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The fitness of an introgressing haplotype changes over the course of divergence and depends on its size and genomic location

The genomic era has made clear that introgression, or the movement of genetic material between species, is a common feature of evolution. Examples of both adaptive and deleterious introgression exist in a variety of systems. What is unclear is how the fitness of an introgressing haplotype changes as...

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Autores principales: Dagilis, Andrius J., Matute, Daniel R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10374083/
https://www.ncbi.nlm.nih.gov/pubmed/37459351
http://dx.doi.org/10.1371/journal.pbio.3002185
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author Dagilis, Andrius J.
Matute, Daniel R.
author_facet Dagilis, Andrius J.
Matute, Daniel R.
author_sort Dagilis, Andrius J.
collection PubMed
description The genomic era has made clear that introgression, or the movement of genetic material between species, is a common feature of evolution. Examples of both adaptive and deleterious introgression exist in a variety of systems. What is unclear is how the fitness of an introgressing haplotype changes as species diverge or as the size of the introgressing haplotype changes. In a simple model, we show that introgression may more easily occur into parts of the genome which have not diverged heavily from a common ancestor. The key insight is that alleles from a shared genetic background are likely to have positive epistatic interactions, increasing the fitness of a larger introgressing block. In regions of the genome where few existing substitutions are disrupted, this positive epistasis can be larger than incompatibilities with the recipient genome. Further, we show that early in the process of divergence, introgression of large haplotypes can be favored more than introgression of individual alleles. This model is consistent with observations of a positive relationship between recombination rate and introgression frequency across the genome; however, it generates several novel predictions. First, the model suggests that the relationship between recombination rate and introgression may not exist, or may be negative, in recently diverged species pairs. Furthermore, the model suggests that introgression that replaces existing derived variation will be more deleterious than introgression at sites carrying ancestral variants. These predictions are tested in an example of introgression in Drosophila melanogaster, with some support for both. Finally, the model provides a potential alternative explanation to asymmetry in the direction of introgression, with expectations of higher introgression from rapidly diverged populations into slowly evolving ones.
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spelling pubmed-103740832023-07-28 The fitness of an introgressing haplotype changes over the course of divergence and depends on its size and genomic location Dagilis, Andrius J. Matute, Daniel R. PLoS Biol Research Article The genomic era has made clear that introgression, or the movement of genetic material between species, is a common feature of evolution. Examples of both adaptive and deleterious introgression exist in a variety of systems. What is unclear is how the fitness of an introgressing haplotype changes as species diverge or as the size of the introgressing haplotype changes. In a simple model, we show that introgression may more easily occur into parts of the genome which have not diverged heavily from a common ancestor. The key insight is that alleles from a shared genetic background are likely to have positive epistatic interactions, increasing the fitness of a larger introgressing block. In regions of the genome where few existing substitutions are disrupted, this positive epistasis can be larger than incompatibilities with the recipient genome. Further, we show that early in the process of divergence, introgression of large haplotypes can be favored more than introgression of individual alleles. This model is consistent with observations of a positive relationship between recombination rate and introgression frequency across the genome; however, it generates several novel predictions. First, the model suggests that the relationship between recombination rate and introgression may not exist, or may be negative, in recently diverged species pairs. Furthermore, the model suggests that introgression that replaces existing derived variation will be more deleterious than introgression at sites carrying ancestral variants. These predictions are tested in an example of introgression in Drosophila melanogaster, with some support for both. Finally, the model provides a potential alternative explanation to asymmetry in the direction of introgression, with expectations of higher introgression from rapidly diverged populations into slowly evolving ones. Public Library of Science 2023-07-17 /pmc/articles/PMC10374083/ /pubmed/37459351 http://dx.doi.org/10.1371/journal.pbio.3002185 Text en © 2023 Dagilis, Matute 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, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Dagilis, Andrius J.
Matute, Daniel R.
The fitness of an introgressing haplotype changes over the course of divergence and depends on its size and genomic location
title The fitness of an introgressing haplotype changes over the course of divergence and depends on its size and genomic location
title_full The fitness of an introgressing haplotype changes over the course of divergence and depends on its size and genomic location
title_fullStr The fitness of an introgressing haplotype changes over the course of divergence and depends on its size and genomic location
title_full_unstemmed The fitness of an introgressing haplotype changes over the course of divergence and depends on its size and genomic location
title_short The fitness of an introgressing haplotype changes over the course of divergence and depends on its size and genomic location
title_sort fitness of an introgressing haplotype changes over the course of divergence and depends on its size and genomic location
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10374083/
https://www.ncbi.nlm.nih.gov/pubmed/37459351
http://dx.doi.org/10.1371/journal.pbio.3002185
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