Coupling of 12 chromosomal inversions maintains a strong barrier to gene flow between ecotypes

Abstract

Chromosomal rearrangements lead to the coupling of reproductive barriers, but whether and how they contribute to completion of speciation remains unclear. Marine snails of the genusLittorinarepeatedly form hybrid zones between taxa segregating for inversion arrangements, providing opportunities to study this question. Here, we analysed two adjacent transects across hybrid zones between large and dwarf ecotypes ofLittorina fabaliscovering wave exposure gradients in a Swedish island. Applying whole-genome sequences we found 12 putative inversions reaching near differential fixation between the opposite ends of each transect, and being in strong linkage disequilibrium. These inversions cover 20% of the genome and carry 93% of divergent SNPs. Bimodal hybrid zones in both transects indicate that the two ecotypes ofLittorina fabalismaintain their genetic and phenotypic integrity following contact due to strong coupling between inversion clines that strengthened the reproductive barrier. The bimodality resulting from the linked inversions extends into collinear parts of the genome, suggesting a genome-wide coupling. Demographic inference suggests that the coupling built up during a period of allopatry, and has been maintained for more than 1K generations after secondary contact. Overall, this study shows that the coupling of multiple chromosomal inversions contributes to strong reproductive isolation. Importantly, two of the inversions overlap with inverted genomic regions associated with ecotype differences in a closely-related species (L. saxatilis), suggesting the same regions, with similar structural variants, repeatedly contribute to ecotype evolution in distinct species.

The genomic landscape of adaptation to a new host plant

“…In spite of mounting support for inversions having a role in speciation (Jones et al, 2012;Küpper et al, 2016;Tuttle et al, 2016;Hooper and Price, 2017;Wellenreuther and Bernatchez, 2018;Faria, Chaube, et al, 2019;Faria, Johannesson, et al, 2019;Lucek et al, 2023), studies that uncover how they contribute to coupling of genes underlying ecological and reproductively isolating traits, enabling the formation of persistent species are scarce (but see Meyer et al, 2023;Moan et al, 2023). We find compelling evidence for a large inversion enabling host race specific adaptation and progress towards speciation in T. conura.…”

Chromosome-scale genome assembly of the rough periwinkleLittorina saxatilis

“…Moreover, several genomic inversions showing allelic frequency differences between ecotypes (Faria et al 2019a; Westram et al 2021), sex association (Hearn et al 2022) and association with adaptive traits (Koch et al 2021; 2022) have been identified in L. saxatilis and other species of the genus (Reeve et al 2023; Le Moan et al 2023). Inversions can promote the process of local adaptation and speciation and are associated with ecotype divergence in several other natural systems, e .…”

“…saxatilis and other species of the genus (Reeve et al 2023;Le Moan et al 2023). Inversions can promote the process of local adaptation and speciation and are associated with ecotype divergence in several other natural systems, e.g.…”