The influence of anthropogenic habitat fragmentation on the genetic structure and diversity of the malaria vector Anopheles cruzii (Diptera: Culicidae)

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.

Mosquitoes (Diptera: Culicidae) in oviposition traps set in forest fragments of a semideciduous seasonal forest, Atlantic Forest domain, in the state of Rio Grande do Sul, Brazil

“…In this study, although more than one mosquito species was observed in the same breeding site, none of the species showed a significant co-occurring behavior with another in the installed traps. Some studies indicate that semiochemicals produced by Culicidae larvae can mediate the oviposition behavior of other species, enabling pregnant females to avoid ovipositing, for example, in breeding sites previously colonized by predators or by interspecific competitors (Navarro-Silva et al 2009). Thus, apparently, eventual semiochemicals produced by the larvae do not seem to mediate the oviposition pattern of the recorded species.…”

“…The process of hyperfragmentation of the Atlantic Domain landscapes has promoted the phenomenon of taxonomic homogenization of the biota, promoting the proliferation and dominance of groups of animal species with generalist characteristics (Lôbo et al 2011). This forest fragmentation also affects mosquito communities, changing their composition, genetic diversity and behavior (Multini et al 2020;Wilk-da-Silva et al 2020).…”

Atlantic Forest Malaria: A Review of More than 20 Years of Epidemiological Investigation

“…According to Multini et al (2020), the genetic structure among the populations of An. (K.) cruzii collected on the ground and in the canopy of trees in the urban environment near the dense Atlantic Forest in São Paulo and the greater genetic diversity in the urban ground-level population indicates an increased insect–human contact [ 78 ].…”

“…Anthropogenic modifications of the natural habitat of mosquitoes point to a consequent shift to the anthropophilic behavior of An. (K.) cruzii becoming increasingly common [ 78 , 79 ]. Understanding the impact of human modifications in natural habitats of An.…”

Vector role and human biting activity of Anophelinae mosquitoes in different landscapes in the Brazilian Amazon

“…In addition, increased density of mosquito habitats in human-dominated landscapes can lead to augmented abundance of mosquito vectors, resulting in increased malaria incidence. An interrelated chain of ecological events has been shown to lead to alterations in mosquito species composition in environments that are impacted by habitat loss and fragmentation associated with anthropogenic activities [ 17 , 18 ]. An increased abundance of generalist and opportunistic species [ 19 ], including vectors and infectious pathogens [ 20 ], has been shown to have a potential effect on mosquito communities.…”