TY - JOUR
T1 - Massive genome inversion drives coexistence of divergent morphs in common quails
AU - Sanchez-Donoso, Ines
AU - Ravagni, Sara
AU - Rodríguez-Teijeiro, J. Domingo
AU - Christmas, Matthew J.
AU - Huang, Yan
AU - Maldonado-Linares, Andros
AU - Puigcerver, Manel
AU - Jiménez-Blasco, Irene
AU - Andrade, Pedro
AU - Gonçalves, David
AU - Friis, Guillermo
AU - Roig, Ignasi
AU - Webster, Matthew T.
AU - Leonard, Jennifer A.
AU - Vilà, Carles
N1 - Funding Information:
The authors thank all the people who helped with the fieldwork and especially Francesc Sardà-Palomera, Jorge Falagán, and Fernando Gavilán (Spain); Mohamed Maghnouj (Morocco); Jan Staal (the Netherlands); and Pierfrancesco Micheloni (Italy). Joan Navarro and Francisco Ramírez provided support for isotopic analyses. Irene Quintanilla, Anna Cornellas, Sarai López, and the Laboratories of Molecular Ecology (LEM-EBD) and Stable Isotopes (LIE-EBD) at the Doñana Biological Station (EBD-CSIC) helped with the laboratory work. Genome sequencing was performed by the SNP&SEQ Technology Platform in Uppsala. The facility is part of the National Genomics Infrastructure (NGI) Sweden and Science for Life Laboratory. The SNP&SEQ Platform is also supported by the Swedish Research Council and the Knut and Alice Wallenberg Foundation . Informatic facilities were provided by Doñana ICTS-RBD. Micro-project (C.V.) was funded by Severo Ochoa award from the Spanish Government to EBD-CSIC; Spanish Government grants PID2019-108163GB-100 (C.V. and J.D.R.-T.), BFU2016-80370-P , and PID2019-107082RB-I00 (I.R.); Spanish Government fellowship BES-2017- 081291 (S.R.); China Scholarship Council fellowship (Y.H.); and Fundação para a Ciência e Tecnología Research Fellowship PD/BD/114028/2015 (P.A.). Federación de Caza de Euskadi provided financial support for part of the field sampling.
Funding Information:
The authors thank all the people who helped with the fieldwork and especially Francesc Sard?-Palomera, Jorge Falag?n, and Fernando Gavil?n (Spain); Mohamed Maghnouj (Morocco); Jan Staal (the Netherlands); and Pierfrancesco Micheloni (Italy). Joan Navarro and Francisco Ram?rez provided support for isotopic analyses. Irene Quintanilla, Anna Cornellas, Sarai L?pez, and the Laboratories of Molecular Ecology (LEM-EBD) and Stable Isotopes (LIE-EBD) at the Do?ana Biological Station (EBD-CSIC) helped with the laboratory work. Genome sequencing was performed by the SNP&SEQ Technology Platform in Uppsala. The facility is part of the National Genomics Infrastructure (NGI) Sweden and Science for Life Laboratory. The SNP&SEQ Platform is also supported by the Swedish Research Council and the Knut and Alice Wallenberg Foundation. Informatic facilities were provided by Do?ana ICTS-RBD. Micro-project (C.V.) was funded by Severo Ochoa award from the Spanish Government to EBD-CSIC; Spanish Government grants PID2019-108163GB-100 (C.V. and J.D.R.-T.), BFU2016-80370-P, and PID2019-107082RB-I00 (I.R.); Spanish Government fellowship BES-2017- 081291 (S.R.); China Scholarship Council fellowship (Y.H.); and Funda??o para a Ci?ncia e Tecnolog?a Research Fellowship PD/BD/114028/2015 (P.A.). Federaci?n de Caza de Euskadi provided financial support for part of the field sampling. C.V. and I.S.-D. conceived the research. J.D.R.-T. M.P. I.J.-B. I.S.-D. C.V. P.A. and D.G. led the fieldwork, including sampling and phenotypic data collection. I.S.-D. and J.A.L. led stable isotope and molecular genetic lab work. I.R. Y.H. A.M.-L. and S.R. carried out immunofluorescence assays. S.R. I.S.-D. M.J.C. M.T.W. G.F. J.A.L. and C.V. carried out molecular genetic data analyses. I.S.-D. I.J.-B. and J.D.R.-T. carried out phenotype analyses. C.V. I.S.-D. and S.R. wrote the first version of the manuscript. All authors discussed and commented on the manuscript. The authors declare no competing interests.
Publisher Copyright:
© 2021 Elsevier Inc.
PY - 2022/1/24
Y1 - 2022/1/24
N2 - The presence of population-specific phenotypes often reflects local adaptation or barriers to gene flow. The co-occurrence of phenotypic polymorphisms that are restricted within the range of a highly mobile species is more difficult to explain. An example of such polymorphisms is in the common quail Coturnix coturnix, a small migratory bird that moves widely during the breeding season in search of new mating opportunities, following ephemeral habitats,1,2 and whose females may lay successive clutches at different locations while migrating.3 In spite of this vagility, previous studies reported a higher frequency of heavier males with darker throat coloration in the southwest of the distribution (I. Jiménez-Blasco et al., 2015, Int. Union Game Biol., conference). We used population genomics and cytogenetics to explore the basis of this polymorphism and discovered a large inversion in the genome of the common quail. This inversion extends 115 Mbp in length and encompasses more than 7,000 genes (about 12% of the genome), producing two very different forms. Birds with the inversion are larger, have darker throat coloration and rounder wings, are inferred to have poorer flight efficiency, and are geographically restricted despite the high mobility of the species. Stable isotope analyses confirmed that birds carrying the inversion have shorter migratory distances or do not migrate. However, we found no evidence of pre- or post-zygotic isolation, indicating the two forms commonly interbreed and that the polymorphism remains locally restricted because of the effect on behavior. This illustrates a genomic mechanism underlying maintenance of geographically structured polymorphisms despite interbreeding with a lineage with high mobility.
AB - The presence of population-specific phenotypes often reflects local adaptation or barriers to gene flow. The co-occurrence of phenotypic polymorphisms that are restricted within the range of a highly mobile species is more difficult to explain. An example of such polymorphisms is in the common quail Coturnix coturnix, a small migratory bird that moves widely during the breeding season in search of new mating opportunities, following ephemeral habitats,1,2 and whose females may lay successive clutches at different locations while migrating.3 In spite of this vagility, previous studies reported a higher frequency of heavier males with darker throat coloration in the southwest of the distribution (I. Jiménez-Blasco et al., 2015, Int. Union Game Biol., conference). We used population genomics and cytogenetics to explore the basis of this polymorphism and discovered a large inversion in the genome of the common quail. This inversion extends 115 Mbp in length and encompasses more than 7,000 genes (about 12% of the genome), producing two very different forms. Birds with the inversion are larger, have darker throat coloration and rounder wings, are inferred to have poorer flight efficiency, and are geographically restricted despite the high mobility of the species. Stable isotope analyses confirmed that birds carrying the inversion have shorter migratory distances or do not migrate. However, we found no evidence of pre- or post-zygotic isolation, indicating the two forms commonly interbreed and that the polymorphism remains locally restricted because of the effect on behavior. This illustrates a genomic mechanism underlying maintenance of geographically structured polymorphisms despite interbreeding with a lineage with high mobility.
KW - Coturnix coturnix
KW - chromosomal inversion
KW - interbreeding
KW - migration
KW - polymorphism
KW - stable isotopes
KW - structural variation
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U2 - 10.1016/j.cub.2021.11.019
DO - 10.1016/j.cub.2021.11.019
M3 - Article
C2 - 34847353
AN - SCOPUS:85122932440
VL - 32
SP - 462-469.e6
JO - Current Biology
JF - Current Biology
SN - 0960-9822
IS - 2
ER -