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Natural hybridization reveals incompatible alleles that cause melanoma in swordtail fish

Daniel L. Powell, Mateo Garcia, Mackenzie Keegan, Patrick Reilly, Kang Du, Alejandra P. Díaz-Loyo, Shreya Banerjee, Danielle Blakkan, David Reich, View ORCID ProfilePeter Andolfatto, Gil Rosenthal, Manfred Schartl, Molly Schumer
doi: https://doi.org/10.1101/2019.12.12.874586
Daniel L. Powell
1Department of Biology, Stanford University
2Centro de Investigaciones Científicas de las Huastecas “Aguazarca”, A.C.
3Department of Biology, Texas A&M University
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  • For correspondence: dpowell8@stanford.edu schumer@stanford.edu
Mateo Garcia
2Centro de Investigaciones Científicas de las Huastecas “Aguazarca”, A.C.
3Department of Biology, Texas A&M University
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Mackenzie Keegan
4Department of Biology, Northeastern University
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Patrick Reilly
5Lewis Sigler Institute for Integrative Genomics, Princeton University
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Kang Du
6Developmental Biochemistry, Biocenter, University of Würzburg
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Alejandra P. Díaz-Loyo
7Laboratorio de Ecología de la Conducta, Instituto de Fisiología, Benemérita Universidad Autónoma de Puebla
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Shreya Banerjee
1Department of Biology, Stanford University
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Danielle Blakkan
1Department of Biology, Stanford University
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David Reich
8Department of Genetics, Harvard Medical School, Howard Hughes Medical Institute, and the Broad Institute of Harvard and MIT
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Peter Andolfatto
9Department of Biology, Columbia University
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  • ORCID record for Peter Andolfatto
Gil Rosenthal
2Centro de Investigaciones Científicas de las Huastecas “Aguazarca”, A.C.
3Department of Biology, Texas A&M University
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Manfred Schartl
2Centro de Investigaciones Científicas de las Huastecas “Aguazarca”, A.C.
3Department of Biology, Texas A&M University
6Developmental Biochemistry, Biocenter, University of Würzburg
10Hagler Institute for Advanced Study, Texas A&M University
11
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Molly Schumer
1Department of Biology, Stanford University
2Centro de Investigaciones Científicas de las Huastecas “Aguazarca”, A.C.
12Hanna H. Gray Fellow, Howard Hughes Medical Institute
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  • For correspondence: dpowell8@stanford.edu schumer@stanford.edu
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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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Posted December 13, 2019.
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Natural hybridization reveals incompatible alleles that cause melanoma in swordtail fish
Daniel L. Powell, Mateo Garcia, Mackenzie Keegan, Patrick Reilly, Kang Du, Alejandra P. Díaz-Loyo, Shreya Banerjee, Danielle Blakkan, David Reich, Peter Andolfatto, Gil Rosenthal, Manfred Schartl, Molly Schumer
bioRxiv 2019.12.12.874586; doi: https://doi.org/10.1101/2019.12.12.874586
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Natural hybridization reveals incompatible alleles that cause melanoma in swordtail fish
Daniel L. Powell, Mateo Garcia, Mackenzie Keegan, Patrick Reilly, Kang Du, Alejandra P. Díaz-Loyo, Shreya Banerjee, Danielle Blakkan, David Reich, Peter Andolfatto, Gil Rosenthal, Manfred Schartl, Molly Schumer
bioRxiv 2019.12.12.874586; doi: https://doi.org/10.1101/2019.12.12.874586

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