Publications
123 results found
Burt A, Crisanti A, 2018, Editorial: gene drive for vector control, Pathogens and Global Health, Vol: 111, Pages: 397-398, ISSN: 2047-7724
Burt A, Crisanti A, 2018, Gene drive: evolved and synthetic, ACS Chemical Biology, Vol: 13, Pages: 343-346, ISSN: 1554-8929
Drive is a process of accelerated inheritance from one generation to the next that allows some genes to spread rapidly through populations even if they do not contribute to-or indeed even if they detract from-organismal survival and reproduction. Genetic elements that can spread by drive include gametic and zygotic killers, meiotic drivers, homing endonuclease genes, B chromosomes, and transposable elements. The fact that gene drive can lead to the spread of fitness-reducing traits (including lethality and sterility) makes it an attractive process to consider exploiting to control disease vectors and other pests. There are a number of efforts to develop synthetic gene drive systems, particularly focused on the mosquito-borne diseases that continue to plague us.
Burt A, Coulibaly M, Crisanti A, et al., 2018, Gene drive to reduce malaria transmission in sub-Saharan Africa, Journal of Responsible Innovation, Vol: 5, Pages: S66-S80, ISSN: 2329-9460
Despite impressive progress, malaria continues to impose a substantial burden of mortality and morbidity, particularly in sub-Saharan Africa, and new tools will be needed to achieve elimination. Gene drive is a natural process by which some genes are inherited at a greater-than-Mendelian rate and can spread through a population even if they cause harm to the organisms carrying them. Many different synthetic gene drive systems have been proposed to suppress the number of mosquitoes and/or reduce vector competence. As with any control measure, due attention should be paid to the possible evolution of resistance. No gene drive construct has yet been reported that is ‘field-ready’ for release, and when such constructs are developed, they should be assessed on a case-by-case basis. Gene drive approaches to vector control promise to have a number of key features that motivate their continued development, and scrutiny, by all concerned.
Benedict MQ, Burt A, Capurro ML, et al., 2018, Recommendations for Laboratory Containment and Management of Gene Drive Systems in Arthropods, VECTOR-BORNE AND ZOONOTIC DISEASES, Vol: 18, Pages: 2-13, ISSN: 1530-3667
Nikolov M, Ouedraogo A, Beaghton A, et al., 2018, POPULATION SEASONALITY AND RELEASE TIMING SIGNIFICANTLY AFFECT THE PROBABILITY OF ESTABLISHMENT FOR SMALL RELEASES OF GENE DRIVE MOSQUITOES, 67th Annual Meeting of the American-Society-of-Tropical-Medicine-and-Hygiene (ASTHM), Publisher: AMER SOC TROP MED & HYGIENE, Pages: 367-367, ISSN: 0002-9637
Miles A, Kwiatkowski D, Lawniczak M, et al., 2018, THE MALARIAGEN VECTOR OBSERVATORY: A NETWORK FOR THE GENOMIC SURVEILLANCE OF MALARIA VECTORS IN AFRICA AND SOUTHEAST ASIA, 67th Annual Meeting of the American-Society-of-Tropical-Medicine-and-Hygiene (ASTHM), Publisher: AMER SOC TROP MED & HYGIENE, Pages: 12-13, ISSN: 0002-9637
Eckhoff PA, Wenger EA, Godfray HC, et al., 2017, Impact of mosquito gene drive on malaria elimination in a computational model with explicit spatial and temporal dynamics, Proceedings of the National Academy of Sciences of the United States of America, Vol: 114, Pages: E255-E264, ISSN: 1091-6490
The renewed effort to eliminate malaria and permanently remove its tremendous burden highlights questions of what combination of tools would be sufficient in various settings and what new tools need to be developed. Gene drive mosquitoes constitute a promising set of tools, with multiple different possible approaches including population replacement with introduced genes limiting malaria transmission, driving-Y chromosomes to collapse a mosquito population, and gene drive disrupting a fertility gene and thereby achieving population suppression or collapse. Each of these approaches has had recent success and advances under laboratory conditions, raising the urgency for understanding how each could be deployed in the real world and the potential impacts of each. New analyses are needed as existing models of gene drive primarily focus on nonseasonal or nonspatial dynamics. We use a mechanistic, spatially explicit, stochastic, individual-based mathematical model to simulate each gene drive approach in a variety of sub-Saharan African settings. Each approach exhibits a broad region of gene construct parameter space with successful elimination of malaria transmission due to the targeted vector species. The introduction of realistic seasonality in vector population dynamics facilitates gene drive success compared with nonseasonal analyses. Spatial simulations illustrate constraints on release timing, frequency, and spatial density in the most challenging settings for construct success. Within its parameter space for success, each gene drive approach provides a tool for malaria elimination unlike anything presently available. Provided potential barriers to success are surmounted, each achieves high efficacy at reducing transmission potential and lower delivery requirements in logistically challenged settings.
Miles A, Harding NJ, Botta G, et al., 2017, Genetic diversity of the African malaria vector Anopheles gambiae, Nature, Vol: 552, Pages: 96-100, ISSN: 0028-0836
The sustainability of malaria control in Africa is threatened by the rise of insecticide resistance in Anopheles mosquitoes, which transmit the disease1. To gain a deeper understanding of how mosquito populations are evolving, here we sequenced the genomes of 765 specimens of Anopheles gambiae and Anopheles coluzzii sampled from 15 locations across Africa, and identified over 50 million single nucleotide polymorphisms within the accessible genome. These data revealed complex population structure and patterns of gene flow, with evidence of ancient expansions, recent bottlenecks, and local variation in effective population size. Strong signals of recent selection were observed in insecticide-resistance genes, with several sweeps spreading over large geographical distances and between species. The design of new tools for mosquito control using gene-drive systems will need to take account of high levels of genetic diversity in natural mosquito populations.
Godfray HCJ, North A, Burt A, 2017, How driving endonuclease genes can be used to combat pests and disease vectors, BMC Biology, Vol: 15, ISSN: 1741-7007
Driving endonuclease genes (DEGs) spread through a population by a non-Mendelian mechanism. In a heterozygote,the protein encoded by a DEG causes a double-strand break in the homologous chromosome opposite to where itsgene is inserted and when the break is repaired using the homologue as a template the DEG heterozygote is convertedto a homozygote. Some DEGs occur naturally while several classes of endonucleases can be engineered to spread in thisway, with CRISPR-Cas9 based systems being particularly flexible. There is great interest in using driving endonucleasegenes to impose a genetic load on insects that vector diseases or are economic pests to reduce their population density,or to introduce a beneficial gene such as one that might interrupt disease transmission. This paper reviews both thepopulation genetics and population dynamics of DEGs. It summarises the theory that guides the design of DEG constructsintended to perform different functions. It also reviews the studies that have explored the likelihood of resistance to DEGphenotypes arising, and how this risk may be reduced. The review is intended for a general audience and mathematicaldetails are kept to a minimum.
Beaghton AK, Beaghton PJ, Burt A, 2017, Vector control with driving Y chromosomes: modelling the evolution of resistance, Malaria Journal, Vol: 16, ISSN: 1475-2875
BackgroundThe introduction of new malaria control interventions has often led to the evolution of resistance, both of the parasite to new drugs and of the mosquito vector to new insecticides, compromising the efficacy of the interventions. Recent progress in molecular and population biology raises the possibility of new genetic-based interventions, and the potential for resistance to evolve against these should be considered. Here, population modelling is used to determine the main factors affecting the likelihood that resistance will evolve against a synthetic, nuclease-based driving Y chromosome that produces a male-biased sex ratio. MethodsA combination of deterministic differential equation models and stochastic analyses involving branching processes and Gillespie simulations is utilized to assess the probability that resistance evolves against a driving Y that otherwise is strong enough to eliminate the target population. The model considers resistance due to changes at the target site such that they are no longer cleaved by the nuclease, and due to trans-acting autosomal suppressor alleles. ResultsThe probability that resistance evolves increases with the mutation rate and the intrinsic rate of increase of the population, and decreases with the strength of drive and any pleiotropic fitness costs of the resistant allele. In seasonally varying environments, the time of release can also affect the probability of resistance evolving. Trans-acting suppressor alleles are more likely to suffer stochastic loss at low frequencies than target site resistant alleles. ConclusionsAs with any other intervention, there is a risk that resistance will evolve to new genetic approaches to vector control, and steps should be taken to minimize this probability. Two design features that should help in this regard are to reduce the rate at which resistant mutations arise, and to target sequences such that if they do arise, they impose a significant fitness cost on the mosquito.
Beaghton A, Hammond A, Nolan T, et al., 2017, Requirements for Driving Antipathogen Effector Genes into Populations of Disease Vectors by Homing, Genetics, Vol: 205, Pages: 1587-1596
Davies SK, Leroi A, Burt A, et al., 2016, The mutational structure of metabolism in Caenorhabditis elegans., Evolution, Vol: 70, Pages: 2239-2246, ISSN: 0014-3820
A properly functioning organism must maintain metabolic homeostasis. Deleterious mutations degrade organismal function, presumably at least in part via effects on metabolic function. Here we present an initial investigation into the mutational structure of the Caenorhabditis elegans metabolome by means of a mutation accumulation experiment. We find that pool sizes of 29 metabolites vary greatly in their vulnerability to mutation, both in terms of the rate of accumulation of genetic variance (the mutational variance, VM) and the rate of change of the trait mean (the mutational bias, ΔM). Strikingly, some metabolites are much more vulnerable to mutation than any other trait previously studied in the same way. Although we cannot statistically assess the strength of mutational correlations between individual metabolites, principal component analysis provides strong evidence that some metabolite pools are genetically correlated, but also that there is substantial scope for independent evolution of different groups of metabolites. Averaged over MA lines, PC3 is positively correlated with relative fitness, but a model in which metabolites are uncorrelated with fitness is nearly as good by Akaike's Information Criterion (AIC). This article is protected by copyright. All rights reserved.
Beaghton A, Beaghton PJ, Burt A, 2016, Gene drive through a landscape: Reaction–diffusion models of population suppression and elimination by a sex ratio distorter, Theoretical Population Biology, Vol: 108, Pages: 51-69, ISSN: 1096-0325
Some genes or gene complexes are transmitted from parents to offspring at a greater-than-Mendelian rate, and can spread and persist in populations even if they cause some harm to the individuals carrying them. Such genes may be useful for controlling populations or species that are harmful. Driving-Y chromosomes may be particularly potent in this regard, as they produce a male-biased sex ratio that, if sufficiently extreme, can lead to population elimination. To better understand the potential of such genes to spread over a landscape, we have developed a series of reaction–diffusion models of a driving-Y chromosome in 1-D and radially-symmetric 2-D unbounded domains. The wild-type system at carrying capacity is found to be unstable to the introduction of driving-Y males for all models investigated. Numerical solutions exhibit travelling wave pulses and fronts, and analytical and semi-analytical solutions for the asymptotic wave speed under bounded initial conditions are derived. The driving-Y male invades the wild-type equilibrium state at the front of the wave and completely replaces the wild-type males, leaving behind, at the tail of the wave, a reduced- or zero-population state of females and driving-Y males only. In our simplest model of a population with one life stage and density-dependent mortality, wave speed depends on the strength of drive and the diffusion rate of Y-drive males, and is independent of the population dynamic consequences (suppression or elimination). Incorporating an immobile juvenile stage of fixed duration into the model reduces wave speed approximately in proportion to the relative time spent as a juvenile. If females mate just once in their life, storing sperm for subsequent reproduction, then wave speed depends on the movement of mated females as well as Y-drive males, and may be faster or slower than in the multiple-mating model, depending on the relative duration of juvenile and adult life stages. Numerical solutions are shown
O'Loughlin SM, Magesa SM, Mbogo C, et al., 2016, Genomic signatures of population decline in the malaria mosquito Anopheles gambiae, Malaria Journal, Vol: 15, ISSN: 1475-2875
BACKGROUND: Population genomic features such as nucleotide diversity and linkage disequilibrium are expected to be strongly shaped by changes in population size, and might therefore be useful for monitoring the success of a control campaign. In the Kilifi district of Kenya, there has been a marked decline in the abundance of the malaria vector Anopheles gambiae subsequent to the rollout of insecticide-treated bed nets. METHODS: To investigate whether this decline left a detectable population genomic signature, simulations were performed to compare the effect of population crashes on nucleotide diversity, Tajima's D, and linkage disequilibrium (as measured by the population recombination parameter ρ). Linkage disequilibrium and ρ were estimated for An. gambiae from Kilifi, and compared them to values for Anopheles arabiensis and Anopheles merus at the same location, and for An. gambiae in a location 200 km from Kilifi. RESULTS: In the first simulations ρ changed more rapidly after a population crash than the other statistics, and therefore is a more sensitive indicator of recent population decline. In the empirical data, linkage disequilibrium extends 100-1000 times further, and ρ is 100-1000 times smaller, for the Kilifi population of An. gambiae than for any of the other populations. There were also significant runs of homozygosity in many of the individual An. gambiae mosquitoes from Kilifi. CONCLUSIONS: These results support the hypothesis that the recent decline in An. gambiae was driven by the rollout of bed nets. Measuring population genomic parameters in a small sample of individuals before, during and after vector or pest control may be a valuable method of tracking the effectiveness of interventions.
Deredec A, O'Loughlin SM, Hui T-YJ, et al., 2016, Partitioning the contributions of alternative malaria vector species, Malaria Journal, Vol: 15, ISSN: 1475-2875
BackgroundIn many locations malaria is transmitted by more than one vector species. Some vector control interventions, in particular those using genetic approaches, are likely to be targeted against a single species or species complex, at least initially, and it would therefore be useful to be able to predict the epidemiological impact of controlling a single species when multiple vector species are present.MethodsTo address this issue, the classical Ross-McDonald model of malaria epidemiology is expanded to account for multiple vector species, giving expressions for the equilibrium prevalence, sporozoite rates and reproductive number. These allow one to predict when control of just one vector species will lead to elimination of the disease. Application of the model is illustrated using published data from a particularly extensive entomological and epidemiological survey before the rollout of bed nets in eastern Kenya, where Anopheles gambiae s.l. and An. funestus were vectors.ResultsMeta-analysis indicates that sporozoite rates were 38 % higher in An. gambiae s.l. than in An. funestus, and, according to the model, this difference could be due to An. gambiae s.l. having a higher frequency of feeding on humans, a higher human-to-mosquito transmission rate, a lower adult mortality rate, and/or a shorter incubation period. Further calculations suggest that An. gambiae s.l. would have been sufficient to maintain transmission by itself throughout the region, whereas An. funestus would not have been able to support transmission by itself in Malindi District.ConclusionsPartitioning the contributions of different vector species may allow us to predict whether malaria will persist after targeted vector control.
Hammond A, Galizi R, Kyrou K, et al., 2016, A CRISPR-Cas9 gene drive system-targeting female reproduction in the malaria mosquito vector Anopheles gambiae, Nature Biotechnology, Vol: 34, Pages: 78-83, ISSN: 1087-0156
Gene drive systems that enable super-Mendelian inheritance of a transgene have the potential to modify insect populations over a timeframe of a few years. We describe CRISPR-Cas9 endonuclease constructs that function as gene drive systems in Anopheles gambiae, the main vector for malaria. We identified three genes (AGAP005958, AGAP011377 and AGAP007280) that confer a recessive female-sterility phenotype upon disruption, and inserted into each locus CRISPR-Cas9 gene drive constructs designed to target and edit each gene. For each targeted locus we observed a strong gene drive at the molecular level, with transmission rates to progeny of 91.4 to 99.6%. Population modeling and cage experiments indicate that a CRISPR-Cas9 construct targeting one of these loci, AGAP007280, meets the minimum requirement for a gene drive targeting female reproduction in an insect population. These findings could expedite the development of gene drives to suppress mosquito populations to levels that do not support malaria transmission.
Akbari OS, Bellen HJ, Bier E, et al., 2015, Safeguarding gene drive experiments in the laboratory, SCIENCE, Vol: 349, Pages: 927-929, ISSN: 0036-8075
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- Citations: 179
Koufopanou V, Lomas S, Tsai IJ, et al., 2015, Estimating the fitness effects of new mutations in the wild yeast Saccharomyces paradoxus, Genome Biology and Evolution, Vol: 7, Pages: 1887-1895, ISSN: 1759-6653
The nature of selection acting on a population is in large measure determined by the distribution of fitness effects of new mutations. In this study, we use DNA sequences from four closely related clades of Saccharomyces paradoxus and Saccharomyces cerevisiae to identify and polarize new mutations and estimate their fitness effects. By progressively restricting the analyses to narrower categories of sites, we further seek to characterize sites with predictable mutational effects, that is, unconditionally deleterious, neutral or beneficial. Consistent with previous studies on S. paradoxus, we have failed to find evidence for mutations with beneficial effects, even in regions that were divergent in two outgroup clades, perhaps a consequence of the relatively unchallenged, predominantly asexual and highly inbred lifestyle of this species. On the other hand, there is abundant evidence of deleterious mutations, varying in severity of effect from strongly deleterious to very mild, particularly in regions conserved in the outgroup taxa, indicating a history of persistent purifying selection. Narrowing the analysis down to individual amino acids reduces further the range of effects: for example, mutations changing cysteine are predicted to be nearly always strongly deleterious, whereas those changing arginine, serine, and tyrosine are expected to be nearly neutral. The proportion of mutations with deleterious effects for a particular amino acid is correlated with long-term stasis of that amino acid among highly divergent sequences from a variety of organisms, showing that functionality of sites tends to persist through the diversification of clades and that our findings are also relevant to longer evolutionary times and other taxa.
Hui T-YJ, Burt A, 2015, Estimating effective population size from temporally spaced samples with a novel, efficient maximum-likelihood algorithm, Genetics, Vol: 200, Pages: 285-293, ISSN: 1943-2631
The effective population size Embedded Image is a key parameter in population genetics and evolutionary biology, as it quantifies the expected distribution of changes in allele frequency due to genetic drift. Several methods of estimating Embedded Image have been described, the most direct of which uses allele frequencies measured at two or more time points. A new likelihood-based estimator Embedded Image for contemporary effective population size using temporal data is developed in this article. The existing likelihood methods are computationally intensive and unable to handle the case when the underlying Embedded Image is large. This article tries to work around this problem by using a hidden Markov algorithm and applying continuous approximations to allele frequencies and transition probabilities. Extensive simulations are run to evaluate the performance of the proposed estimator Embedded Image, and the results show that it is more accurate and has lower variance than previous methods. The new estimator also reduces the computational time by at least 1000-fold and relaxes the upper bound of Embedded Image to several million, hence allowing the estimation of larger Embedded Image. Finally, we demonstrate how this algorithm can cope with nonconstant Embedded Image scenarios and be used as a likelihood-ratio test to test for the equality of Embedded Image throughout the sampling horizon. An R package “NB” is now available for download to implement the method described in this article.
Samani P, Low-Decarie E, McKelvey K, et al., 2015, Metabolic variation in natural populations of wild yeast, Ecology and Evolution, Vol: 5, Pages: 722-732, ISSN: 2045-7758
Ecological diversification depends on the extent of genetic variation and on the pattern of covariation with respect to ecological opportunities. We investigated the pattern of utilization of carbon substrates in wild populations of budding yeast Saccharomyces paradoxus. All isolates grew well on a core diet of about 10 substrates, and most were also able to grow on a much larger ancillary diet comprising most of the 190 substrates we tested. There was substantial genetic variation within each population for some substrates. We found geographical variation of substrate use at continental, regional, and local scales. Isolates from Europe and North America could be distinguished on the basis of the pattern of yield across substrates. Two geographical races at the North American sites also differed in the pattern of substrate utilization. Substrate utilization patterns were also geographically correlated at local spatial scales. Pairwise genetic correlations between substrates were predominantly positive, reflecting overall variation in metabolic performance, but there was a consistent negative correlation between categories of substrates in two cases: between the core diet and the ancillary diet, and between pentose and hexose sugars. Such negative correlations in the utilization of substrate from different categories may indicate either intrinsic physiological trade‐offs for the uptake and utilization of substrates from different categories, or the accumulation of conditionally neutral mutations. Divergence in substrate use accompanies genetic divergence at all spatial scales in S. paradoxus and may contribute to race formation and speciation.
Neafsey DE, Waterhouse RM, Abai MR, et al., 2015, Highly evolvable malaria vectors: The genomes of 16 Anopheles mosquitoes, Science, Vol: 347
Harrison E, MacLean RC, Koufopanou V, et al., 2014, Sex drives intracellular conflict in yeast, JOURNAL OF EVOLUTIONARY BIOLOGY, Vol: 27, Pages: 1757-1763, ISSN: 1010-061X
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- Citations: 7
Burt A, 2014, Heritable strategies for controlling insect vectors of disease, PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, Vol: 369, ISSN: 0962-8436
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- Citations: 139
Galizi R, Doyle LA, Menichelli M, et al., 2014, A synthetic sex ratio distortion system for the control of the human malaria mosquito, Nature Communications, Vol: 5, ISSN: 2041-1723
It has been theorized that inducing extreme reproductive sex ratios could be a method to suppress or eliminate pest populations. Limited knowledge about the genetic makeup and mode of action of naturally occurring sex distorters and the prevalence of co-evolving suppressors has hampered their use for control. Here we generate a synthetic sex distortion system by exploiting the specificity of the homing endonuclease I-PpoI, which is able to selectively cleave ribosomal gene sequences of the malaria vector Anopheles gambiae that are located exclusively on the mosquito’s X chromosome. We combine structure-based protein engineering and molecular genetics to restrict the activity of the potentially toxic endonuclease to spermatogenesis. Shredding of the paternal X chromosome prevents it from being transmitted to the next generation, resulting in fully fertile mosquito strains that produce >95% male offspring. We demonstrate that distorter male mosquitoes can efficiently suppress caged wild-type mosquito populations, providing the foundation for a new class of genetic vector control strategies.
O'Loughlin SM, Magesa S, Mbogo C, et al., 2014, Genomic Analyses of Three Malaria Vectors Reveals Extensive Shared Polymorphism but Contrasting Population Histories, MOLECULAR BIOLOGY AND EVOLUTION, Vol: 31, Pages: 889-902, ISSN: 0737-4038
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- Citations: 31
Murchison EP, Wedge DC, Alexandrov LB, et al., 2014, Transmissable Dog Cancer Genome Reveals the Origin and History of an Ancient Cell Lineage, SCIENCE, Vol: 343, Pages: 437-440, ISSN: 0036-8075
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- Citations: 109
O'Loughlin S, Burt A, 2013, INFERRING DEMOGRAPHY AND SELECTION IN EAST AFRICAN ANOPHELES GAMBIAE SL FROM GENOME WIDE SNPS, PATHOGENS AND GLOBAL HEALTH, Vol: 107, Pages: 416-416, ISSN: 2047-7724
Koufopanou V, Swire J, Lomas S, et al., 2013, Primers for fourteen protein-coding genes and the deep phylogeny of the true yeasts, FEMS YEAST RESEARCH, Vol: 13, Pages: 574-584, ISSN: 1567-1356
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North A, Burt A, Godfray HCJ, 2013, Modelling the spatial spread of a homing endonuclease gene in a mosquito population, Journal of Applied Ecology, Vol: 50, Pages: 1216-1225, ISSN: 1365-2664
1. Homing endonuclease genes (HEGs) exist naturally in many single-celled organisms and can show extremely strong genetic drive allowing them to spread through populations into which they are introduced. They are being investigated as tools to manipulate the populations of important vectors of human disease, in particular the mosquitoes that transmit malaria. Before HEGs can be deployed, it is important to study their spatial spread in order to design efficient release strategies.2. A spatially explicit model is developed to study the spread of a HEG through a landscape whose structure is defined by the distribution of mosquito breeding and feeding sites. The model is motivated by the biology of the major vectors of malaria in Africa. The conditions for spread, fixation and loss of two major types of HEG are explored in different landscapes.3. In landscapes where mosquito resources are abundant, the conditions for spread are well approximated by a mean-field model. Where a HEG imposes a genetic load, it can cause population extinction, though spatial models more often predict population suppression.4. In certain types of landscapes where mosquito resources are rare, an introduced HEG may be prevented from moving between local mosquito populations and so a simple release strategy is unlikely to be effective, yet if the HEG succeeds in spreading population extinction is a feasible outcome. Increasing the number of release sites at the expense of releasing fewer mosquitoes per site reduces the probability that a HEG will fail.5. Synthesis and applications. The model presented asks for the first time how the spatial structure of mosquito populations will influence the effectiveness of a technology that is being rapidly developed for vector control. If homing endonuclease genes (HEGs) are to be used in this way, we have qualified the importance of accounting for landscape characteristics in both the execution and the expectation of their application. The next stage is to
Leroi AM, MacCallum RM, Mauch M, et al., 2012, Reply to Claidiere et al.: Role of psychological bias in evolution depends on the kind of culture, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, Vol: 109, Pages: E3527-E3527, ISSN: 0027-8424
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