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Roesti, M.

Publications and source records attributed to Roesti, M..

5 recordsLinked to original sources

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↗

Heterogeneous evolution of effective recombination landscapes across percomorph fishes

Recombination shapes allelic combinations across the genome and plays a central role in adaptation and speciation. While recombination rates are known to vary and evolve, how recombination landscapes diverge between populations and which processes drive this divergence remains poorly understood. Here, we use the Population Recombination Divergence Index (PRDI) to quantify divergence in effective recombination landscapes between seven pairs of populations and species from four percomorph fish lineages (cichlids, sticklebacks, killifish, and clownfish). While accounting for stochasticity and confounders of linkage disequilibrium (LD) -based recombination rate estimates, we find that recombination landscapes diverged substantially in all comparisons. This divergence generally increases with genetic differentiation and divergence time, but the amount of PRDI accumulated per unit of genetic divergence (FST), net nucleotide divergence (da), or divergence time varies markedly among population and species pairs. Comparisons across systems suggest that PRDI accumulation tends to be faster (per unit of FST, da, or divergence time) in pairs with higher inferred gene flow. We also introduce a local version of PRDI (_l) to better characterize genomic heterogeneity in effective recombination divergence. We find that higher inferred gene flow between populations tends to be associated with stronger intragenomic correlation between local FST and _l. Finally, we propose a conceptual framework for investigating how divergent selection and gene flow may interact to shape effective recombination landscape divergence. Our work highlights the heterogeneous dynamics of effective recombination landscape evolution, and motivates further theoretical and empirical efforts to integrate recombination landscape evolution into studies of adaptation and speciation.

evolutionary biology↗

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↗

Species interactions, divergence, and the rapid evolution of ecological sexual dimorphism in threespine sticklebacks

Variation in ecological sexual dimorphism (ESD), defined as differences between the sexes in ecologically-relevant traits, is a common feature of adaptive radiation, yet its causes remain unclear. Competition between the sexes for alternative resources can promote evolution of ESD when interspecific competition is reduced (competition hypothesis). Alternatively, sex-specific selection on ecological traits might weaken under strong directional selection in new environments (divergence hypothesis). We tested these hypotheses via their expected evolutionary outcomes in threespine stickleback populations from southwestern Canada. We found striking among-population variation in magnitude of ESD. Consistent with the divergence hypothesis, dimorphism along the main axis of body shape variation was reduced in recently derived freshwater populations compared to their contemporary marine ancestor. However, dimorphism only weakly declined with increasing phenotypic divergence. Average dimorphism along major freshwater body shape axes was similar between solitary populations and those coexisting with a competing species, contrary to the competition hypothesis. Instead, sympatry with a Benthic ecotype led to increased sexual size dimorphism in Limnetics, and total shape dimorphism was elevated in the sympatric stickleback species compared with solitary populations. In contrast to the mechanisms considered in existing theory, interactions in sympatry might produce elevated ESD by generating novel sex-specific selection pressures.

evolutionary biology↗

Chromosomal inversions can limit adaptation to new environments

Chromosomal inversions are often thought to facilitate local adaptation and population divergence because they can link multiple adaptive alleles into non-recombining genomic blocks. Selection should thus be more efficient in driving inversion-linked adaptive alleles to high frequency in a population, particularly in the face of maladaptive gene flow. But, what if ecological conditions and hence selection on inversion-linked alleles change? Reduced recombination within inversions could then constrain the formation of optimal combinations of pre-existing alleles under these new ecological conditions. Here, we outline this idea of inversions limiting adaptation and divergence when ecological conditions change across time or space. We reason that the benefit of inversions for local adaptation and divergence under one set of ecological conditions can come with a concomitant constraint for adaptation to novel sets of ecological conditions. This limitation of inversions to adaptation may also provide one possible explanation for why inversions are often maintained as polymorphisms within species.

evolutionary biology↗