Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulus guttatus.

Most species are superbly and intricately adapted to the environments in which they live. Adaptive evolution by natural selection is the primary force shaping biological diversity. Differences between closely related species in ecologically selected characters such as habitat preference, reproductiv...

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Main Authors: Kevin M Wright, Deborah Lloyd, David B Lowry, Mark R Macnair, John H Willis
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS Biology
Online Access:http://europepmc.org/articles/PMC3582499?pdf=render
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author Kevin M Wright
Deborah Lloyd
David B Lowry
Mark R Macnair
John H Willis
author_facet Kevin M Wright
Deborah Lloyd
David B Lowry
Mark R Macnair
John H Willis
author_sort Kevin M Wright
collection DOAJ
description Most species are superbly and intricately adapted to the environments in which they live. Adaptive evolution by natural selection is the primary force shaping biological diversity. Differences between closely related species in ecologically selected characters such as habitat preference, reproductive timing, courtship behavior, or pollinator attraction may prevent interbreeding in nature, causing reproductive isolation. But does ecological adaptation cause reproductive incompatibilities such as hybrid sterility or lethality? Although several genes causing hybrid incompatibilities have been identified, there is intense debate over whether the genes that contribute to ecological adaptations also cause hybrid incompatibilities. Thirty years ago, a genetic study of local adaptation to copper mine soils in the wildflower Mimulus guttatus identified a locus that appeared to cause copper tolerance and hybrid lethality in crosses to other populations. But do copper tolerance and hybrid lethality have the same molecular genetic basis? Here we show, using high-resolution genome mapping, that copper tolerance and hybrid lethality are not caused by the same gene but are in fact separately controlled by two tightly linked loci. We further show that selection on the copper tolerance locus indirectly caused the hybrid incompatibility allele to go to high frequency in the copper mine population because of hitchhiking. Our results provide a new twist on Darwin's original supposition that hybrid incompatibilities evolve as an incidental by-product of ordinary adaptation to the environment.
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spelling doaj.art-82ce677c55554010878d91a54f6440582022-12-21T22:58:52ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852013-01-01112e100149710.1371/journal.pbio.1001497Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulus guttatus.Kevin M WrightDeborah LloydDavid B LowryMark R MacnairJohn H WillisMost species are superbly and intricately adapted to the environments in which they live. Adaptive evolution by natural selection is the primary force shaping biological diversity. Differences between closely related species in ecologically selected characters such as habitat preference, reproductive timing, courtship behavior, or pollinator attraction may prevent interbreeding in nature, causing reproductive isolation. But does ecological adaptation cause reproductive incompatibilities such as hybrid sterility or lethality? Although several genes causing hybrid incompatibilities have been identified, there is intense debate over whether the genes that contribute to ecological adaptations also cause hybrid incompatibilities. Thirty years ago, a genetic study of local adaptation to copper mine soils in the wildflower Mimulus guttatus identified a locus that appeared to cause copper tolerance and hybrid lethality in crosses to other populations. But do copper tolerance and hybrid lethality have the same molecular genetic basis? Here we show, using high-resolution genome mapping, that copper tolerance and hybrid lethality are not caused by the same gene but are in fact separately controlled by two tightly linked loci. We further show that selection on the copper tolerance locus indirectly caused the hybrid incompatibility allele to go to high frequency in the copper mine population because of hitchhiking. Our results provide a new twist on Darwin's original supposition that hybrid incompatibilities evolve as an incidental by-product of ordinary adaptation to the environment.http://europepmc.org/articles/PMC3582499?pdf=render
spellingShingle Kevin M Wright
Deborah Lloyd
David B Lowry
Mark R Macnair
John H Willis
Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulus guttatus.
PLoS Biology
title Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulus guttatus.
title_full Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulus guttatus.
title_fullStr Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulus guttatus.
title_full_unstemmed Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulus guttatus.
title_short Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulus guttatus.
title_sort indirect evolution of hybrid lethality due to linkage with selected locus in mimulus guttatus
url http://europepmc.org/articles/PMC3582499?pdf=render
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