Natural hybridization reveals incompatible alleles that cause melanoma in swordtail fish
Open accessPublished version of a preprint
Abstract
Abstract The establishment of reproductive barriers between populations is the key process that fuels the evolution of new species. A genetic framework for this process was proposed over 80 years ago, which posits “incompatible” interactions between genes that result in reduced survival or reproduction in hybrids. Despite this foundational work, progress has been slow in identifying individual genes that underlie hybrid incompatibilities, with only a handful known to date. Here, we use a combination of approaches to precisely map the genes that drive the development of a melanoma incompatibility in swordtail fish hybrids. We find that one of the genes involved in this incompatibility also causes melanoma in hybrids between distantly related species. Moreover, we show that this melanoma reduces survival in the wild, likely due to progressive degradation of the fin. Together, this work represents only the second case where the genes underlying a vertebrate hybrid incompatibility have been identified and provides the first glimpse into the action of these genes in natural hybrid populations. One sentence summary Using a combination of mapping approaches, we identify interacting genes that lead to melanoma in hybrids and characterize their effects in natural hybrid populations.
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Genome-wide association studies hold great promise for identifying hybrid incompatibility loci, especially in natural hybrids.
“Although still limited to cases where incompatibility has a clear phenotype, genome-wide association studies hold great promise for identifying hybrid incompatibility loci, especially in natural hybrids (Powell et al., 2020).”
From Genomics of plant speciation (2023) · cites this paper as Powell et al., 2020
In “Loci associated with the spotting phenotype in X. birchmanni,” the paper reports a GWAS of spotting in the parental species. In “Genetic architecture of the melanoma incompatibility,” it reports mapping melanoma loci in natural hybrids, but uses admixture mapping rather than GWAS. The study supports the promise of genome-wide mapping for a visibly expressed hybrid incompatibility, but does not establish the stated limitation to clear phenotypes or demonstrate GWAS of incompatibility loci in natural hybrids. (LLM, conf=0.84)
Experimental — accuracy not yet measuredMany known examples of incompatible genes involve strongly diverged species, presenting a risk that they arose after the speciation process was complete.
“many of the known examples of incompatible genes involve strongly diverged species (Powell et al. 2020), presenting a risk that they arose after the speciation process was complete.”
From Finding Hybrid Incompatibilities Using Genome Sequences from Hybrid Populations (2021) · cites this paper as Powell et al. 2020
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References 107 · Cited by 124
Research works printed but not linked: 3
- [20]Schumer M, eLife 3, e02535 (2014).
- [26]Schartl A, Malitschek B, Kazianis S, Borowsky R, Schartl M, Cancer Res. 55, 159– 165 (1995). 7805027
- [47]Powell D, Natural hybridization reveals incompatible alleles that cause melanoma in swordtail fish. Dryad (2020). PMC8074799 32409469
- Authors
- Powell, D. L., García-Olazábal, M., Keegan, M., Reilly, P., Du, K., Díaz-Loyo, A. P., Banerjee, S., Blakkan, D., Reich, D., Andolfatto, P., Rosenthal, G. G., Schartl, M., & Schumer, M.
- Affiliations
- Howard Hughes Medical Institute (US)
- Centro de Investigaciones Cientifícas de las Huastecas 'Aguazarca' (MX)
- Northeastern University (US)
- Princeton University (US)
- University of Würzburg (DE)
- Benemérita Universidad Autónoma de Puebla (MX)
- Broad Institute (US)
- Columbia University (US)
- Texas State University (US)
- Corresponding author
- Powell, Daniel L.
- Schumer, Molly
- ORCID
- Venue
- Science
- Published
- 2020-05-15
- Volume
- 368
- Issue
- 6492
- Pages
- 731-736
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC8074799
- OpenAlex
- W3024064700
- Cited by
- 124
- References
- 107
- Citations by year
- 2026: 17 · 2025: 14 · 2024: 27 · 2023: 12 · 2022: 16 · 2021: 27 · 2020: 11
- FWCI
- 10.66
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- cc-by-nc-nd
- Locations
- Science (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Padua Research Archive (University of Padova) (submittedVersion, cc-by)
- Funders
- National Science Foundation (1354172)
- National Institutes of Health (1R35GM133774)
- Howard Hughes Medical Institute (Hanna H Gray Fellowship)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- hybrid incompatibility, melanoma, swordtail fish, natural hybridization, introgression, admixture mapping, genome-wide association study, genetic interactions, convergent evolution, Xiphophorus
- MeSH terms
- Alleles, Animals, Chimera, Cyprinodontiformes, Fish Diseases, Hybridization, Genetic, Melanoma, Receptor Protein-Tyrosine Kinases, Fish Proteins, Genome-Wide Association Study, Genetic Loci, Animal Fins
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