Gene-drive into insect populations with age and spatial structure: a theoretical assessment

The potential benefits and risks of genetically engineered gene‐drive systems for replacing wild pest strains with more benign strains must be assessed prior to any field releases. We develop a computer simulation model to assess the feasibility of using engineered underdominance constructs to drive transgenes into age‐ and spatially structured mosquito populations. Our practical criterion for success is the achievement of a transgene frequency of at least 0.80 within 3 years of release. The impacts of a number of parameters that may affect the success of gene‐drive, such as the release area, release age, density‐dependent larval survival, fitness cost of the engineered genes, and migration probability of adults, are examined. Results show that patchy release generally requires the release of fewer engineered insects to achieve success than central release. When the fitness cost is very low, central release covering 25% of the total area can be more effective than a completely uniform release over the whole area. This study demonstrates that to determine the best method of spatial release, and the total number of engineered insects that must be released, it is important to take into account the age and sex of the released insects and spatial structure of the population.

[1]  Willem Takken,et al.  The ecology of genetically modified mosquitoes. , 2002, Science.

[2]  Christopher Dye,et al.  Models for the population dynamics of the yellow fever mosquito, Aedes aegypti , 1984 .

[3]  T. Scott,et al.  Why Do Female Aedes aegypti (Diptera: Culicidae) Feed Preferentially and Frequently on Human Blood? , 2001, Journal of medical entomology.

[4]  M. Turelli,et al.  Rapid spread of an inherited incompatibility factor in California Drosophila , 1991, Nature.

[5]  M. Bonsall,et al.  Aedes aegypti control: the concomitant role of competition, space and transgenic technologies , 2008 .

[6]  A. L. Rae,et al.  Qualitative theory of the spread of a new gene into a resident population , 2003 .

[7]  J. Rasgon.  Population Subdivision Can Help or Hinder Wolbachia Introductions Into Vector Populations , 2003 .

[8]  J. Maynard Smith,et al.  The Stability of Predator‐Prey Systems , 1973 .

[9]  Mihály Kovács,et al.  Fractional Reproduction-Dispersal Equations and Heavy Tail Dispersal Kernels , 2007, Bulletin of mathematical biology.

[10]  Lawrence M. Wein,et al.  Analyzing the control of mosquito-borne diseases by a dominant lethal genetic system , 2007, Proceedings of the National Academy of Sciences.

[11]  P. McDonald.  Population characteristics of domestic Aedes aegypti (Diptera: culicidae) in villages on the Kenya Coast I. Adult survivorship and population size. , 1977, Journal of medical entomology.

[12]  Hugh P. Possingham,et al.  Population models for marine reserve design: A retrospective and prospective synthesis , 2003 .

[13]  T. Scott,et al.  Wolbachia-Induced Mortality as a Mechanism to Modulate Pathogen Transmission by Vector Arthropods , 2003, Journal of medical entomology.

[14]  P. Driessche,et al.  Dispersal data and the spread of invading organisms. , 1996 .

[15]  A. Lloyd,et al.  Density-Dependent Intraspecific Competition in the Larval Stage of Aedes aegypti (Diptera: Culicidae): Revisiting the Current Paradigm , 2009, Journal of medical entomology.

[16]  R. Levins.  The strategy of model building in population biology , 1966 .

[17]  M. Kot,et al.  Integrodifference equations, Allee effects, and invasions , 2002, Journal of mathematical biology.

[18]  P Grewe,et al.  Engineered underdominance allows efficient and economical introgression of traits into pest populations. , 2001, Journal of theoretical biology.

[19]  A. Lloyd,et al.  INTRODUCING DESIRABLE TRANSGENES INTO INSECT POPULATIONS USING Y-LINKED MEIOTIC DRIVE—A THEORETICAL ASSESSMENT , 2007, Evolution; international journal of organic evolution.

[20]  I. Kiss,et al.  A network approach to modeling population aggregation and genetic control of pest insects. , 2008, Theoretical population biology.

[21]  M. Hoddle,et al.  Assessing fitness costs for transgenic Aedes aegypti expressing the GFP marker and transposase genes. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[22]  M J Wade,et al.  The population dynamics of maternal-effect selfish genes. , 1994, Genetics.

[23]  S. Sinkins,et al.  Gene drive systems for insect disease vectors , 2006, Nature Reviews Genetics.

[24]  Michael Turelli,et al.  CYTOPLASMIC INCOMPATIBILITY IN POPULATIONS WITH OVERLAPPING GENERATIONS , 2010, Evolution; international journal of organic evolution.

[25]  A. Lloyd,et al.  Introducing transgenes into insect populations using combined gene-drive strategies: modeling and analysis. , 2007, Insect biochemistry and molecular biology.

[26]  P A Singer,et al.  Grand Challenges in Global Health , 2003, Science.

[27]  Paul Schliekelman,et al.  Population genetics of autocidal control and strain replacement. , 2004, Annual review of entomology.

[28]  A. James.  Gene drive systems in mosquitoes: rules of the road. , 2005, Trends in parasitology.

[29]  John B. Silver,et al.  Mosquito Ecology: Field Sampling Methods , 2008 .

[30]  T. Bellows.  The Descriptive Properties of Some Models for Density Dependence , 1981 .

[31]  A. Lloyd,et al.  Gene-drive in age-structured insect populations , 2008, Evolutionary applications.

[32]  M. Bonsall,et al.  Importance of Space and Competition in Optimizing Genetic Control Strategies , 2009, Journal of economic entomology.

[33]  T. Scott,et al.  Skeeter Buster: A Stochastic, Spatially Explicit Modeling Tool for Studying Aedes aegypti Population Replacement and Population Suppression Strategies , 2009, PLoS neglected tropical diseases.

[34]  T. Scott,et al.  Dispersal of the dengue vector Aedes aegypti within and between rural communities. , 2005, The American journal of tropical medicine and hygiene.

[35]  C. Curtis,et al.  History of the Sterile Insect Technique , 2021, Sterile Insect Technique.

[36]  P. Kareiva,et al.  Allee Dynamics and the Spread of Invading Organisms , 1993 .

[37]  P. Schofield.  Spatially explicit models of Turelli-Hoffmann Wolbachia invasive wave fronts. , 2002, Journal of theoretical biology.

[38]  Fred Gould,et al.  Genetically Engineered Underdominance for Manipulation of Pest Populations: A Deterministic Model , 2006, Genetics.

[39]  R. Fisher.  THE WAVE OF ADVANCE OF ADVANTAGEOUS GENES , 1937 .

[40]  T. Scott,et al.  Impact of population age structure on Wolbachia transgene driver efficacy: ecologically complex factors and release of genetically modified mosquitoes. , 2004, Insect biochemistry and molecular biology.

[41]  Claudia Torres Codeço,et al.  Daily survival rates and dispersal of Aedes aegypti females in Rio de Janeiro, Brazil. , 2007, The American journal of tropical medicine and hygiene.

[42]  N. Barton,et al.  The dynamics of hybrid zones , 1979, Heredity.