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Parallel pattern of differentiation at a genomic island shared between clinal and mosaic hybrid zones in a complex of cryptic seahorse lineages

View ORCID ProfileFlorentine Riquet, Cathy Liautard-Haag, Lucy Woodall, Carmen Bouza, Patrick Louisy, Bojan Hamer, Francisco Otero-Ferrer, Philippe Aublanc, Vickie Béduneau, Olivier Briard, Tahani El Ayari, Sandra Hochscheid, Khalid Belkhir, Sophie Arnaud-Haond, Pierre-Alexandre Gagnaire, Nicolas Bierne
doi: https://doi.org/10.1101/161786
Florentine Riquet
Institut des Sciences de l’Evolution de Montpellier, Université Montpellier, Montpellier, FranceCNRS Institut des Sciences de l’Evolution, UMR5554 UM-CNRS-IRD-EPHE, Station Marine OREME, Sète, France
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  • ORCID record for Florentine Riquet
Cathy Liautard-Haag
Institut des Sciences de l’Evolution de Montpellier, Université Montpellier, Montpellier, FranceCNRS Institut des Sciences de l’Evolution, UMR5554 UM-CNRS-IRD-EPHE, Station Marine OREME, Sète, France
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Lucy Woodall
Department of Zoology, University of Oxford, John Krebs Field Station, Wytham, OX2 8QJ, UKNatural History Museum, Cromwell Road, London SW7 5BD, UK
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Carmen Bouza
Department of Genetics, Faculty of Veterinary Science, Universidade de Santiago de Compostela, Campus de Lugo, Lugo, Spain
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Patrick Louisy
University of Nice Sophia Antipolis, ECOMERS Laboratory, Faculty of Sciences, Parc Valrose, Nice, FranceAssociation Peau-Bleue, 46 rue des Escais, Agde, France
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Bojan Hamer
Center for Marine Research, Ruder Boskovic Institute, Giordano Paliaga 5, 52210 Rovinj, Croatia
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Francisco Otero-Ferrer
Grupo en Biodiversidad y Conservación, IU-ECOAQUA, Universidad de Las Palmas de Gran Canaria, Crta. Taliarte s/n, 35214 Telde, Spain
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Philippe Aublanc
Institut océanographique Paul Ricard, Ile des Embiez, Six-Fours-les-Plages, France
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Vickie Béduneau
Océarium du Croisic, Avenue de Saint Goustan, Le Croisic, France
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Olivier Briard
Aquarium de Biarritz, Biarritz Océan, Plateau de l’Atalaye, Biarritz, France
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Tahani El Ayari
Institut des Sciences de l’Evolution de Montpellier, Université Montpellier, Montpellier, FranceCNRS Institut des Sciences de l’Evolution, UMR5554 UM-CNRS-IRD-EPHE, Station Marine OREME, Sète, France
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Sandra Hochscheid
Stazione Zoologica Anton Dohrn, Department Research Infrastructures for Marine Biological Resources, Aquarium Unit, Napoli, Italy
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Khalid Belkhir
Institut des Sciences de l’Evolution de Montpellier, Université Montpellier, Montpellier, FranceCNRS Institut des Sciences de l’Evolution, UMR5554 UM-CNRS-IRD-EPHE, Station Marine OREME, Sète, France
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Sophie Arnaud-Haond
Institut des Sciences de l’Evolution de Montpellier, Université Montpellier, Montpellier, FranceIfremer - MARine Biodiversity, Exploitation and Conservation, UMR 9190 IRD-IFREMER-UM-CNRS, Sète, France
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Pierre-Alexandre Gagnaire
Institut des Sciences de l’Evolution de Montpellier, Université Montpellier, Montpellier, FranceCNRS Institut des Sciences de l’Evolution, UMR5554 UM-CNRS-IRD-EPHE, Station Marine OREME, Sète, France
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Nicolas Bierne
Institut des Sciences de l’Evolution de Montpellier, Université Montpellier, Montpellier, FranceCNRS Institut des Sciences de l’Evolution, UMR5554 UM-CNRS-IRD-EPHE, Station Marine OREME, Sète, France
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Abstract

Diverging semi-isolated lineages either meet in narrow clinal hybrid zones, or have a mosaic distribution associated with environmental variation. Intrinsic reproductive isolation is often emphasized in the former and local adaptation in the latter, although both can contribute to isolation. Rarely these two patterns of spatial distribution are reported in the same study system. Here we report that the long-snouted seahorse Hippocampus guttulatus is subdivided into discrete panmictic entities by both types of hybrid zones. Along the European Atlantic coasts, a northern and a southern lineage meet in the southwest of France where they coexist in sympatry with little hybridization. In the Mediterranean Sea, two lineages have a mosaic distribution, associated with lagoon-like and marine habitats. A fifth lineage was identified in the Black Sea. Genetic homogeneity over large spatial scales contrasts with isolation maintained in sympatry or close parapatry at a fine scale. A high variation in locus-specific introgression rates provides additional evidence that partial reproductive isolation must be maintaining the divergence. Surprisingly, fixed differences between lagoon and marine populations in the Mediterranean Sea belong to the most differentiated SNPs between the two Atlantic lineages, against the genome-wide pattern of structure. These parallel outlier SNPs cluster on a single chromosome-wide island of differentiation. Since Atlantic lineages do not match the lagoon-sea habitat variation, genetic parallelism at the genomic island suggests a shared genetic barrier contributes to reproductive isolation in contrasting contexts -i.e. spatial vs. ecological. We discuss how a genomic hotspot of parallel differentiation could have evolved and become associated either with space or with a patchy environment in a single study system.

Footnotes

  • This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (https://dx.doi.org/10.24072/pci.evolbiol.100056).

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Parallel pattern of differentiation at a genomic island shared between clinal and mosaic hybrid zones in a complex of cryptic seahorse lineages
Florentine Riquet, Cathy Liautard-Haag, Lucy Woodall, Carmen Bouza, Patrick Louisy, Bojan Hamer, Francisco Otero-Ferrer, Philippe Aublanc, Vickie Béduneau, Olivier Briard, Tahani El Ayari, Sandra Hochscheid, Khalid Belkhir, Sophie Arnaud-Haond, Pierre-Alexandre Gagnaire, Nicolas Bierne
bioRxiv 161786; doi: https://doi.org/10.1101/161786
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Parallel pattern of differentiation at a genomic island shared between clinal and mosaic hybrid zones in a complex of cryptic seahorse lineages
Florentine Riquet, Cathy Liautard-Haag, Lucy Woodall, Carmen Bouza, Patrick Louisy, Bojan Hamer, Francisco Otero-Ferrer, Philippe Aublanc, Vickie Béduneau, Olivier Briard, Tahani El Ayari, Sandra Hochscheid, Khalid Belkhir, Sophie Arnaud-Haond, Pierre-Alexandre Gagnaire, Nicolas Bierne
bioRxiv 161786; doi: https://doi.org/10.1101/161786

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