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Genetic Technologies for Sustainable Management of Insect Pests and Disease Vectors sustainability Review Genetic Technologies for Sustainable Management of Insect Pests and Disease Vectors Silvia Grilli 1, Roberto Galizi 2 and Chrysanthi Taxiarchi 1,* 1 Department of Life Sciences, Imperial College London, London SW7 2AZ, UK; [email protected] 2 Centre for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Staffordshire ST5 5GB, UK; [email protected] * Correspondence: [email protected] Abstract: Recent advancements in genetic and genome editing research, augmented by the discovery of new molecular tools such as CRISPR, have revolutionised the field of genetic engineering by enabling precise site-specific genome modifications with unprecedented ease. These technologies have found a vast range of applications, including the development of novel methods for the control of vector and pest insects. According to their genetic makeup and engineering, these tools can be tuned to impose different grades of impact on the targeted populations. Here, we review some of the most recent genetic control innovations under development, describing their molecular mechanisms and performance, highlighting the sustainability potentials of such interventions. Keywords: sustainability; genetic control; disease vectors; genome editing; gene drive 1. Introduction Citation: Grilli, S.; Galizi, R.; A few harmful insect species dramatically threaten humankind by directly or indirectly Taxiarchi, C. Genetic Technologies for affecting numerous aspects of society, especially public health, the environment, and Sustainable Management of Insect the economy. Vector-borne diseases (VBDs) including malaria, dengue, schistosomiasis, Pests and Disease Vectors. trypanosomiasis, leishmaniasis, yellow fever, Japanese encephalitis, and onchocerciasis, Sustainability 2021, 13, 5653. https:// collectively claim around 700,000 lives per year [1]. In addition to this, it has been estimated doi.org/10.3390/su13105653 that between 17 and 40% of essential food crops are destroyed annually by agricultural pests. Tropical and subtropical regions, where a great proportion of the population struggle Academic Editor: Gerhart U. Ryffel with poverty and malnutri tion, are among the most affected by agricultural pests and vector-borne diseases [2]. Furthermore, globalization, population growth, and climate Received: 14 April 2021 change, along with forest degradation and urbanization, have exacerbated the burden of Accepted: 12 May 2021 insect vectors [3]. For instance, an increase in frequency and severity of extreme climate Published: 18 May 2021 events has caused crop damages with consequent loss of food productivity, and has affected the ecosystems, causing a shift of species distribution and prolonged disease transmission Publisher’s Note: MDPI stays neutral seasons [4]. For instance, many species of exotic mosquitoes of the genus Aedes, which are with regard to jurisdictional claims in published maps and institutional affil- vectors of several arboviruses, are now also established in Europe [4], where they caused iations. outbreaks of Dengue in France in 2015 [5] and Chikungunya in Italy in 2007 and 2017 [6]. Historically, efforts to manage harmful insects have significantly reduced the impact of many infectious diseases. Nonetheless, global eradication of the major vector-borne diseases remains a major challenge [7]. Integrated pest and vector management (IPVM), which incorporates a panel of control strategies, active engagement of local communities, Copyright: © 2021 by the authors. modelling of population dynamics and disease transmission, risk assessment, and moni- Licensee MDPI, Basel, Switzerland. toring, has been adopted worldwide to promote sustainable interventions for controlling This article is an open access article distributed under the terms and insect vectors (Figure1)[ 8,9]. Traditional control methods including cultural, biological, conditions of the Creative Commons physical, and chemical approaches can be advantageous locally, but they are unsuitable Attribution (CC BY) license (https:// for area-wide control programmes [4,10–13]. Although insecticides play a key role in the creativecommons.org/licenses/by/ reduction of morbidity and mortality of various VBDs [11], concerns about their potential 4.0/). Sustainability 2021, 13, 5653. https://doi.org/10.3390/su13105653 https://www.mdpi.com/journal/sustainability Sustainability 2021, 13, x FOR PEER REVIEW 2 of 20 Sustainability 2021, 13, 5653 2 of 19 reduction of morbidity and mortality of various VBDs [11], concerns about their potential hazardhazard on on ecosystems ecosystems and and human human health health exis existt among among the public the public and scientific and scientific community commu- [12].nity The [12 ].extensive The extensive use of use insecticides of insecticides has led has to led increasing to increasing genetic genetic resistance resistance in ininsects, insects, whichwhich progressively progressively reduces reduces their their effectiveness effectiveness [14]. [14 ].Similarly, Similarly, while while similarly, similarly, pathogens pathogens havehave developed developed resistance resistance to todrugs, drugs, affecting affecting the the efficacy efficacy of of treatments treatments [15]. [15 ].Due Due to to the the aboveabove issues issues and and the the necessity necessity to to implement implement alternative alternative and and sustainable sustainable tools tools to to combat combat pestspests and and disease disease vectors, vectors, genetic genetic control control stra strategiestegies have have received received growing growing interest interest over over thethe last last decades. decades. The The consistent consistent progress progress of of genome genome editing editing technologies technologies and mathematicalmathemati- calmodelling modelling has has led led to to the the improved improved performance performance of of existing existing approaches approaches and and the the develop-devel- opmentment ofof newnew ones.ones. In this review, review, we we descr describeibe the the status status of of genetic genetic control control of of harmful harmful insectsinsects and and their their capacity capacity to to exert exert a asustainable sustainable effect. effect. FigureFigure 1. 1.IntegratedIntegrated pest pest and and vector vector management management (IPV (IPVM).M). IPVM IPVM integrates integrates biological, biological, physical, physical, cultural,cultural, chemical, chemical, and and genetic genetic vector vector control control prac practicestices with with active active engagement engagement of of local local communi- communities ties risk assessment and code of ethical aspects, monitoring and modelling of population dynam- risk assessment and code of ethical aspects, monitoring and modelling of population dynamics and ics and disease transmission. Cultural practices are aimed at rendering the environment unfavour- disease transmission. Cultural practices are aimed at rendering the environment unfavourable for able for the spread of insects, for example, by removing larvae breeding sites or improving water supply.the spread Biological of insects, control for exploits example, the by use removing of natural larvae predators breeding such sitesas larvivorous or improving fish wateragainst supply. mosquitoBiological larvae control [13]. exploits Physical the control use of creates natural a barrier predators between such asthe larvivorous insect and the fish host, against for exam- mosquito ple,larvae using [13 bed-nets,]. Physical whose control efficacy creates can abe barrier improv betweened by adding the insect insecticides and the (insecticide-treated host, for example, using nets,bed-nets, ITNs) whoseand indoor efficacy residual can be sprays improved (IRSs) by [7]. adding insecticides (insecticide-treated nets, ITNs) and indoor residual sprays (IRSs) [7]. 2. Genetic Control 2. Genetic Control Genetic control methods rely on insect mating to transmit a genetic element or mod- Genetic control methods rely on insect mating to transmit a genetic element or modifi- ification to the offspring to introduce a desirable trait in a wild population. Such strategies cation to the offspring to introduce a desirable trait in a wild population. Such strategies can can be designed to either reduce insect population size or, in the case of pathogen trans- be designed to either reduce insect population size or, in the case of pathogen transmitting mitting insects, mitigate the vectorial capacity. The two approaches are, respectively, insects, mitigate the vectorial capacity. The two approaches are, respectively, known as known as population suppression and population replacement (Figure 2). On the one population suppression and population replacement (Figure2). On the one hand, popula- hand, population suppression is pursued by imposing a fitness load to the target popula- tion suppression is pursued by imposing a fitness load to the target population, to reduce tion, to reduce the number of vectors to an extent that disease transmission is not sup- the number of vectors to an extent that disease transmission is not supported. This can ported. This can be achieved either by affecting insect fertility [16], sex determination [17], be achieved either by affecting insect fertility [16], sex determination [17], or biasing the or biasing the population sex ratio in favour of male, which is usually the non-damaging population sex ratio in favour of male, which is usually the non-damaging or non-disease
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