Gene drives have shown great promise for suppression of pest populations. These engineered alleles can function by a variety of mechanisms, but the most common is the CRISPR homing drive, which converts wild-type alleles to drive alleles in the germline of heterozygotes. Some potential target species are haplodiploid, in which males develop from unfertilized eggs and thus have only one copy of each chromosome. This prevents drive conversion, a substantial disadvantage compared to diploids where drive conversion can take place in both sexes. Here, we study homing suppression gene drives in haplodiploids and find that a drive targeting a female fertility gene could still be successful. However, such drives are less powerful than in diploids and suffer more from functional resistance alleles. They are substantially more vulnerable to high resistance allele formation in the embryo owing to maternally deposited Cas9 and guide RNA and also to somatic cleavage activity. Examining spatial models where organisms move over a continuous landscape, we find that haplodiploid suppression drives surprisingly perform nearly as well as in diploids, possibly owing to their ability to spread further before inducing strong suppression. Together, these results indicate that gene drive can potentially be used to effectively suppress haplodiploid populations. 

Modelling homing suppression gene drive in haplodiploid organisms

Hornets are large, predatory wasps that have the potential to alter biotic communities and harm honey bee colonies once established in non-native locations. Mated, diapausing females (gynes) can easily be transported to new habitats, where their behavioral flexibility allows them to found colonies using local food and nest materials. Of the 22 species in the genus Vespa, five species are now naturalized far from their endemic populations and another four have been detected either in nature or during inspections at borders of other countries. By far the most likely pathway of long-distance dispersal is the transport of gynes in transoceanic shipments of goods. Thereafter, natural dispersal of gynes in spring and accidental local transport by humans cause shorter-range expansions and contribute to the invasion process. Propagule pressure of hornets is unquantified, although it is likely low but unrelenting. The success of introduced populations is limited by low propagule size and the consequences of genetic founder effects, including the extinction vortex linked to single-locus, complementary sex determination of most hymenopterans. Invasion success is enhanced by climatic similarity between source locality and introduction site, as well as genetic diversity conferred by polyandry in some species. These and other factors that may have influenced the successful establishment of invasive populations of V. velutina, V. tropica, V. bicolor, V. orientalis, and V. crabro are discussed. The highly publicized detections of V. mandarinia in North America and research into its status provide a real-time example of an unfolding hornet invasion.

/pdf/invasion-potential-of-hornets-hymenoptera-vespidae-vespa-spp-1uhfq22a.pdf

Invasion potential of hornets (Hymenoptera: Vespidae: Vespa spp.)

Abstract Social insects are very successful invasive species, and the continued increase of global trade and transportation has exacerbated this problem. The yellow-legged hornet, Vespa velutina nigrithorax (henceforth Asian hornet), is drastically expanding its range in Western Europe. As an apex insect predator, this hornet poses a serious threat to the honey bee industry and endemic pollinators. Current suppression methods have proven too inefficient and expensive to limit its spread. Gene drives might be an effective tool to control this species, but their use has not yet been thoroughly investigated in social insects. Here, we built a model that matches the hornet’s life history and modelled the effect of different gene drive scenarios on an established invasive population. To test the broader applicability and sensitivity of the model, we also incorporated the invasive European paper wasp Polistes dominula . We find that, due to the haplodiploidy of social hymenopterans, only a gene drive targeting female fertility is promising for population control. Our results show that although a gene drive can suppress a social wasp population, it can only do so under fairly stringent gene drive-specific conditions. This is due to a combination of two factors: first, the large number of surviving offspring that social wasp colonies produce make it possible that, even with very limited formation of resistance alleles, such alleles can quickly spread and rescue the population. Second, due to social wasp life history, infertile individuals do not compete with fertile ones, allowing fertile individuals to maintain a large population size even when drive alleles are widespread. Nevertheless, continued improvements in gene drive technology may make it a promising method for the control of invasive social insects in the future. 

/pdf/the-suppressive-potential-of-a-gene-drive-in-populations-of-1uh3bxel.pdf

The suppressive potential of a gene drive in populations of invasive social wasps is currently limited

Gene drives have shown great promise for suppression of pest populations. These engineered alleles can function by a variety of mechanisms, but the most common is the CRISPR homing drive, which converts wild-type alleles to drive alleles in the germline of heterozygotes. Some potential target species are haplodiploid, in which males develop from unfertilized eggs and thus have only one copy of each chromosome. This prevents drive conversion, a substantial disadvantage compared to diploids where drive conversion can take place in both sexes. Here, we study the characteristics of homing suppression gene drives in haplodiploids and find that a drive targeting a female fertility gene could still be successful. However, such drives are less powerful than in diploids. They are substantially more vulnerable to high resistance allele formation in the embryo due to maternally deposited Cas9 and gRNA and also to somatic cleavage activity. Examining models of continuous space where organisms move over a landscape, we find that haplodiploid suppression drives surprisingly perform nearly as well as in diploids, possibly due to their ability to spread further before inducing strong suppression. Together, these results indicate that gene drive can potentially be used to effectively suppress haplodiploid populations.

/pdf/modeling-homing-suppression-gene-drive-in-haplodiploid-3das5ng6rs.pdf

Modeling homing suppression gene drive in haplodiploid organisms

<p indent="0mm">Gene drive refers to the phenomenon that specific genes or genetic elements are passed from parent to offspring in the form of super-Mendelian inheritance. In recent years, based on the genetic characteristics of gene drive and the theoretical basis of their molecular mechanisms, and supported by CRISPR/Cas9 gene-editing system, gene-driven genetic control technology has become an advanced research hotspot in the field of basic mosquito biology and genetic control. And there have emerged some practical and effective achievements that take into account ecological stability. This paper reviews the basic principles of gene drive, CRISPR/Cas9-mediated and HDR-type drive technology strategies, improved strategies to reduce gene-driven resistance and potential risks, and simulation analysis of gene drive. It is hoped to provide a reference for the development of a gene-driven mosquito genetic control technology system that takes both high efficiency and safety into consideration. 

CRISPR/Cas9介导的HDR型基因驱动技术在蚊虫遗传防控中的研究进展

Varroa mites (Varroa destructor) are the most significant threat to beekeeping worldwide. They are directly or indirectly responsible for millions of colony losses each year. Beekeepers are somewhat able to control varroa populations through the use of physical and chemical treatments. However, these methods range in effectiveness, can harm honey bees, can be physically demanding on the beekeeper, and do not always provide complete protection from varroa. More importantly, in some populations varroa mites have developed resistance to available acaricides. Overcoming the varroa mite problem will require novel and targeted treatment options. Here, we explore the potential of gene drive technology to control varroa. We show that spreading a neutral gene drive in varroa is possible but requires specific colony-level management practices to overcome the challenges of both inbreeding and haplodiploidy. Furthermore, continued treatment with acaricides is necessary to give a gene drive time to fix in the varroa population. Unfortunately, a gene drive that impacts female or male fertility does not spread in varroa. Therefore, we suggest that the most promising way forward is to use a gene drive which carries a toxin precursor or removes acaricide resistance alleles.

/pdf/a-gene-drive-does-not-spread-easily-in-populations-of-the-4szdz3z0gw.pdf

A gene drive does not spread easily in populations of the honey bee parasite Varroa destructor

Varroa mites (Varroa destructor) are the most significant threat to beekeeping worldwide. They are directly or indirectly responsible for millions of colony losses each year. Beekeepers are somewhat able to control Varroa populations through the use of physical and chemical treatments. However, these methods range in effectiveness, can harm honey bees, can be physically demanding on the beekeeper, and do not always provide complete protection from Varroa. More importantly, in some populations Varroa mites have developed resistance to available acaricides. Overcoming the Varroa mite problem will require novel and targeted treatment options. Here, we explore the potential of gene drive technology to control Varroa. We show that spreading a neutral gene drive in Varroa is possible but requires specific colony-level management practices to overcome the challenges of both inbreeding and haplodiploidy. Furthermore, continued treatment with acaricides is necessary to give a gene drive time to fix in the Varroa population. Unfortunately, a gene drive that impacts female or male fertility does not spread in Varroa. Therefore, we suggest that the most promising way forward is to use a gene drive which carries a toxin precursor or removes acaricide resistance alleles.

/pdf/a-gene-drive-does-not-spread-easily-in-populations-of-the-13xxhjvb1s.pdf

Social insects are very successful invasive species, and the continued increase of global trade and transportation has exacerbated this problem. The yellow-legged hornet, Vespa velutina nigrithorax (henceforth Asian hornet), is drastically expanding its range in Western Europe. As an apex insect predator, this hornet poses a serious threat to the honey bee industry and endemic pollinators. Current suppression methods have proven too inefficient and expensive to limit its spread. Gene drives might be an effective tool to control this species, but their use has not yet been thoroughly investigated in social insects. Here, we built a model that matches the hornet’s life history and modelled the effect of different gene drive scenarios on an established invasive population. To test the broader applicability and sensitivity of the model, we also incorporated the invasive European paper wasp Polistes dominula . We find that although a gene drive can spread through a social wasp population, it can only do so under stringent gene drive-specific conditions. The main issue is that the large number of offspring that social wasp colonies produce guarantees that, even with very limited formation of resistance alleles, such alleles will quickly spread and rescue the population. Furthermore, we find that only a gene drive targeting female fertility is promising for population control due to the haplodiploidy of social insects. Nevertheless, continued improvements in gene drive technology may make it a promising method for the control of invasive social insects. 

Adriaan B. Meiborg

Papers

A gene drive does not spread easily in populations of the honey bee parasite Varroa destructor

The suppressive potential of a gene drive in populations of invasive social wasps is currently limited

A gene drive does not spread easily in populations of the honey bee parasite Varroa destructor

The suppressive potential of a gene drive in populations of invasive social wasps is currently limited