Abstract

Fragmentation of natural environments as a result of human interference has been associated with a decrease in species richness and increase in abundance of a few species that have adapted to these environments. The Brazilian Atlantic Forest, which has been undergoing an intense process of fragmentation and deforestation caused by human-made changes to the environment, is an important hotspot for malaria transmission. The main vector of simian and human malaria in this biome is the mosquito Anopheles cruzii. Anthropogenic processes reduce the availability of natural resources at the tree canopies, An. cruzii primary habitat. As a consequence, An. cruzii moves to the border of the Atlantic Forest nearing urban areas seeking resources, increasing their contact with humans in the process. We hypothesized that different levels of anthropogenic changes to the environment can be an important factor in driving the genetic structure and diversity in An. cruzii populations. Five different hypotheses using a cross-sectional and a longitudinal design were tested to assess genetic structure in sympatric An. cruzii populations and microevolutionary processes driving these populations. Single nucleotide polymorphisms were used to assess microgeographic genetic structure in An. cruzii populations in a low-endemicity area in the city of São Paulo, Brazil. Our results show an overall weak genetic structure among the populations, indicating a high gene flow system. However, our results also pointed to the presence of significant genetic structure between sympatric An. cruzii populations collected at ground and tree-canopy habitats in the urban environment and higher genetic variation in the ground-level population. This indicates that anthropogenic modifications leading to habitat fragmentation and a higher genetic diversity and structure in ground-level populations could be driving the behavior of An. cruzii, ultimately increasing its contact with humans. Understanding how anthropogenic changes in natural areas affect An. cruzii is essential for the development of more effective mosquito control strategies and, on a broader scale, for malaria-elimination efforts in the Brazilian Atlantic Forest.

Highlights

  • Anthropogenic interference in the environment is a major driving force of e­ volution[1,2]

  • Comparisons of the test for Hardy–Weinberg equilibrium (HWE) for all the populations showed that expected heterozygosity was higher than observed heterozygosity (Ho) (Table 2)

  • There is probably still movement between An. cruzii from tree canopies to ground level and vice-versa, our results suggest that in areas close to human dwellings, An. cruzii populations are more diverse and genetic structured at ground level

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Summary

Introduction

Anthropogenic interference in the environment is a major driving force of e­ volution[1,2]. The Atlantic Forest is an important malaria transmission ­hotspot[23,24] and is home to Anopheles (Kerteszia) cruzii Dyar and Knab, a neotropical mosquito found abundantly in this biome, where it is the main vector of simian and human malaria This mosquito has a close relationship with plants from the Bromeliaceae family (bromeliads)[25] as it uses the water accumulated in the bromeliad water tanks as its primary/exclusive breeding ­habitat[26]. Some studies have found an association between anthropogenic changes in the environment and the occurrence of human malaria, asymptomatic plasmodial infections and zoonotic malaria transmission in the Atlantic F­ orest[28,29,30,31] Because of this species’ close relationship with the Atlantic Forest environment and because of its acrodendrophilic habits (i.e., its preference for inhabiting tree canopies), the ecology and phenotype of An. cruzii are believed to be affected by the fragmentation of the Atlantic Forest ­biome[30,32,33]. The species was found to be more active at ground level in areas with a greater edge effect and greater loss of forested ­areas[37], a factor which may contribute to the zoonotic transmission of Plasmodium

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