? 0.1). Anopheline species collected included An. coluzzii (91.1%) and An. gambiae s.s. (8.9%). GIS mapping indicated a heterogeneous distribution of anopheline breeding habitats in the city of Yaoundé. Land cover analysis indicated high variability of the city of Yaoundé's landscape. CONCLUSIONS:The data confirms adaptation of An. gambiae s.l. to the urban domain in the city of Yaoundé and calls for urgent actions to improve malaria vector control.

Project description:Background: Malaria remains a major public health problem in Cameroon; however, despite reports on the adaptation of anopheline species to urban habitats, there is still not enough information on malaria transmission pattern in urban settings. In the frame of a larval control trial in the city of Yaoundé, we conducted baseline surveys to assess malaria transmission dynamics in this city. Methods: Adult mosquitoes were collected indoors and outdoors using CDC light traps and human landing catches from March 2017 to March 2018 in 30 districts of Yaoundé, Cameroon. Mosquitoes were sorted by genus and identified to the species level using PCR. The TaqMan method and ELISA were used to determine mosquito infection status to Plasmodium. Bioassays were conducted to assess female Anopheles gambiae susceptibility to insecticides. Results: A total of 218,991 mosquitoes were collected. The main malaria vectors were An. gambiae s.l. (n=6154) and An. funestus s.l. (n=229). Of the 1476 An. gambiae s.l. processed by PCR, 92.19% were An. coluzzii and 7.81% An. gambiae. An. funestus s.l. was composed of 93.01% (173/186) An. funestus and 4.84% (13/186) An. leesoni. The average biting rate of anopheline was significantly high outdoor than indoor (P=0.013). Seasonal variation in mosquito abundance and biting rate was recorded. The infection rate by Plasmodium falciparum was 2.13% (104/4893 mosquitoes processed). The annual entomological inoculation rate was found to vary from 0 to 92 infective bites/man/year (ib/m/y). Malaria transmission risk was high outdoor (66.65 ib/m/y) compared to indoor (31.14 ib/m/y). An. gambiae s.l. was found highly resistant to DDT, permethrin and deltamethrin. High prevalence of the West Africa kdr allele 1014F was recorded and this was not found to influence An. gambiae s.l. infection status. Conclusion: The study suggests high malaria transmission occurring in the city of Yaoundé and call for immediate actions to improve control strategies.

Project description:A key factor affecting malaria vector control efforts in Cameroon is the rapid expansion of insecticide resistance in Anopheles gambiae s.l (An. gambiae) populations; however, mechanisms involved in insecticide resistance in forest mosquito populations are still not well documented yet. The present study was conducted to screen molecular mechanisms conferring insecticide resistance in An. gambiae s.l. populations from the South Cameroon forest region. WHO bioassays were conducted with F0 An. gambiae females aged three to four days from forest (Sangmelima, Nyabessan, and Mbandjock) and urban sites (Yaoundé (Bastos and Nkolondom)), against pyrethroids (permethrin 0.75% and deltamethrin 0.05%) and carbamates (bendiocarb 0.1%). Members of the An. Gambiae s.l. species complex were identified using molecular diagnostic tools. TaqMan assays were used to screen for target site mutations. The expression profiles of eight genes implicated in insecticide resistance were assessed using RT-qPCR. Cuticle hydrocarbon lipids were measured to assess their potential implication in insecticide resistance. Both An. Gambiae and An. coluzzii were detected. An. gambiae was highly prevalent in Sangmelima, Nyabessan, Mbandjock, and Nkolondom. An. coluzzii was the only species found in the Yaoundé city center (Bastos). Low mortality rate to both pyrethroids and bendiocarb was recorded in all sites. High frequency of L1014F allele (75.32-95.82%) and low frequencies of L1014S (1.71-23.05%) and N1575Y (5.28-12.87%) were recorded. The G119S mutation (14.22-35.5%) was detected for the first time in An. gambiae populations from Cameroon. This mutation was rather absent from An. coluzzii populations. The detoxification genes Cyp6m2, Cyp9k1, Cyp6p4, Cyp6z1, as well as Cyp4g16 which catalyzes epicuticular hydrocarbon biosynthesis, were found to be overexpressed in at least one population. The total cuticular hydrocarvbon content, a proxy of cuticular resistance, did not show a pattern associated with pyrethroid resistance in these populations. The rapid emergence of multiple resistance mechanisms in An. Gambiae s.l. population from the South Cameroon forest region is of big concern and could deeply affect the sustainability of insecticide-based interventions strategies in this region.

Project description:BackgroundThe sibling species of the malaria mosquito, Anopheles gambiae (sensu stricto) and Anopheles coluzzii co-exist in many parts of West Africa and are thought to have recently diverged through a process of ecological speciation with gene flow. Divergent larval ecological adaptations, resulting in Genotype-by-Environment (G × E) interactions, have been proposed as important drivers of speciation in these species. In West Africa, An. coluzzii tends to be associated with permanent man-made larval habitats such as irrigated rice fields, which are typically more eutrophic and mineral and ammonia-rich than the temporary rain pools exploited by An. gambiae (s.s.) METHODS: To highlight G × E interactions at the larval stage and their possible role in ecological speciation of these species, we first investigated the effect of exposure to ammonium hydroxide and water mineralisation on larval developmental success. Mosquito larvae were exposed to two water sources and increasing ammonia concentrations in small containers until adult emergence. In a second experiment, larval developmental success was compared across two contrasted microcosms to highlight G × E interactions under conditions such as those found in the natural environment.ResultsThe first experiment revealed significant G × E interactions in developmental success and phenotypic quality for both species in response to increasing ammonia concentrations and water mineralisation. The An. coluzzii strain outperformed the An. gambiae (s.s.) strain under limited conditions that were closer to more eutrophic habitats. The second experiment revealed divergent crisscrossing reaction norms in the developmental success of the sibling species in the two contrasted larval environments. As expected, An. coluzzii had higher emergence rates in the rice paddy environment with emerging adults of superior phenotypic quality compared to An. gambiae (s.s.), and vice versa, in the rain puddle environment.ConclusionsEvidence for such G × E interactions lends support to the hypothesis that divergent larval adaptations to the environmental conditions found in man-made habitats such as rice fields in An. coluzzii may have been an important driver of its ecological speciation.

Dataset Information

Gene expression divergence between malaria vector sibling species Anopheles gambiae and An. coluzzii from rural and urban Yaounde Cameroon.

Publications

Gene expression divergence between malaria vector sibling species Anopheles gambiae and An. coluzzii from rural and urban Yaoundé Cameroon.

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