Saladin, V. | Search bioRxiv

bioRxiv2026

A chromosomal inversion acts as a hotspot for divergence in multiple ecologically relevant traits

Chromosomal inversions are proposed to aid local adaptation to divergent habitats when there is gene flow by creating regions of low recombination that can maintain tight linkage between multiple locally adaptive alleles. However, key theoretical predictions about the role of chromosomal inversions in local adaptation remain largely untested in empirical systems. Here, we test the prediction that inversions will concentrate relatively small genetic effects across multiple ecologically relevant traits by exploring inversion-phenotype associations of three inversions in threespine stickleback (Gasterosteus aculeatus). Using complementary approaches of association mapping in wild-caught individuals and genetic mapping in lab-raised individuals from two divergent genomic backgrounds, we found that an inversion on chromosome XXI influences multiple ecologically relevant traits. The inversion has small-to-moderate effects on these traits, as expected for inversions involved in polygenic adaptation. Further consistent with theoretical predictions, inversion heterozygotes show intermediate phenotypes. While most inversion-phenotype associations are consistent across different genomic backgrounds and experimental approaches, some inversion-phenotype associations were specific to a single dataset. These results indicate that the phenotypic effects of inversions are shaped by both genomic and environmental context, which could facilitate population-specific adaptation. Together, these results support the role of the chromosome XXI inversion in ecological divergence in threespine stickleback. More broadly, our results suggest that inversions can contribute to local adaptation by preserving linkage between small-effect adaptive alleles despite extensive gene flow.

evolutionary biology↗

bioRxiv2026

Disentangling site-specific and shared local adaptation in a classic system of repeated evolution

Repeated divergence across contrasting habitats is widely used to infer natural selection and adaptation. However, such inferences remain inherently correlative and capture only adaptation shared among populations from the same habitat type, thereby missing site-specific adaptation unique to individual populations. Field transplant experiments test adaptation more directly by measuring fitness in nature, but they are typically limited to pairwise reciprocal exchanges between populations and therefore cannot separate shared habitat-level and unique site-specific adaptation. Here we extend the typical transplant framework to include multiple populations from both within and across habitat types, allowing fitness variation to be partitioned into shared habitat-level and unique site-specific components. We apply this framework to lake-stream stickleback, a classic system for studying adaptation via repeated divergence. Specifically, we transplanted laboratory-reared fish from a panmictic lake population and four independent stream populations across one lake and two stream sites. Stream fish outperformed lake fish in streams and vice versa, demonstrating adaptive lake-stream divergence. However, at both stream sites, local stream fish also outperformed foreign stream fish. Strikingly, this site-specific advantage was twice as large as the advantage of foreign stream fish over lake fish, reflecting the fitness benefit of shared stream adaptation. These results show that most fitness-relevant evolutionary variation in this system is unique to individual populations and therefore invisible to approaches that rely on repeated evolution to infer adaptation. More broadly, our work underscores the importance of ecological scale for understanding adaptation and evolutionary predictability. Significance statementRepeated evolutionary responses to similar environments commonly serve as evidence for adaptation. However, such comparative approaches do not directly measure fitness or resolve whether variation among populations from the same nominal habitat reflects adaptation to site-specific conditions. Using laboratory-raised lake and stream stickleback transplanted both within and across habitat types, we separated the fitness effects of shared adaptation to the same nominal habitat and site-specific adaptation unique to individual populations. Site-specific adaptation explained two-thirds of the total fitness variation, exceeding the contribution of adaptation shared among populations from the same habitat type. Our study highlights that natural selection generates fitness-relevant divergence at finer ecological scales than comparative approaches can resolve, underscoring the irreplaceable value of field experiments for understanding evolution.

evolutionary biology↗