The primary Amazonian malaria vector Anopheles darlingi has the ability to adapt quickly to micro- geographic changes resulting from novel environmental conditions such as those encountered in agricultural settlements. Therefore, it is a substantial health threat in Latin America. This proposal examines three understudied aspects of An. darlingi to identify the main mechanism responsible for its success in transmission: broad plasticity or genetic specialization. First, we will test the Frontier Malaria Hypothesis (FMH), tht settlement age predicts malaria incidence, by explicitly separating the effects of settlement age and forest cover. We will use a state-of-the art ecologically-based experimental design that compares environmental variables in three levels of forest cover and two habitat types in both new and old settlements in two regions of Amazonian Brazil. Entomological metrics, most notably the entomological inoculation rate (EIR), will be compared among 12 settlements. We anticipate that a modified FMH, that accounts for both age and forest cover, will provide stronger predictive power for the invasiveness of An. darlingi and other vectors in a wide range of fragmented landscape types. Secondly, we will compare population genomics of An. darlingi exposed to (i) different levels of Plasmodium in the endemic Amazonian region versus southern Brazil where malaria is rare, and (ii) environmental variables in multiple Amazonian settlements. Development of SNPs across the An. darlingi genome will allow us to determine whether populations of An. darlingi differ in their genetic capacity to resist Plasmodium and to discover genomic signatures of selection among populations and regions. Thirdly, we will conduct life-history experiments that focus on the reaction norms to temperature of traits that are directly linked to vectorial capacity. We will test for regional genetic variation for traits and their plasticities, and evaluate whether there has been selection for these differences. By providing original data on the genotypic and phenotypic characteristics integral to the rapid response of An. darlingi to landscape fragmentation, our work will have a significant impact on frontier malaria in the Amazon and in other similar settings. The proposed work is conceptually innovative because it links landscape fragmentation, genetics and life-history traits with the precise localities that are likely to become foci of increased transmission. It is technically innovative because of the use of a next-gen RADseq method to evaluate populations of An. darlingi from localities with varying exposure to Plasmodium. Our long-term goal is to predict where and when An. darlingi populations will expand, resulting in new foci of malaria risk.

Public Health Relevance

Malaria is an immense global public health concern and in the Americas, Brazil has the greatest proportion (>50%) of annual malaria cases. This research will provide innovative information on the mechanisms enabling the primary Latin American malaria vector, Anopheles darlingi, to rapidly adapt to novel environments, such as those created by deforestation. Our studies of such high malaria regions in Amazonian Brazil, will identify predictors of local malaria risk, facilitating the development of new ways to reduce malaria transmission in similar settings globally. 1

National Institute of Health (NIH)
National Institute of Allergy and Infectious Diseases (NIAID)
Research Project (R01)
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Vector Biology Study Section (VB)
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Costero, Adriana
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Prussing, Catharine; Moreno, Marta; Saavedra, Marlon P et al. (2018) Decreasing proportion of Anopheles darlingi biting outdoors between long-lasting insecticidal net distributions in peri-Iquitos, Amazonian Peru. Malar J 17:86
Chaves, Leonardo Suveges Moreira; Conn, Jan E; López, Rossana Verónica Mendoza et al. (2018) Abundance of impacted forest patches less than 5?km2 is a key driver of the incidence of malaria in Amazonian Brazil. Sci Rep 8:7077
Bourke, Brian P; Conn, Jan E; de Oliveira, Tatiane M P et al. (2018) Exploring malaria vector diversity on the Amazon Frontier. Malar J 17:342
Prussing, Catharine; Bickersmith, Sara A; Moreno, Marta et al. (2018) Nyssorhynchus dunhami: bionomics and natural infection by Plasmodium falciparum and P. vivax in the Peruvian Amazon. Mem Inst Oswaldo Cruz 113:e180380
Ilacqua, Roberto Cardoso; Chaves, Leonardo Suveges Moreira; Bergo, Eduardo Sterlino et al. (2018) A method for estimating the deforestation timeline in rural settlements in a scenario of malaria transmission in frontier expansion in the Amazon Region. Mem Inst Oswaldo Cruz 113:e170522
Rosero-garcÍa, Doris; Bickersmith, Sara A; Suaza-Vasco, Juan David et al. (2017) Molecular operational taxonomic units of mosquitoes (Diptera: Culicidae) collected in high Andean mountain ecosystems of Antioquia, Colombia. Zootaxa 4277:369-385
Moreno, Marta; Saavedra, Marlon P; Bickersmith, Sara A et al. (2017) Intensive trapping of blood-fed Anopheles darlingi in Amazonian Peru reveals unexpectedly high proportions of avian blood-meals. PLoS Negl Trop Dis 11:e0005337
Bickersmith, Sara A; Lainhart, William; Moreno, Marta et al. (2015) A sensitive, specific and reproducible real-time polymerase chain reaction method for detection of Plasmodium vivax and Plasmodium falciparum infection in field-collected anophelines. Mem Inst Oswaldo Cruz 110:573-6
Emerson, Kevin J; Conn, Jan E; Bergo, Eduardo S et al. (2015) Brazilian Anopheles darlingi Root (Diptera: Culicidae) Clusters by Major Biogeographical Region. PLoS One 10:e0130773
Lainhart, William; Bickersmith, Sara A; Moreno, Marta et al. (2015) Changes in Genetic Diversity from Field to Laboratory During Colonization of Anopheles darlingi Root (Diptera: Culicidae). Am J Trop Med Hyg 93:998-1001

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