Genome-wide divergence among invasive populations of Aedes aegypti in California

Y, Lee; Schmidt, Hanno; Collier, Travis C.; Conner, William R.; Hanemaaijer, Mark J.; Slatkin, Montgomery; Marshall, John M.; Chiu, Joanna C.; Smartt, Chelsea T.; Lanzaro, Gregory C.; Mulligan, F. S.; Cornel, Anthony J.

doi:10.1186/s12864-019-5586-4

Cited by 51 publications

(63 citation statements)

References 32 publications

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“…aegypti mosquitoes sampled throughout California, Florida, Mexico, and South Africa (Fig. S1, Table S1) (49). From this analysis, we discovered a putative gRNA target sequence in exon 3 of white (gRNA w ) that was 100% conserved in these wild populations ( Fig.…”

Section: Rational Target Site Selection For the Drivementioning

confidence: 99%

Development of a Confinable Gene-Drive System in the Human Disease Vector,Aedes aegypti

Li¹,

Yang²,

Kandul³

et al. 2019

Preprint

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Aedes aegypti, the principal mosquito vector for many arboviruses that causes yellow fever, dengue, Zika, and chikungunya, increasingly infects millions of people every year. With an escalating burden of infections and the relative failure of traditional control methods, the development of innovative control measures has become of paramount importance. The use of gene drives has recently sparked significant enthusiasm for the genetic control of mosquito populations, however no such system has been developed in Ae. aegypti. To fill this void and demonstrate efficacy in Ae. aegypti, here we develop several CRISPR-based split-gene drives for use in this vector. With cleavage rates up to 100% and transmission rates as high as 94%, 2 mathematical models predict that these systems could spread anti-pathogen effector genes into wild Ae. aegypti populations in a safe, confinable and reversible manner appropriate for field trials and effective for controlling disease. These findings could expedite the development of effectorlinked gene drives that could safely control wild populations of Ae. aegypti to combat local pathogen transmission. Significance StatementAe. aegypti is a globally distributed arbovirus vector spreading deadly pathogens to millions of people annually. Current control methods are inadequate and therefore new technologies need to be innovated and implemented. With the aim of providing new tools for controlling this pest, here we engineered and tested several split gene drives in this species. These drives functioned at very high efficiency and may provide a tool to fill the void in controlling this vector. Taken together, our results provide compelling path forward for the feasibility of future effector-linked split-drive technologies that can contribute to the safe, sustained control and potentially the elimination of pathogens transmitted by this species.

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Section: Rational Target Site Selection For the Drivementioning

confidence: 99%

Development of a Confinable Gene-Drive System in the Human Disease Vector,Aedes aegypti

Li¹,

Yang²,

Kandul³

et al. 2019

Preprint

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“…Using ddRADseq, Burford Reiskind, Labadie, Bargielowski, Lounibos, and Reiskind (2018) show differentiation between the four Florida populations included in their analysis. Previous work with microsatellite and SNP chip data (Gloria‐Soria, Brown, Kramer, Yoshimizu, & Powell, 2014; Pless et al., 2017), as well as whole‐genome sequencing data (Lee et al., 2019), indicates multiple invasions of Ae. aegypti into California, probably at least one from the US southeast and one from the US southwest and/or northern Mexico.…”

Section: Introductionmentioning

confidence: 99%

“…Previous work with microsatellite and SNP chip data (Gloria-Soria, Brown, Kramer, Yoshimizu, & Powell, 2014;Pless et al, 2017), as well as whole-genome sequencing data (Lee et al, 2019), indicates multiple invasions of Ae. aegypti into California, probably at least one from the US southeast and one from the US southwest and/or F I G U R E 1 Aedes aegypti (a) sampling sites in southern California (b) and Florida (c), showing region size and sampling design.…”

mentioning

confidence: 99%

Sunshine versus gold: The effect of population age on genetic structure of an invasive mosquito

Pless

Hopperstad

Ledesma

et al. 2020

Ecology and Evolution

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The genetic diversity and structure of invasive species are affected by the time since invasion, but it is not well understood how. We compare likely the oldest populations of Aedes aegypti in continental North America with some of the newest to illuminate the range of genetic diversity and structure that can be found within the invasive range of this important disease vector. Aedes aegypti populations in Florida have probably persisted since the 1600‐1700s, while populations in southern California derive from new invasions that occurred in the last 10 years. For this comparison, we genotyped 1,193 individuals from 28 sites at 12 highly variable microsatellites and a subset of these individuals at 23,961 single nucleotide polymorphisms (SNPs). This is the largest sample analyzed for genetic structure for either region, and it doubles the number of southern California populations previously analyzed. As predicted, the older populations (Florida) showed fewer indicators of recent founder effect and bottlenecks; in particular, these populations have dramatically higher genetic diversity and lower genetic structure. Geographic distance and driving distance were not good predictors of genetic distance in either region, especially southern California. Additionally, southern California had higher levels of genetic differentiation than any comparably sized documented region throughout the worldwide distribution of the species. Although population age and demographic history are likely driving these differences, differences in climate and transportation practices could also play a role.

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“…While a dramatic reduction in malaria-related deaths was seen in the early part of this century, progress has halted since 2015 (Bhatt et al, 2015; Feachem et al, 2019), and models predict that elimination is not possible in the majority of disease-endemic countries with currently available tools (Walker et al, 2016). The burden of other vector-borne diseases is on the rise, with dengue incidence and mortality increasing in much of the world (Stanaway et al, 2016), Zika recently sweeping through Latin America and the Caribbean (O’Reilly et al, 2018), and the mosquito species responsible for vectoring these diseases, Aedes aegypti and Aedes albopictus , greatly expanding their geographic range (Kraemer et al, 2015; Lee et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

“…Ae. aegypti -transmitted arboviruses are of particular concern at present, as the mosquito vector has rapidly expanded its range in recent years (Huang et al, 2017; Lee et al, 2019; Ryan et al, 2019). In response, a variety of approaches have recently been taken to engineer mosquitoes refractory to these diseases, including: i) transgene-based RNA interference (RNAi) in the midgut (Franz et al, 2006) and salivary glands (Mathur et al, 2010), ii) expression of synthetic miRNAs (Buchman et al, 2019b), iii) use of broadly neutralizing, single-chain variable fragments (scFv) (Buchman et al, 2019a), iv) use of antiviral hammerhead enzymes (Mishra et al, 2016), and v) transgenic activation of antiviral pathways (Jupatanakul et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Winning the Tug-of-War Between Effector Gene Design and Pathogen Evolution in Vector Population Replacement Strategies

et al. 2019

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While efforts to control malaria with available tools have stagnated, and arbovirus outbreaks persist around the globe, the advent of clustered regularly interspaced short palindromic repeat (CRISPR)-based gene editing has provided exciting new opportunities for genetics-based strategies to control these diseases. In one such strategy, called “population replacement”, mosquitoes, and other disease vectors are engineered with effector genes that render them unable to transmit pathogens. These effector genes can be linked to “gene drive” systems that can bias inheritance in their favor, providing novel opportunities to replace disease-susceptible vector populations with disease-refractory ones over the course of several generations. While promising for the control of vector-borne diseases on a wide scale, this sets up an evolutionary tug-of-war between the introduced effector genes and the pathogen. Here, we review the disease-refractory genes designed to date to target Plasmodium falciparum malaria transmitted by Anopheles gambiae, and arboviruses transmitted by Aedes aegypti, including dengue serotypes 2 and 3, chikungunya, and Zika viruses. We discuss resistance concerns for these effector genes, and genetic approaches to prevent parasite and viral escape variants. One general approach is to increase the evolutionary hurdle required for the pathogen to evolve resistance by attacking it at multiple sites in its genome and/or multiple stages of development. Another is to reduce the size of the pathogen population by other means, such as with vector control and antimalarial drugs. We discuss lessons learned from the evolution of resistance to antimalarial and antiviral drugs and implications for the management of resistance after its emergence. Finally, we discuss the target product profile for population replacement strategies for vector-borne disease control. This differs between early phase field trials and wide-scale disease control. In the latter case, the demands on effector gene efficacy are great; however, with new possibilities ushered in by CRISPR-based gene editing, and when combined with surveillance, monitoring, and rapid management of pathogen resistance, the odds are increasingly favoring effector genes in the upcoming evolutionary tug-of-war.

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Genome-wide divergence among invasive populations of Aedes aegypti in California

Cited by 51 publications

References 32 publications

Development of a Confinable Gene-Drive System in the Human Disease Vector,Aedes aegypti

Development of a Confinable Gene-Drive System in the Human Disease Vector,Aedes aegypti

Sunshine versus gold: The effect of population age on genetic structure of an invasive mosquito

Winning the Tug-of-War Between Effector Gene Design and Pathogen Evolution in Vector Population Replacement Strategies

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