Increasing outdoor host-seeking in Anopheles gambiae over 6 years of vector control on Bioko Island.

BACKGROUND: Vector control through indoor residual spraying (IRS) has been employed on Bioko Island, Equatorial Guinea, under the Bioko Island Malaria Control Project (BIMCP) since 2004. This study analyses the change in mosquito abundance, species composition and outdoor host-seeking proportions from 2009 to 2014, after 11 years of vector control on Bioko Island. METHODS: All-night indoor and outdoor human landing catches were performed monthly in the Bioko Island villages of Mongola, Arena Blanca, Biabia and Balboa from 2009 to 2014. Collected mosquitoes were morphologically identified and a subset of Anopheles gambiae sensu lato (s.l.) were later identified molecularly to their sibling species. Mosquito collection rates, species composition and indoor/outdoor host-seeking sites were analysed using generalized linear mixed models to assess changes in mosquito abundance and behaviour. RESULTS: The overall mosquito collection rate declined in each of the four Bioko Island villages. Anopheles coluzzii and Anopheles melas comprised the An. gambiae s.l. mosquito vector population, with a range of species proportions across the four villages. The proportion of outdoor host-seeking An. gambiae s.l. mosquitoes increased significantly in all four villages with an average increase of 58.8 % [57.9, 59.64 %] in 2009 to 70.0 % [67.8, 72.0 %] in 2014. Outdoor host-seeking rates did not increase in the month after an IRS spray round compared to the month before, suggesting that insecticide repellency has little impact on host-seeking behaviour. CONCLUSION: While vector control on Bioko Island has succeeded in substantial reduction in overall vector biting rates, populations of An. coluzzii and An. melas persist. Host-seeking behaviour has changed in these An. gambiae s.l. populations, with a shift towards outdoor host-seeking. During this study period, the proportion of host-seeking An. gambiae s.l. caught outdoors observed on Bioko Island increased to high levels, exceeding 80 % in some locations. It is possible that there may be a genetic basis underlying this large shift in host-seeking behaviour, in which case outdoor feeding could pose a serious threat to current vector control programmes. Currently, the BIMCP is preparing for this potential challenge by testing source reduction as a complementary control effort that also targets outdoor transmission

Species-specific chemosensory gene expression in the olfactory organs of the malaria vector Anopheles gambiae

Background: The malaria mosquito Anopheles gambiae has a high preference for human hosts, a characteristic that contributes greatly to its capacity for transmitting human malaria. A sibling species, An. quadriannulatus, has a quite different host preference and feeds mostly on bovids. For this reason it does not contribute to human malaria transmission. Host seeking in mosquitoes is modulated by the olfactory system, which is primarily housed in the antennae and maxillary palps. Therefore, the detection of differing host odors by sibling species may be reflected in the expression level of the olfactory genes involved. Accordingly, we compared the transcriptomes of the antennae and maxillary palps of An. gambiae and An. quadriannulatus. Results: We identified seven relatively abundant olfactory receptors, nine ionotropic receptors and three odorant binding proteins that are substantially up-regulated in An. gambiae antennae. Interestingly, we find that the maxillary palps of An. gambiae contain a species-specific olfactory receptor, Or52, and five An. gambiae-specific gustatory receptors (AgGr48-52) that are relatively abundant. These five gustatory receptors are also expressed in An. gambiae antennae, although at lower level, indicating a likely role in olfaction, rather than gustation. We also document an approximately three-fold higher overall expression of olfaction genes in the maxillary palps of An. quadriannulatus, indicating an important role of this organ in the olfaction system of this species. Finally, the expression of the CO2 receptor genes is five to six-fold higher in the zoophilic An. quadriannulatus, implying a much higher sensitivity for detecting CO2. Conclusions: These results identify potential human host preference genes in the malaria vector An. gambiae. Interestingly, species-specific expression of several gustatory receptors in the olfactory organs indicate a role in olfaction rather than gustation. Additionally, a more expansive role for maxillary palps in olfaction is implicated than previously thought, albeit more so in the zoophilic An. quadriannulatus.(The Retraction Note to this article has been published in BMC Genomics 2015 16:572

Chemosensory gene expression in olfactory organs of the anthropophilic Anopheles coluzzii and zoophilic Anopheles quadriannulatus

Background: Anopheles (An.) coluzzii, one of Africa's primary malaria vectors, is highly anthropophilic. This human host preference contributes greatly to its ability to transmit malaria. In contrast, the closely related An. quadriannulatus prefers to feed on bovids and is not thought to contribute to malaria transmission. The diverged preference for host odor profiles between these sibling species is likely reflected in chemosensory gene expression levels in the olfactory organs. Therefore, we compared the transcriptomes of the antennae and maxillary palps between An. coluzzii and An. quadriannulatus, focusing on the major chemosensory gene families. Results: While chemosensory gene expression is strongly correlated between the two species, various chemosensory genes show significantly enhanced expression in one of the species. In the antennae of An. coluzzii the expression of six olfactory receptors (Ors) and seven ionotropic receptors (Irs) is considerably enhanced, whereas 11 Ors and 3 Irs are upregulated in An. quadriannulatus. In the maxillary palps, leaving aside Irs with very low level of expression, one Ir is strongly enhanced in each species. In addition, we find divergence in odorant binding protein (Obp) gene expression, with several highly expressed Obps being enhanced in the antennae and palps of An. coluzzii. Finally, the expression of several gustatory receptors (Grs) in the palps appears to be species-specific, including a homolog of a sugar-sensing Drosophila Gr. Conclusions: A considerable number of Ors and Irs are differentially expressed between these two closely related species with diverging host preference. These chemosensory genes could play a role in the human host preference of the malaria vector An. coluzzii. Additionally, divergence in Obp expression between the two species suggests a possible role of these odor carrier proteins in determining host preference. Finally, divergence in chemosensory expression in the palps may point towards a possible role for the maxillary palps in host differentiation.</p

Anopheles coluzzii and Anopheles quadriannulatus olfactory gene expression

RNAseq data from Anopheles coluzzii and Anopheles quadriannulatus antennae and maxillary palps

Anopheles coluzzii and Anopheles quadriannulatus olfactory gene expression

RNAseq data from Anopheles coluzzii and Anopheles quadriannulatus antennae and maxillary palps

Anopheles coluzzii and Anopheles quadriannulatus olfactory gene expression

RNAseq data from Anopheles coluzzii and Anopheles quadriannulatus antennae and maxillary palps

MOESM1 of Increasing outdoor host-seeking in Anopheles gambiae over 6Â years of vector control on Bioko Island

Additional file 1. Month and year of IRS spray rounds by village