Slow and steady wins the race: spatial and stochastic processes and the failure of suppression gene drives

Abstract

Gene drives that skew sex ratios offer a new management tool to suppress or eradicate pest populations. Early models and empirical work suggest that these suppression drives can completely eradicate well-mixed populations, but models that incorporate stochasticity and space (i.e., drift, and founder events) often result in loss or failure of the drive. We developed a stochastic model to examine these processes in a simple 1-dimensional space. This simple space allows us to map the events and outcomes that emerged and examine how properties of the drive’s wave of invasion affect outcomes. Our simulations, across a biologically-realistic section of parameter space, suggest that drive failure might be a common outcome in spatially explicit, stochastic systems, and that properties of the drive wave appear to mediate outcomes. Surprisingly, the drives that would be considered fittest in an aspatial model were strongly associated with failure in the spatial setting. The fittest drives cause fast moving, narrow drive waves that have a high chance of being penetrated by founder events, leading to failure. Our results also show that high rates of dispersal reduce the chance of failure because drive waves get disproportionately wider as dispersal rates increase. Overall, wide, slow-moving drive waves were much less prone to failure. Our results point to the complexity inherent in using a genetic system to effect demographic outcomes and speak to a clear need for ecological and evolutionary modelling to inform the drive design process.

Controlling the frequency dynamics of homing gene drives for intermediate outcomes

“…2019) or the gene drive allele frequency reaching an equilibrium within population (Unckless et al 2015; Rode et al 2019). The intermediate outcomes, either through transience or equilibrium, are often overlooked in gene drive models in favor of the more extreme fixation or loss outcomes when intending to suppress a population (Backus and Gross 2016; Paril and Phillips 2022). However, these outcomes could be of great relevance under specific scenario of population management.…”

“…Four distinct outcomes have been described for gene drives: the fixation of the gene drive allele, the loss of the gene drive allele (Gantz and Bier 2016), the transient establishment of the gene drive allele (Drury et al 2017;Noble et al 2019) or the gene drive allele frequency reaching an equilibrium within population (Unckless et al 2015;Rode et al 2019). The intermediate outcomes, either through transience or equilibrium, are often overlooked in gene drive models in favor of the more extreme fixation or loss outcomes when intending to suppress a population (Backus and Gross 2016;Paril and Phillips 2022). However, these outcomes could be of great relevance under specific scenario of population management.…”

Adversarial interspecies relationships facilitate population suppression by gene drive in spatially explicit models

“…In this situation, wild-type individuals might benefit from the lack of competition in empty areas cleared by the drive, allowing them to quickly reproduce before the drive arrive again from an adjacent region. The drive and wild-type alleles could coexist until the end of simulation, with the drive "chasing" the wild-type alleles but never eliminating them all [15][16][17][18][19][20] . To avoid this situation and quickly eliminate a population, higher overall drive quality is required 15,17 .…”