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

Type Article
Date 2019-04
Language English
Author(s) Riquet FlorentineORCID1, 2, Liautard-Haag Cathy1, 2, Woodall Lucy3, 4, Bouza Carmen5, Louisy Patrick6, 7, Hamer Bojan8, Otero-Ferrer Francisco9, Aublanc Philippe10, Beduneau Vickie11, Briard Olivier12, El Ayari Tahani1, 2, Hochscheid Sandra13, Belkhir Khalid1, 2, Arnaud-Haond SophieORCID1, 14, Gagnaire Pierre-Alexandre1, 2, Bierne Nicolas1, 2
Affiliation(s) 1 : Univ Montpellier, Inst Sci Evolut Montpellier, Montpellier, France.
2 : UM, CNRS, UMR5554, IRD,EPHE,Inst Sci Evolut, Sete, France.
3 : Univ Oxford, Dept Zool, Wytham OX2 8QJ, England.
4 : Nat Hist Museum, London SW7 5BD, England.
5 : Univ Santiago de Compostela, Fac Vet Sci, Dept Genet, Lugo, Spain.
6 : Univ Nice Sophia Antipolis, Fac Sci, ECOMERS Lab, Parc Valrose, Nice, France.
7 : Assoc Peau Bleue, 46 Rue Escais, Agde, France.
8 : Rudjer Boskovic Inst, Ctr Marine Res, Giordano Paliaga 5, Rovinj 52210, Croatia.
9 : Univ Las Palmas Gran Canaria, ECOAQUA, Grp Biodiversidad & Conservac, IU, Crta Taliarte S-N, Telde 35214, Spain.
10 : Inst Oceanog Paul Ricard, Ile Des Embiez, Six Fours Les P, France.
11 : Ocearium Crois, Ave St Goustan, Le Croisic, France.
12 : Aquarium Biarritz, Biarritz Ocean, Plateau De Latalaye, Biarritz, France.
13 : Stn Zool Anton Dohrn, Dept Res Infrastruct Marine Biol Resources, Aquarium Unit, Naples, Italy.
14 : UM, IFREMER, CNRS, UMR 9190,IRD,MARine Biodivers Exploitat & Conserv, Sete, France.
Source Evolution (0014-3820) (Wiley), 2019-04 , Vol. 73 , N. 4 , P. 817-835
DOI 10.1111/evo.13696
WOS© Times Cited 20
Keyword(s) Clinal hybrid zone, ecological speciation, local adaptation, mosaic hybrid zone, parallel evolution, reproductive isolation
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 reduce gene flow between groups. Rarely are these two patterns of spatial distribution 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 sympatryi.e., in the same geographical zonewith 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. We find that 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 that mostly follow geography. These parallel outlier SNPs cluster on a single chromosome-wide island of differentiation. Since Atlantic lineages do not map to 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 versus ecological. We discuss how a genomic hotspot of parallel differentiation could have evolved and become associated both with space and with a patchy environment in a single study system.
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Riquet Florentine, Liautard-Haag Cathy, Woodall Lucy, Bouza Carmen, Louisy Patrick, Hamer Bojan, Otero-Ferrer Francisco, Aublanc Philippe, Beduneau Vickie, Briard Olivier, El Ayari Tahani, Hochscheid Sandra, Belkhir Khalid, Arnaud-Haond Sophie, Gagnaire Pierre-Alexandre, Bierne Nicolas (2019). Parallel pattern of differentiation at a genomic island shared between clinal and mosaic hybrid zones in a complex of cryptic seahorse lineages. Evolution, 73(4), 817-835. Publisher's official version : https://doi.org/10.1111/evo.13696 , Open Access version : https://archimer.ifremer.fr/doc/00501/61294/