Mate choice against gene drives leads to evolutionary rescue

Abstract

Artificial gene drives offer a promising approach for controlling populations of agricultural pests, invasive species and disease vectors, such as malaria-carrying mosquitoes. Gene-drive alleles induce a transmission bias, meaning there is a greater than 50% probability that they will be inherited by offspring, facilitating their rapid propagation through populations. When these alleles induce high fitness costs, their spread can lead to the eradication of target populations. While gene drives hold great potential, there are various barriers that can hinder their effectiveness. One such barrier, precopulatory mate choice, has been suggested to impact the spread of gene drives, yet it remains underexplored. Here, we use individual-based simulations to investigate the spread of gene drives while allowing female mating preferences to evolve. In our model, gene-drive alleles exhibit transmission bias but also incur survival costs. Crucially, females are assumed to be able to distinguish between drive carriers and wild-type males based on drive-associated phenotypic differences. Consequently, females can evolve to prefer wild- type or drive-carrying males as mates. Our simulations show that under certain parameter settings, mating preferences against drive carriers can evolve during the spread of a gene drive. This can result in the eradication of the drive alleles and the evolutionary rescue of the population. The impact of mate choice was most pronounced when the gene drive spread relatively slowly, as this allowed more time for preferences against drives to evolve. In addition, evolutionary rescue occurred less frequently for recessive drives than for dominant ones. Our results demonstrate that mate choice can indeed impair the effectives of gene drive as a mechanism of population control and should therefore be seen as a potential risk. We further consider the implications for scientists developing gene drives as a population control technology. Lay summaryMost genes exist in multiple versions called alleles, with each having a 50% chance of being passed on by parents during sexual reproduction. However, some alleles, known as gene drives, manipulate inheritance to spread more widely across populations, even if they reduce the fitness of individuals carrying them. Gene drives occur naturally but can also be engineered in the laboratory. Recent technological advancements have led scientists to explore gene drives as a promising tool for controlling pests, invasive species, and disease vectors like malaria-carrying mosquitoes. However, before releasing any gene drives into the wild, it is crucial to assess their feasibility and potential risks. Here, we used computer simulations to explore how artificial gene drives spread when mate choice is allowed to evolve, assuming females can differentiate between males carrying gene drives and those without them. While gene drives have a transmission advantage, they also reduce the survival of carriers. Our results show that evolution can act rapidly after a gene drive is released. Females evolve to discriminate against drive-carrying males, which can sometimes result in the eradication of the gene drive. When gene drives have high survival costs, this evolutionary response can prevent population extinction, potentially undermining the drives purpose. The impact of mate choice is greatest when gene drives spread slowly, giving more time for evolution to act. These findings highlight the importance of considering mate choice dynamics when developing gene drives for population control.