Larval Metal Pollutant Exposure Alters the Epigenetic Architecture of the Major Malaria Vector Anopheles Arabiensis (Diptera: Culicidae)

Abstract

BackgroundAnopheles arabiensis (a member of the An. gambiae species complex) is a major vector of malaria. These mosquitoes typically breed in clean bodies of water, but can also utilise polluted waters. Although this expands their breeding range, adaptation to breeding in polluted waters necessitates coping with a large amount of environmental stress in the form of exposure to heavy metal pollutants. Environmental stress can induce heritable changes to an organism without altering the basal genetic code. This occurs by rapid changes in the regulatory elements associated with nucleic acids that result in changes in patterns of gene expression and silencing. This is known as epigenetic regulation. There is currently little information on epigenetic regulation in An. arabiensis. The aim of this study was to examine whether exposure to metal pollutants at the larval stage induced alterations of epigenetic markers resulting in phenotypic changes in insecticide susceptible and resistant laboratory strains of An. arabiensis. ResultsThere was a marked difference in the phenotypic response in adult mosquitoes of the insecticide susceptible strain compared to that of its’ resistant counterpart. The susceptible strain showed reduced fertility and fecundity in response to epigenetic manipulation. For males and females of the resistant strain, exposure to nucleic acid modifying drugs typically increased their tolerance to insecticides. In the insecticide susceptible strain, regulatory signals associated with gene silencing were increased, while those associated with gene expression were reduced in response to heavy metal exposure. By contrast, the insecticide resistant strain showed a decrease in signatures associated with gene silencing as well as an increase in signatures associate with chromatin remodelling. ConclusionsLarval exposure to heavy metal contaminants can result in heritable changes in gene expression. These data suggest that exposure to the same pollutants can result in different biological outcomes in insecticide susceptible and resistant adult An. arabiensis, and that these changes are reflected in their respective global? epigenetic signatures.

Insect Epigenetic Mechanisms Facing Anthropogenic-Derived Contamination, an Overview

“…The study of anthropogenically derived influences as epigenetic stimuli, such as pollution and climate change, are among the fast-growing areas of interest within insect EMMs [ 79 , 80 , 81 ]. The goal of these studies is to assess how stressors may affect different ecological levels [ 82 ], considering exposure to pesticides [ 41 , 44 , 83 ], endocrine disruptors [ 11 , 84 , 85 ], heavy metals [ 84 , 86 , 87 ], or temperature changes [ 88 ] as triggers of epigenetic changes. In Table 2 , we summarize the different responses of insect biology to different kinds of toxicants and whether there is evidence of the role of EMMs in these processes.…”

“…Over half of the studies shown in Table 2 were conducted on dipterans as model organisms, with considerable focus on species with aquatic phases during development such as mosquitoes (e.g., [ 11 , 84 , 132 ]). Of all the toxicants reviewed, the only group without studies in aquatic environments is the carbamate cholinesterase inhibitors, a group of organic compounds derived from carbamic acid (NH 2 COOH) found in broad-spectrum pesticides (e.g., [ 107 , 108 , 109 , 110 ]).…”

“…As shown in Table 2 , many studies have been performed in artificial [ 84 , 89 , 101 , 125 ] and natural [ 91 , 94 , 122 ] aquatic settings to emulate scenarios of water pollution. This kind of study is vital in order to gauge the impact of the presence and application of chemicals in the environmEntomol.…”

“…This kind of study is vital in order to gauge the impact of the presence and application of chemicals in the environmEntomol. Since aquatic insects are routinely used as bioindicators of the toxicity of different chemicals [ 98 ], it is not surprising that interest in their epigenetic responses to harmful stimuli has grown recently [ 11 , 84 , 85 ].…”