Functional genetic validation of key genes conferring insecticide resistance in the major African malaria vector, Anopheles gambiae

ABSTRACTResistance in Anopheles gambiae to members of all four major classes (pyrethroids, carbamates, organochlorines and organophosphates) of public health insecticides limits effective control of malaria transmission in Africa. Increased expression of detoxifying enzymes has been associated with resistance, but direct functional validation in An. gambiae has been lacking. Here we perform transgenic analysis using the GAL4/UAS system to examine insecticide resistance phenotypes conferred by increased expression of the three genes - Cyp6m2, Cyp6p3 and Gste2 - most often found upregulated in resistant An. gambiae. We report the first evidence in An. gambiae that organophosphate and organochlorine resistance is conferred by overexpression of GSTE2 in a broad tissue profile. Pyrethroid and carbamate resistance is bestowed by similar Cyp6p3 overexpression, and Cyp6m2 confers only pyrethroid resistance when overexpressed in the same tissues. Conversely, such Cyp6m2 overexpression increases susceptibility to the organophosphate malathion, presumably due to conversion to a more toxic metabolite. No resistant phenotypes are conferred when either Cyp6 gene overexpression is restricted to the midgut or oenocytes, answering long standing questions related to the importance of these tissues in resistance to contact insecticides. Validation of genes conferring resistance provides markers to guide control strategies, and the observed negative cross-resistance due to Cyp6m2 gives credence to proposed dual insecticide strategies to overcome pyrethroid resistance. These trasnsgenic An. gambiae resistant lines are being used to test potential liabilities in new active compounds early in development.SIGNIFICANCE STATEMENTInsecticide resistance in Anopheles gambiae mosquitoes can derail malaria control programs, and to overcome it we need to discover the underlying molecular basis. Here, for the first time, we characterise three genes most often associated with insecticide resistance directly by their overproduction in genetically modified An. gambiae. We show that overexpression of each gene confers resistance to representatives of at least one insecticide class and, taken together, the three genes provide cross-resistance to all four major insecticide classes currently used in public health. These data validate the candidate genes as markers to monitor the spread of resistance in mosquito populations. The modified mosquitoes produced are also valuable tools to pre-screen new insecticides for potential liabilities to existing resistance mechanisms.

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Functional genetic validation of key genes conferring insecticide resistance in the major African malaria vector,Anopheles gambiae

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1914633116 ◽

2019 ◽

Vol 116 (51) ◽

pp. 25764-25772 ◽

Cited By ~ 13

Author(s):

Adriana Adolfi ◽

Beth Poulton ◽

Amalia Anthousi ◽

Stephanie Macilwee ◽

Hilary Ranson ◽

...

Keyword(s):

Insecticide Resistance ◽

Anopheles Gambiae ◽

Pyrethroid Resistance ◽

Control Strategies ◽

Effective Control ◽

Cross Resistance ◽

Toxic Metabolite ◽

Detoxifying Enzymes ◽

Resistant Lines ◽

Key Genes

Resistance inAnopheles gambiaeto members of all 4 major classes (pyrethroids, carbamates, organochlorines, and organophosphates) of public health insecticides limits effective control of malaria transmission in Africa. Increase in expression of detoxifying enzymes has been associated with insecticide resistance, but their direct functional validation inAn. gambiaeis still lacking. Here, we perform transgenic analysis using the GAL4/UAS system to examine insecticide resistance phenotypes conferred by increased expression of the 3 genes—Cyp6m2,Cyp6p3, andGste2—most often found up-regulated in resistantAn. gambiae. We report evidence inAn. gambiaethat organophosphate and organochlorine resistance is conferred by overexpression of GSTE2 in a broad tissue profile. Pyrethroid and carbamate resistance is bestowed by similarCyp6p3overexpression, andCyp6m2confers only pyrethroid resistance when overexpressed in the same tissues. Conversely, suchCyp6m2overexpression increases susceptibility to the organophosphate malathion, presumably due to conversion to the more toxic metabolite, malaoxon. No resistant phenotypes are conferred when eitherCyp6gene overexpression is restricted to the midgut or oenocytes, indicating that neither tissue is involved in insecticide resistance mediated by the candidate P450s examined. Validation of genes conferring resistance provides markers to guide control strategies, and the observed negative cross-resistance due toCyp6m2gives credence to proposed dual-insecticide strategies to overcome pyrethroid resistance. These transgenicAn. gambiae-resistant lines are being used to test the “resistance-breaking” efficacy of active compounds early in their development.

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Phenotypic Insecticide Resistance in Anopheles gambiae (Diptera: Culicidae): Specific Characterization of Underlying Resistance Mechanisms Still Matters

Journal of Medical Entomology ◽

10.1093/jme/tjaa195 ◽

2020 ◽

Author(s):

Adandé A Medjigbodo ◽

Luc S Djogbenou ◽

Aubin A Koumba ◽

Laurette Djossou ◽

Athanase Badolo ◽

...

Keyword(s):

Insecticide Resistance ◽

Anopheles Gambiae ◽

Resistance Mechanisms ◽

Malaria Vectors ◽

Effective Control ◽

Anopheles Coluzzii ◽

Anopheles Gambiae S.S ◽

Diagnostic Dose ◽

Pirimiphos Methyl ◽

Old Adult

Abstract An effective control of malaria vectors requires an extensive knowledge of mechanisms underlying the resistance-phenotypes developed by these vectors against insecticides. We investigated Anopheles gambiae mosquitoes from Benin and Togo for their intensity of insecticide resistance and we discussed the involvement of genotyped mechanisms in the resistance-phenotypes observed. Three- to five-day-old adult mosquitoes emerged from field and laboratory An. gambiae larvae were assayed using WHO tube intensity tests against various doses of deltamethrin: 1× (0.05%); 2× (0.1%); 5× (0.25%); 7.5× (0.375%) and those of pirimiphos-methyl: 0.5× (0.125%); 1× (0.25%). Members of An. gambiae complex were screened in field populations using polymerase chain reaction (PCR) assays. The presence of kdrR(1014F/1014S) and ace-1R(119S) mutations was also investigated using TaqMan and PCR-RFLP techniques, respectively. Anopheles gambiae from field were very resistant to deltamethrin, whereas KisKdr and AcerKdrKis strains displayed 100% mortality rates at 2× the diagnostic dose. In contrast, the field mosquitoes displayed a low resistance-intensity against 1× the diagnostic dose of pirimiphos-methyl, whereas AcerKis and AcerKdrKis strains showed susceptibility at 0.5× the diagnostic dose. Anopheles gambiae s.s., Anopheles coluzzii, and Anopheles arabiensis were identified. Allelic frequencies of kdrR (1014F) and ace-1R (119S) mutations in the field populations varied from 0.65 to 1 and 0 to 0.84, respectively. The field An. gambiae displayed high-resistance levels against deltamethrin and pirimiphos-methyl when compared with those of the laboratory An. gambiae-resistant strains. These results exhibit the complexity of underlying insecticide resistance mechanisms in these field malaria vectors.

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Phenotypic, genotypic and biochemical changes during pyrethroid resistance selection in Anopheles gambiae mosquitoes

Scientific Reports ◽

10.1038/s41598-020-75865-1 ◽

2020 ◽

Vol 10 (1) ◽

Author(s):

Maxwell G. Machani ◽

Eric Ochomo ◽

Daibin Zhong ◽

Guofa Zhou ◽

Xiaoming Wang ◽

...

Keyword(s):

Public Health ◽

Insecticide Resistance ◽

Anopheles Gambiae ◽

Selection Pressure ◽

Pyrethroid Resistance ◽

Natural Populations ◽

Biochemical Changes ◽

Moderate Intensity ◽

Agricultural System ◽

Selection For

Abstract The directional selection for insecticide resistance due to indiscriminate use of insecticides in public health and agricultural system favors an increase in the frequency of insecticide-resistant alleles in the natural populations. Similarly, removal of selection pressure generally leads to decay in resistance. Past investigations on the emergence of insecticide resistance in mosquitoes mostly relied on field survey of resistance in vector populations that typically had a complex history of exposure to various public health and agricultural pest control insecticides in nature, and thus the effect of specific insecticides on rate of resistance emergency or resistance decay rate is not known. This study examined the phenotypic, genotypic, and biochemical changes that had occurred during the process of selection for pyrethroid resistance in Anopheles gambiae, the most important malaria vector in Africa. In parallel, we also examined these changes in resistant populations when there is no selection pressure applied. Through repeated deltamethrin selection in adult mosquitoes from a field population collected in western Kenya for 12 generations, we obtained three independent and highly pyrethroid-resistant An. gambiae populations. Three susceptible populations from the same parental population were generated by removing selection pressure. These two lines of mosquito populations differed significantly in monooxygenase and beta-esterase activities, but not in Vgsc gene mutation frequency, suggesting metabolic detoxification mechanism plays a major role in generating moderate-intensity resistance or high-intensity resistance. Pre-exposure to the synergist piperonyl butoxide restored the susceptibility to insecticide among the highly resistant mosquitoes, confirming the role of monooxygenases in pyrethroid resistance. The rate of resistance decay to become fully susceptible from moderate-intensity resistance took 15 generations, supporting at least 2-years interval is needed when the rotational use of insecticides with different modes of action is considered for resistance management.

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Section 4. Pyrethroid and endosulfan resistance: selection and cross resistance studies

Bulletin of entomological research supplement series ◽

10.1017/s1367426900000102 ◽

1993 ◽

Vol 1 ◽

pp. 28-35 ◽

Cited By ~ 21

Author(s):

Neil W. Forrester ◽

Matthew Cahill ◽

Lisa J. Bird ◽

Jacquelyn K. Layland

Keyword(s):

Insecticide Resistance ◽

Lower Order ◽

Management Strategy ◽

Pyrethroid Resistance ◽

Resistance Management ◽

Resistance Mechanisms ◽

Cross Resistance ◽

Male And Female ◽

Insecticide Resistance Management ◽

Resistance Selection

SummaryResistance to endosulfan and pyrethroids in Helicoverpa armigera in Australia was shown to be due to multiple rather than cross resistance. The independence of the endosulfan and pyrethroid resistance mechanisms vindicates the sequential use of these two groups in Stages I and II of the insecticide resistance management strategy, respectively. Within the cyclodienes, greatest resistance occurred to dieldrin with lower order cross resistance to endosulfan and endrin. Male and female moths expressed cyclodiene resistance equally.

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Review of Insecticide Resistance and Its Underlying Mechanisms in Tribolium castaneum

10.5772/intechopen.100050 ◽

2021 ◽

Author(s):

U. Shamjana ◽

Tony Grace

Keyword(s):

Insecticide Resistance ◽

Tribolium Castaneum ◽

Control Strategies ◽

Management Strategies ◽

Resistance Mechanisms ◽

Whole Genome Sequence ◽

Next Generation Sequencing Technology ◽

Biological Targets ◽

Control Programs ◽

Underlying Mechanisms

The red flour beetle Tribolium castaneum has emerged as the genetically tractable model insect for population genetics, functional genomics, and evolutionary studies. This agricultural pest is notorious for its potential to severely damage stored products. T. castaneum has developed resistance to almost all insecticides. The reports of insecticide resistance from different parts of the world show that sustained insecticide usage has only aggravated the problem. As insecticides continue to be the mainstay of pest control programs, it is essential to identify the factors influencing insecticide resistance for implementing effective pest-management strategies. The development and progression of insecticide resistance in T. castaneum is thus an escalating global issue requiring immediate solutions. Several studies have investigated the multiple resistance mechanisms found in T. castaneum, such as reduced cuticular penetration, increased metabolic detoxification, and target-site insensitivity. The availability of Whole Genome Sequence and recent advances in Next Generation Sequencing technology has furthered a geneticist’s grasp of resistance study in Tribolium. The strategic containment of this organism calls for an in-depth understanding of resistance development. The review mainly focuses on different kinds of resistance mechanisms and genes mediating insecticide resistance. Also, it exhaustively explores the CYP450 gene superfamily in Tribolium to emphasize its role in governing resistance. The consolidated insights from this study will facilitate further research on identifying biological targets, thereby developing novel control strategies for effective insect control.

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Anopheles bionomics, insecticide resistance mechanisms, and malaria transmission in the Korhogo area, northern Côte d’Ivoire: a pre-intervention study

Parasite ◽

10.1051/parasite/2019040 ◽

2019 ◽

Vol 26 ◽

pp. 40 ◽

Cited By ~ 1

Author(s):

Barnabas Zogo ◽

Dieudonné Diloma Soma ◽

Bertin N’Cho Tchiekoi ◽

Anthony Somé ◽

Ludovic P. Ahoua Alou ◽

...

Keyword(s):

Insecticide Resistance ◽

Anopheles Gambiae ◽

Malaria Transmission ◽

Cote D'ivoire ◽

Rainy Season ◽

Côte D’Ivoire ◽

Resistance Mechanisms ◽

Effective Control ◽

Cote D’Ivoire ◽

Côte D'ivoire

A better understanding of malaria transmission at a local scale is essential for developing and implementing effective control strategies. In the framework of a randomized controlled trial (RCT), we aimed to provide an updated description of malaria transmission in the Korhogo area, northern Côte d’Ivoire, and to obtain baseline data for the trial. We performed human landing collections (HLCs) in 26 villages in the Korhogo area during the rainy season (September–October 2016, April–May 2017) and the dry season (November–December 2016, February–March 2017). We used PCR techniques to ascertain the species of the Anopheles gambiae complex, Plasmodium falciparum sporozoite infection, and insecticide resistance mechanisms in a subset of Anopheles vectors. Anopheles gambiae s.l. was the predominant malaria vector in the Korhogo area. Overall, more vectors were collected outdoors than indoors (p < 0.001). Of the 774 An. gambiae s.l. tested in the laboratory, 89.65% were An. gambiae s.s. and 10.35% were An. coluzzii. The frequencies of the kdr allele were very high in An. gambiae s.s. but the ace-1 allele was found at moderate frequencies. An unprotected individual living in the Korhogo area received an average of 9.04, 0.63, 0.06 and 0.12 infected bites per night in September–October, November–December, February–March, and April–May, respectively. These results demonstrate that the intensity of malaria transmission is extremely high in the Korhogo area, especially during the rainy season. Malaria control in highly endemic areas such as Korhogo needs to be strengthened with complementary tools in order to reduce the burden of the disease.

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Phenotypic and haplotypic profiles of insecticide resistance in populations of Aedes aegypti larvae (Diptera: Culicidae) from central Lao PDR

Tropical Medicine and Health ◽

10.1186/s41182-021-00321-3 ◽

2021 ◽

Vol 49 (1) ◽

Author(s):

Takaki Shimono ◽

Seiji Kanda ◽

Pheophet Lamaningao ◽

Yuki Murakami ◽

Andrew Waleluma Darcy ◽

...

Keyword(s):

Aedes Aegypti ◽

Insecticide Resistance ◽

Vector Control ◽

Pyrethroid Resistance ◽

Control Strategies ◽

Lao Pdr ◽

Resistance Mechanisms ◽

Cytochrome P450 Monooxygenases ◽

Bacillus Thuringiensis Israelensis ◽

Vector Management

Abstract Background Aedes aegypti, which is widely distributed in the Lao People’s Democratic Republic (PDR), is the primary vector of arboviral diseases. Chemical insecticides have been intensively used to eliminate mosquito-borne diseases, resulting in the development of insecticide resistance. However, little is known about the insecticide resistance of mosquito populations in Lao PDR and the mechanisms responsible for it, which have important implications for vector management programs. Here, we examined the phenotypic and haplotypic profiles of insecticide resistance in populations of Ae. aegypti larvae from central Lao PDR. Methods Ae. aegypti larvae were collected from four sites in Lao PDR, and their susceptibility to temephos, deltamethrin, permethrin, and Bacillus thuringiensis israelensis (Bti) was tested using larval bioassays. Synergistic tests were also conducted to evaluate the activity of insecticide-metabolizing enzymes in the larvae. Deltamethrin-resistant and Deltamethrin-susceptible larvae were then genotyped for knockdown resistance (kdr) mutations to determine the associations between each genotype and resistance. Results Ae. aegypti larvae from central Lao PDR were considered to be “resistant” (<98% mortality) to organophosphates and pyrethroids. The bio-insecticide Bti remains effective against such larvae. The resistance mechanisms of Ae. aegypti larvae were found to vary among populations, especially for pyrethroid resistance. Kdr mutations were significantly associated with deltamethrin resistance in Ae. aegypti from the Xaythany population. In contrast, synergist assays with piperonyl butoxide suggested that cytochrome P450 monooxygenases played an important role in the resistance seen in the Khounkham and Thakhek populations. Conclusion This study obtained information that will aid the design and implementation of insecticide-based vector management of Ae. aegypti in central Lao PDR. Ae. aegypti larvae from central Lao PDR were highly susceptible to Bti, while they were resistant to temephos at a diagnostic dose of 0.0286 mg/L. Given the limited number of insecticides that are approved for vector control, it is important to alternate between temephos and other larvicides, such as Bti and pyriproxyfen. The differences in pyrethroid resistance mechanisms seen among the Ae. aegypti populations highlight the need to tailor vector-control strategies to each region to increase the success of dengue control in Lao PDR.

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First detection of the kdr mutation (L1014F) in the plague vector Xenopsylla cheopis (Siphonaptera: Pulicidae)

Parasites & Vectors ◽

10.1186/s13071-019-3775-2 ◽

2019 ◽

Vol 12 (1) ◽

Author(s):

Nian Liu ◽

Xiangyang Feng ◽

Mei Li ◽

Xinghui Qiu

Keyword(s):

Network Analysis ◽

Insecticide Resistance ◽

Dna Sequences ◽

Pyrethroid Resistance ◽

Control Strategies ◽

Effective Control ◽

Phenotypic Effect ◽

Pyrethroid Insecticides ◽

Xenopsylla Cheopis ◽

Flea Control

Abstract Background The oriental rat flea, Xenopsylla cheopis, is the most efficient vector of the plague. Pyrethroid insecticides such as cypermethrin, cyhalothrin and deltamethrin have been often used to limit plague transmission via controlling the vector during outbreaks. However, this strategy is threatened by the development of insecticide resistance. Understanding the mechanisms underlying pyrethroid resistance is the prerequisite for successful flea control. Methods Partial DNA sequences of X. cheopis voltage gated sodium channel (VGSC) gene were amplified from a total of 111 individuals, collected from a natural plague epidemic foci in Baise City, Guangxi Zhuang Autonomous Region of China. These DNA fragments were sequenced. The frequency and distribution of kdr mutations were assessed in four X. cheopis populations. The origin of kdr mutations was investigated by phylogenetic and network analysis. Results The classical knockdown resistance (kdr) mutation (L1014F) was detected in four field populations at frequencies ranging between 0.021–0.241. The mutant homozygote was observed only in one of the four populations. Seven haplotypes were identified, with two of them carrying the resistance L1014F mutation. Phylogenetic tree and network analysis indicated that the L1014F allele was not singly originated. Based on polymerase chain reaction restriction fragment length polymorphism (PCR-RFLP) profiling, an easy-to-use and accurate molecular assay for screening individual fleas for the L1014F mutation was developed. Conclusions To our knowledge, this work represents the first report of the L1014F mutation in the plague vector X. cheopis. The incidence of the L1014F allele highlights the need of further studies on the phenotypic effect of this mutation in this plague vector. Early detection and monitoring of insecticide resistance is suggested in order to make effective control strategies in case of plague outbreaks in this region.

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Evolution of the Pyrethroids Target-Site Resistance Mechanisms in Senegal: Early Stage of the Vgsc-1014F and Vgsc-1014S Allelic Frequencies Shift

Genes ◽

10.3390/genes12121948 ◽

2021 ◽

Vol 12 (12) ◽

pp. 1948

Author(s):

Moussa Diallo ◽

Majidah Hamid-Adiamoh ◽

Ousmane Sy ◽

Pape Cheikh Sarr ◽

Jarra Manneh ◽

...

Keyword(s):

Insecticide Resistance ◽

Anopheles Gambiae ◽

Pyrethroid Resistance ◽

Early Stage ◽

Resistance Mechanisms ◽

Sub Saharan Africa ◽

Malaria Vectors ◽

Malaria Control Programme ◽

Anopheles Coluzzii ◽

Resistance Mutations

The evolution and spread of insecticide resistance mechanisms amongst malaria vectors across the sub-Saharan Africa threaten the effectiveness and sustainability of current insecticide-based vector control interventions. However, a successful insecticide resistance management plan relies strongly on evidence of historical and contemporary mechanisms circulating. This study aims to retrospectively determine the evolution and spread of pyrethroid resistance mechanisms among natural Anopheles gambiae s.l. populations in Senegal. Samples were randomly drawn from an existing mosquito sample, collected in 2013, 2017, and 2018 from 10 sentinel sites monitored by the Senegalese National Malaria Control Programme (NMCP). Molecular species of An. gambiae s.l. and the resistance mutations at the Voltage-gated Sodium Channel 1014 (Vgsc-1014) locus were characterised using PCR-based assays. The genetic diversity of the Vgsc gene was further analyzed by sequencing. The overall species composition revealed the predominance of Anopheles arabiensis (73.08%) followed by An. gambiae s.s. (14.48%), Anopheles coluzzii (10.94%) and Anopheles gambiae–coluzii hybrids (1.48%). Both Vgsc-1014F and Vgsc-1014S mutations were found in all studied populations with a spatial variation of allele frequencies from 3% to 90%; and 7% to 41%, respectively. The two mutations have been detected since 2013 across all the selected health districts, with Vgsc-L1014S frequency increasing over the years while Vgsc-1014F decreasing. At species level, the Vgsc-1014F and Vgsc-1014S alleles were more frequent amongst An. gambiae s.s. (70%) and An. arabiensis (20%). The Vgsc gene was found to be highly diversified with eight different haplotypes shared between Vgsc-1014F and Vgsc-1014S. The observed co-occurrence of Vgsc-1014F and Vgsc-1014S mutations suggest that pyrethroid resistance is becoming a widespread phenomenon amongst malaria vector populations, and the NMCP needs to address this issue to sustain the gain made in controlling malaria.

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Insecticide resistance status of Aedes aegypti in Bangladesh

Parasites & Vectors ◽

10.1186/s13071-020-04503-6 ◽

2020 ◽

Vol 13 (1) ◽

Author(s):

Hasan Mohammad Al-Amin ◽

Fatema Tuj Johora ◽

Seth R. Irish ◽

Muhammad Riadul Haque Hossainey ◽

Lucrecia Vizcaino ◽

...

Keyword(s):

Aedes Aegypti ◽

Insecticide Resistance ◽

Pyrethroid Resistance ◽

Control Strategies ◽

Resistance Mechanisms ◽

Capital City ◽

Detoxification Enzymes ◽

Knockdown Resistance ◽

Metabolic Resistance ◽

Pyrethroid Insecticides

Abstract Background Arboviral diseases, including dengue and chikungunya, are major public health concerns in Bangladesh where there have been unprecedented levels of transmission reported in recent years. The primary approach to control these diseases is to control the vector Aedes aegypti using pyrethroid insecticides. Although chemical control has long been practiced, no comprehensive analysis of Ae. aegypti susceptibility to insecticides has been conducted to date. The aim of this study was to determine the insecticide resistance status of Ae. aegypti in Bangladesh and investigate the role of detoxification enzymes and altered target site sensitivity as resistance mechanisms. Methods Eggs of Aedes mosquitoes were collected using ovitraps from five districts across Bangladesh and in eight neighborhoods of the capital city Dhaka, from August to November 2017. CDC bottle bioassays were conducted for permethrin, deltamethrin, malathion, and bendiocarb using 3- to 5-day-old F0–F2 non-blood-fed female mosquitoes. Biochemical assays were conducted to detect metabolic resistance mechanisms, and real-time PCR was performed to determine the frequencies of the knockdown resistance (kdr) mutations Gly1016, Cys1534, and Leu410. Results High levels of resistance to permethrin were detected in all Ae. aegypti populations, with mortality ranging from 0 to 14.8% at the diagnostic dose. Substantial resistance continued to be detected against higher (2×) doses of permethrin (5.1–44.4% mortality). Susceptibility to deltamethrin and malathion varied between populations while complete susceptibility to bendiocarb was observed in all populations. Significantly higher levels of esterase and oxidase activity were detected in most of the test populations as compared to the susceptible reference Rockefeller strain. A significant association was detected between permethrin resistance and the presence of Gly1016 and Cys1534 homozygotes. The frequency of kdr (knockdown resistance) alleles varied across the Dhaka Aedes populations. Leu410 was not detected in any of the tested populations. Conclusions The detection of widespread pyrethroid resistance and multiple resistance mechanisms highlights the urgency for implementing alternate Ae. aegypti control strategies. In addition, implementing routine monitoring of insecticide resistance in Ae. aegypti in Bangladesh will lead to a greater understanding of susceptibility trends over space and time, thereby enabling the development of improved control strategies.

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