Anopheles homing suppression drive candidates exhibit unexpected performance differences in simulations with spatial structure

  1. Samuel E Champer
  2. Isabel K Kim
  3. Andrew G Clark
  4. Philipp W Messer
  5. Jackson Champer  Is a corresponding author
  1. Cornell University, United States
  2. Peking University, China

Abstract

Recent experiments have produced several Anopheles gambiae homing gene drives that disrupt female fertility genes, thereby eventually inducing population collapse. Such drives may be highly effective tools to combat malaria. One such homing drive, based on the zpg promoter driving CRISPR/Cas9, was able to eliminate a cage population of mosquitoes. A second version, purportedly improved upon the first by incorporating an X-shredder element (which biases inheritance towards male offspring), was similarly successful. Here, we analyze experimental data from each of these gene drives to extract their characteristics and performance parameters and compare these to previous interpretations of their experimental performance. We assess each suppression drive within an individual-based simulation framework that models mosquito population dynamics in continuous space. We find that the combined homing/X-shredder drive is actually less effective at population suppression within the context of our mosquito population model. In particular, the combined drive often fails to completely suppress the population, instead resulting in an unstable equilibrium between drive and wild-type alleles. By contrast, otherwise similar drives based on the nos promoter may prove to be more promising candidates for future development than originally thought.

Data availability

All SLiM files for the implementation of these suppression drives are available on GitHub (https://github.com/jchamper/ChamperLab/tree/main/Mosquito-Drive-Modeling).

The following data sets were generated

Article and author information

Author details

  1. Samuel E Champer

    Department of Computational Biology, Cornell University, Ithaca, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4559-7627
  2. Isabel K Kim

    Department of Computational Biology, Cornell University, Ithaca, United States
    Competing interests
    No competing interests declared.
  3. Andrew G Clark

    Department of Computational Biology, Cornell University, Ithaca, United States
    Competing interests
    No competing interests declared.
  4. Philipp W Messer

    Department of Computational Biology, Cornell University, Ithaca, United States
    Competing interests
    Philipp W Messer, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8453-9377
  5. Jackson Champer

    Center for Bioinformatics, Peking University, Beijing, China
    For correspondence
    jchamper@pku.edu.cn
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3814-3774

Funding

NIH (F32AI138476)

  • Jackson Champer

NIH (R01GM127418)

  • Philipp W Messer

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. George H Perry, Pennsylvania State University, United States

Version history

  1. Preprint posted: March 28, 2022 (view preprint)
  2. Received: March 31, 2022
  3. Accepted: October 14, 2022
  4. Accepted Manuscript published: October 14, 2022 (version 1)
  5. Version of Record published: October 25, 2022 (version 2)

Copyright

© 2022, Champer et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 812
    views
  • 142
    downloads
  • 13
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Samuel E Champer
  2. Isabel K Kim
  3. Andrew G Clark
  4. Philipp W Messer
  5. Jackson Champer
(2022)
Anopheles homing suppression drive candidates exhibit unexpected performance differences in simulations with spatial structure
eLife 11:e79121.
https://doi.org/10.7554/eLife.79121

Share this article

https://doi.org/10.7554/eLife.79121

Further reading

    1. Ecology
    2. Evolutionary Biology
    Théo Constant, F Stephen Dobson ... Sylvain Giroud
    Research Article

    Seasonal animal dormancy is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year (the physiological constraint hypothesis). However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the ‘life-history’ hypothesis), but comparative tests across animal species are few. Using the phylogenetic comparative method applied to more than 20 hibernating mammalian species, we found support for both hypotheses as explanations for the phenology of dormancy. In accordance with the life-history hypotheses, sex differences in hibernation emergence and immergence were favored by the sex difference in reproductive effort. In addition, physiological constraint may influence the trade-off between survival and reproduction such that low temperatures and precipitation, as well as smaller body mass, influence sex differences in phenology. We also compiled initial evidence that ectotherm dormancy may be (1) less temperature dependent than previously thought and (2) associated with trade-offs consistent with the life-history hypothesis. Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously thought.

    1. Ecology
    Ari Grele, Tara J Massad ... Lora A Richards
    Research Article

    Declines in biodiversity generated by anthropogenic stressors at both species and population levels can alter emergent processes instrumental to ecosystem function and resilience. As such, understanding the role of biodiversity in ecosystem function and its response to climate perturbation is increasingly important, especially in tropical systems where responses to changes in biodiversity are less predictable and more challenging to assess experimentally. Using large-scale transplant experiments conducted at five neotropical sites, we documented the impacts of changes in intraspecific and interspecific plant richness in the genus Piper on insect herbivory, insect richness, and ecosystem resilience to perturbations in water availability. We found that reductions of both intraspecific and interspecific Piper diversity had measurable and site-specific effects on herbivory, herbivorous insect richness, and plant mortality. The responses of these ecosystem-relevant processes to reduced intraspecific Piper richness were often similar in magnitude to the effects of reduced interspecific richness. Increased water availability reduced herbivory by 4.2% overall, and the response of herbivorous insect richness and herbivory to water availability were altered by both intra- and interspecific richness in a site-dependent manner. Our results underscore the role of intraspecific and interspecific richness as foundations of ecosystem function and the importance of community and location-specific contingencies in controlling function in complex tropical systems.