Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulus guttatus
Open accessAbstract
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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The locus controlling hybrid necrosis (Nec1) is tightly linked to the copper tolerance locus (Tol1), and markers linked to both exhibit high FST relative to unlinked markers.
“The locus controlling hybrid necrosis (Nec1) is tightly linked to the copper tolerance locus (Tol1), and markers linked to both exhibit high FST relative to unlinked markers (Figure 5; Wright et al., 2013).”
From Genomics of plant speciation (2023) · cites this paper as Wright et al., 2013
In Mimulus guttatus, a hybrid necrosis allele has been swept to high frequency because of genetic hitchhiking with a copper tolerance allele favored by local selection to copper mine tailings.
“In Mimulus guttatus, a hybrid necrosis allele has been swept to high frequency because of genetic hitchhiking with a copper tolerance allele favored by local selection to copper mine tailings (Figure 5; Wright et al., 2013).”
From Genomics of plant speciation (2023) · cites this paper as Wright et al., 2013
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- Authors
- Wright, K. M., Lloyd, D., Lowry, D. B., Macnair, M. R., & Willis, J. H.
- Affiliations
- Harvard University (US)
- University of Exeter (GB)
- The University of Texas at Austin (US)
- Duke University (US)
- Corresponding author
- Wright, Kevin M.
- Venue
- PLoS Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-02-26
- Volume
- 11
- Issue
- 2
- Pages
- e1001497
- ISSN
- 1544-9173 (ISSN-L)
- 1545-7885
- PMC
- PMC3582499
- OpenAlex
- W2065541891
- Cited by
- 121
- References
- 55
- Citations by year
- 2026: 1 · 2025: 7 · 2024: 6 · 2023: 5 · 2022: 8 · 2021: 3 · 2020: 8 · 2019: 11 · 2018: 13 · 2017: 10 · 2016: 14 · 2015: 9 · 2014: 15 · 2013: 11
- FWCI
- 10.84
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Biology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Texas ScholarWorks (Texas Digital Library) (submittedVersion, cc-by)
- Funders
- National Science Foundation (0710318, 0723814, 0328636)
- Joint Genome Institute
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Mapping and Diversity in Plants and Animals
- Keywords
- hybrid lethality, hybrid incompatibility, Mimulus guttatus, copper tolerance, local adaptation, hitchhiking, linkage, genome mapping, reproductive isolation, ecological adaptation, natural selection
- MeSH terms
- Adaptation, Physiological, Alleles, Chimera, Chromosome Mapping, Biological Evolution, Genetic Linkage, Mimulus, Quantitative Trait Loci
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