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

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 sympatry—i.e., in the same geographical zone—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. 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.

Beyond parallel evolution: when several species colonize the same environmental gradient

“…However, we found no significant inter-specific correlation for sliding-widows average FST between North Sea and Baltic Sea lineages (Table S6), except between the flounder PEL and DEM lineages, which may reflect contemporary gene flow between the populations (Riquet et al, 2019;Welch and Jiggins, 2014). Moreover, the 5% most differentiated regions (both with FST and dXY) were strongly and negatively correlated in all the species comparisons (Table S6).…”

The role of hybridization during ecological divergence of southwestern white pine (Pinus strobiformis) and limber pine (P. flexilis)

“…The geographic cline in h , asymmetry in excess ancestry loci towards P. flexilis and elevated estimates of F ST–periphery , however, indicate the potential for geographically driven neutral introgression to generate biased signals of local adaptation within the peripheral populations (Geraldes et al., ). Ongoing investigations using replicate populations in the hybrid zone across gradients of geographic proximity and climate similarity will be able to address this issue in further detail (Lotterhos & Whitlock, ; Riquet et al., ).…”

The role of hybridization during ecological divergence of southwestern white pine (Pinus strobiformis) and limber pine (P. flexilis)

“…The geographic cline in h , asymmetry in excess ancestry loci towards P. flexilis , and elevated estimates of F ST –periphery , however, indicate the potential for geographically driven neutral introgression to generate biased signals of local adaptation within the peripheral populations (Geraldes et al 2014). Ongoing investigations using replicate populations in the hybrid zone across gradients of geographic proximity and climate similarity will be able to address this issue in further detail (Lotterhos & Whitlock 2015; Riquet et al 2017).…”