Chromosomal inversions accelerate genetic evolution and drive ecological speciation across an island gradient.

Abstract

Chromosomal rearrangements are hypothesized to facilitate speciation by suppressing recombination in locally adapted genomic regions, yet how they shape evolutionary rates during rapid divergence remains poorly understood. Here, we investigate the genomic architecture of two sister Carex (Cyperaceae) species on Réunion Island, which rapidly diverged (∼0.5 Mya) to occupy contrasting tropical-montane and dry-subalpine habitats. Using chromosome-level assemblies and population genomics, we show that genomic divergence is not uniform across the genome but is concentrated within specific large-scale inversions. Crucially, genes within these structural variants exhibit significantly accelerated rates of protein evolution, as evidenced by elevated ω, compared to the collinear genome. This is consistent with recombination suppression and subsequent relaxation of purifying selection driving these patterns, which may complement or even outweigh the signal of positive selection. Functional analysis and environmental associations reveal that these "genomic accelerators" include key adaptive loci: Inversions on chromosomes 14 and 28 are enriched for mechanosensitive ion channels and auxin transport, which is consistent with facilitating the interspecific physiological shift to aridity. Partial redundancy analyses reveal that ongoing intraspecific ecological adaptation is highly polygenic across the collinear genome. Our results demonstrate that genomic architecture actively dictates evolutionary speed, suggesting that certain lineages boosted by structural variants may bypass the typical constraints of purifying selection to rapidly exploit vacant ecological opportunities.