Inferring the demographic history underlying parallel genomic divergence among pairs of parasitic and nonparasitic lamprey ecotypes.
Understanding the evolutionary mechanisms generating parallel genomic divergence patterns among replicate ecotype pairs remains an important challenge in speciation research. We investigated the genomic divergence between the anadromous parasitic river lamprey (Lampetra fluviatilis) and the freshwater-resident nonparasitic brook lamprey (Lampetra planeri) in nine population pairs displaying variable levels of geographic connectivity. We genotyped 338 individuals with RAD sequencing and inferred the demographic divergence history of each population pair using a diffusion approximation method. Divergence patterns in geographically connected population pairs were better explained by introgression after secondary contact, whereas disconnected population pairs have retained a signal of ancient migration. In all ecotype pairs, models accounting for differential introgression among loci outperformed homogeneous migration models. Generating neutral predictions from the inferred divergence scenarios to detect highly differentiated markers identified greater proportions of outliers in disconnected population pairs than in connected pairs. However, increased similarity in the most divergent genomic regions was found among connected ecotype pairs, indicating that gene flow was instrumental in generating parallelism at the molecular level. These results suggest that heterogeneous genomic differentiation and parallelism among replicate ecotype pairs have partly emerged through restricted introgression in genomic islands.
INRA, UMR 985 Ecologie et Santé des Ecosystèmes, 35042, Rennes, France.|Agrocampus Ouest, UMR ESE, 65 rue de Saint-Brieuc, 35042, Rennes, France.
Quentin
Q
Rougemont
Institut des Sciences de l'Evolution (UMR 5554), CNRS-UM2-IRD, Place Eugène Bataillon, F-34095, Montpellier, France.|Station Méditerranéenne de l'Environnement Littoral, Université de Montpellier, 2 Rue des Chantiers, F-34200, Sète, France.
Pierre-Alexandre
PA
Gagnaire
CEFE-CNRS, Centre D'Ecologie Fonctionnelle et Evolutive, Route de Mende, 34090, Montpellier, France.
Charles
C
Perrier
Plateforme génomique INRA GenoToul Chemin de Borderouge - Auzeville, 31320, Castanet-Tolosan, France.
Clémence
C
Genthon
INRA, UMR 985 Ecologie et Santé des Ecosystèmes, 35042, Rennes, France.|Agrocampus Ouest, UMR ESE, 65 rue de Saint-Brieuc, 35042, Rennes, France.
Anne-Laure
AL
Besnard
INRA, UMR 985 Ecologie et Santé des Ecosystèmes, 35042, Rennes, France.|Agrocampus Ouest, UMR ESE, 65 rue de Saint-Brieuc, 35042, Rennes, France.
Sophie
S
Launey
INRA, UMR 985 Ecologie et Santé des Ecosystèmes, 35042, Rennes, France.|Agrocampus Ouest, UMR ESE, 65 rue de Saint-Brieuc, 35042, Rennes, France.
Guillaume
G
Evanno
D000818:Animals; D060146:Ecotype; D051456:Gene Flow; D005828:Genetics, Population; D016678:Genome; D007798:Lampreys / Q000145:classification*; D008957:Models, Genetic
Lampetra sp.; allele surfing; demographic history; ecotypic divergence; genetic parallelism; heterogeneous differentiation; secondary contact