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The sterile insect technique is protected from evolution of mate discrimination

BACKGROUND: The sterile insect technique (SIT) has been used to suppress and even extinguish pest insect populations. The method involves releasing artificially reared insects (usually males) that, when mating with wild individuals, sterilize the broods. If administered on a large enough scale, the...

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Autores principales: Bull, James J., Gomulkiewicz, Richard
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9022645/
https://www.ncbi.nlm.nih.gov/pubmed/35462772
http://dx.doi.org/10.7717/peerj.13301
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author Bull, James J.
Gomulkiewicz, Richard
author_facet Bull, James J.
Gomulkiewicz, Richard
author_sort Bull, James J.
collection PubMed
description BACKGROUND: The sterile insect technique (SIT) has been used to suppress and even extinguish pest insect populations. The method involves releasing artificially reared insects (usually males) that, when mating with wild individuals, sterilize the broods. If administered on a large enough scale, the sterility can collapse the population. Precedents from other forms of population suppression, especially chemicals, raise the possibility of resistance evolving against the SIT. Here, we consider resistance in the form of evolution of female discrimination to avoid mating with sterile males. Is resistance evolution expected? METHODS: We offer mathematical models to consider the dynamics of this process. Most of our models assume a constant-release protocol, in which the same density of males is released every generation, regardless of wild male density. A few models instead assume proportional release, in which sterile releases are adjusted to be a constant proportion of wild males. RESULTS: We generally find that the evolution of female discrimination, although favored by selection, will often be too slow to halt population collapse when a constant-release implementation of the SIT is applied appropriately and continually. The accelerating efficacy of sterile males in dominating matings as the population collapses works equally against discriminating females as against non-discriminating females, and rare genes for discrimination are too slow to ascend to prevent the loss of females that discriminate. Even when migration from source populations sustains the treated population, continued application of the SIT can prevent evolution of discrimination. However, periodic premature cessation of the SIT does allow discrimination to evolve. Likewise, use of a ‘proportional-release’ protocol is also prone to escape from extinction if discriminating genotypes exist in the population, even if those genotypes are initially rare. Overall, the SIT is robust against the evolution of mate discrimination provided care is taken to avoid some basic pitfalls. The models here provide insight for designing programs to avoid those pitfalls.
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spelling pubmed-90226452022-04-22 The sterile insect technique is protected from evolution of mate discrimination Bull, James J. Gomulkiewicz, Richard PeerJ Agricultural Science BACKGROUND: The sterile insect technique (SIT) has been used to suppress and even extinguish pest insect populations. The method involves releasing artificially reared insects (usually males) that, when mating with wild individuals, sterilize the broods. If administered on a large enough scale, the sterility can collapse the population. Precedents from other forms of population suppression, especially chemicals, raise the possibility of resistance evolving against the SIT. Here, we consider resistance in the form of evolution of female discrimination to avoid mating with sterile males. Is resistance evolution expected? METHODS: We offer mathematical models to consider the dynamics of this process. Most of our models assume a constant-release protocol, in which the same density of males is released every generation, regardless of wild male density. A few models instead assume proportional release, in which sterile releases are adjusted to be a constant proportion of wild males. RESULTS: We generally find that the evolution of female discrimination, although favored by selection, will often be too slow to halt population collapse when a constant-release implementation of the SIT is applied appropriately and continually. The accelerating efficacy of sterile males in dominating matings as the population collapses works equally against discriminating females as against non-discriminating females, and rare genes for discrimination are too slow to ascend to prevent the loss of females that discriminate. Even when migration from source populations sustains the treated population, continued application of the SIT can prevent evolution of discrimination. However, periodic premature cessation of the SIT does allow discrimination to evolve. Likewise, use of a ‘proportional-release’ protocol is also prone to escape from extinction if discriminating genotypes exist in the population, even if those genotypes are initially rare. Overall, the SIT is robust against the evolution of mate discrimination provided care is taken to avoid some basic pitfalls. The models here provide insight for designing programs to avoid those pitfalls. PeerJ Inc. 2022-04-18 /pmc/articles/PMC9022645/ /pubmed/35462772 http://dx.doi.org/10.7717/peerj.13301 Text en ©2022 Bull and Gomulkiewicz https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Agricultural Science
Bull, James J.
Gomulkiewicz, Richard
The sterile insect technique is protected from evolution of mate discrimination
title The sterile insect technique is protected from evolution of mate discrimination
title_full The sterile insect technique is protected from evolution of mate discrimination
title_fullStr The sterile insect technique is protected from evolution of mate discrimination
title_full_unstemmed The sterile insect technique is protected from evolution of mate discrimination
title_short The sterile insect technique is protected from evolution of mate discrimination
title_sort sterile insect technique is protected from evolution of mate discrimination
topic Agricultural Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9022645/
https://www.ncbi.nlm.nih.gov/pubmed/35462772
http://dx.doi.org/10.7717/peerj.13301
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