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Genomic islands of differentiation in two songbird species reveal candidate genes for hybrid female sterility

L. Mořkovský, V. Janoušek, J. Reif, J. Rídl, J. Pačes, L. Choleva, K. Janko, MW. Nachman, R. Reifová,

. 2018 ; 27 (4) : 949-958. [pub] 20180226

Language English Country England, Great Britain

Document type Journal Article, Research Support, N.I.H., Extramural, Research Support, Non-U.S. Gov't

Persistent link   https://www.medvik.cz/link/bmc19012928

Hybrid sterility is a common first step in the evolution of postzygotic reproductive isolation. According to Haldane's Rule, it affects predominantly the heterogametic sex. While the genetic basis of hybrid male sterility in organisms with heterogametic males has been studied for decades, the genetic basis of hybrid female sterility in organisms with heterogametic females has received much less attention. We investigated the genetic basis of reproductive isolation in two closely related avian species, the common nightingale (Luscinia megarhynchos) and the thrush nightingale (L. luscinia), that hybridize in a secondary contact zone and produce viable hybrid progeny. In accordance with Haldane's Rule, hybrid females are sterile, while hybrid males are fertile, allowing gene flow to occur between the species. Using transcriptomic data from multiple individuals of both nightingale species, we identified genomic islands of high differentiation (FST ) and of high divergence (Dxy ), and we analysed gene content and patterns of molecular evolution within these islands. Interestingly, we found that these islands were enriched for genes related to female meiosis and metabolism. The islands of high differentiation and divergence were also characterized by higher levels of linkage disequilibrium than the rest of the genome in both species indicating that they might be situated in genomic regions of low recombination. This study provides one of the first insights into genetic basis of hybrid female sterility in organisms with heterogametic females.

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$a Hybrid sterility is a common first step in the evolution of postzygotic reproductive isolation. According to Haldane's Rule, it affects predominantly the heterogametic sex. While the genetic basis of hybrid male sterility in organisms with heterogametic males has been studied for decades, the genetic basis of hybrid female sterility in organisms with heterogametic females has received much less attention. We investigated the genetic basis of reproductive isolation in two closely related avian species, the common nightingale (Luscinia megarhynchos) and the thrush nightingale (L. luscinia), that hybridize in a secondary contact zone and produce viable hybrid progeny. In accordance with Haldane's Rule, hybrid females are sterile, while hybrid males are fertile, allowing gene flow to occur between the species. Using transcriptomic data from multiple individuals of both nightingale species, we identified genomic islands of high differentiation (FST ) and of high divergence (Dxy ), and we analysed gene content and patterns of molecular evolution within these islands. Interestingly, we found that these islands were enriched for genes related to female meiosis and metabolism. The islands of high differentiation and divergence were also characterized by higher levels of linkage disequilibrium than the rest of the genome in both species indicating that they might be situated in genomic regions of low recombination. This study provides one of the first insights into genetic basis of hybrid female sterility in organisms with heterogametic females.
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$a Janoušek, Václav $u Department of Zoology, Faculty of Science, Charles University, Prague 2, Czech Republic.
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$a Reif, Jiří $u Institute for Environmental Studies, Faculty of Science, Charles University, Prague 2, Czech Republic.
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$a Rídl, Jakub $u Laboratory of Genomics and Bioinformatics, Institute of Molecular Genetics, The Czech Academy of Sciences, Prague 4, Czech Republic.
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$a Pačes, Jan $u Laboratory of Genomics and Bioinformatics, Institute of Molecular Genetics, The Czech Academy of Sciences, Prague 4, Czech Republic.
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$a Choleva, Lukáš $u Laboratory of Fish Genetics, Institute of Animal Physiology and Genetics, The Czech Academy of Sciences, Liběchov, Czech Republic. Department of Biology and Ecology, Faculty of Science, University of Ostrava, Ostrava, Czech Republic.
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$a Janko, Karel $u Laboratory of Fish Genetics, Institute of Animal Physiology and Genetics, The Czech Academy of Sciences, Liběchov, Czech Republic.
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$a Nachman, Michael W $u Museum of Comparative Zoology and Integrative Biology, University of California, Berkeley, CA, USA.
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