Výsledky projektu Genetická podstata adaptace na hadcový substrát u Arabidopsis arenosa

Parallel evolution is common in nature and provides one of the most compelling examples of rapid environmental adaptation. In contrast to the recent burst of studies addressing genomic basis of parallel evolution, integrative studies linking genomic and phenotypic parallelism are scarce. Edaphic islands of toxic serpentine soils provide ideal systems for studying rapid parallel adap- tation in plants, imposing strong, spatially replicated selection on recently diverged populations. We leveraged threefold indepen- dent serpentine adaptation of Arabidopsis arenosa and combined reciprocal transplants, ion uptake phenotyping, and available genome-wide polymorphisms to test if parallelism is manifested to a similar extent at both genomic and phenotypic levels. We found pervasive phenotypic parallelism in functional traits yet with varying magnitude of fitness differences that was congruent with neutral genetic differentiation between populations. Limited costs of serpentine adaptation suggest absence of soil-driven trade-offs. On the other hand, the genomic parallelism at the gene level was significant, although relatively minor. Therefore, the similarly modified phenotypes, for example, of ion uptake arose possibly by selection on different loci in similar functional pathways. In summary, we bring evidence for the important role of genetic redundancy in rapid adaptation involving traits with polygenic architecture.

Relative contributions of pre-existing vs de novo genomic variation to adaptation are poorly
understood, especially in polyploid organisms. We assess this in high resolution using
autotetraploid Arabidopsis arenosa, which repeatedly adapted to toxic serpentine soils that
exhibit skewed elemental profiles. Leveraging a fivefold replicated serpentine invasion, we
assess selection on SNPs and structural variants (TEs) in 78 resequenced individuals and
discover significant parallelism in candidate genes involved in ion homeostasis. We further
model parallel selection and infer repeated sweeps on a shared pool of variants in nearly all
these loci, supporting theoretical expectations. A single striking exception is represented by
TWO PORE CHANNEL 1, which exhibits convergent evolution from independent de novo
mutations at an identical, otherwise conserved site at the calcium channel selectivity gate.
Taken together, this suggests that polyploid populations can rapidly adapt to environmental
extremes, calling on both pre-existing variation and novel polymorphisms.

Serpentine barrens are among the most challenging settings for plant life. Representing a perfect storm of hazards, serpentines consist of broadly skewed elemental profiles, including abundant toxic metals and low nutrient contents on drought-prone, patchily distributed substrates. Accordingly, plants that can tolerate the challenges of serpentine have fascinated biologists for decades, yielding important insights into adaptation to novel ecologies through physiological change. Here we highlight recent progress from studies which demonstrate the power of serpentine as a model for the genomics of adaptation. Given the moderate – but still tractable – complexity presented by the mix of hazards on serpentine, these venues are well-suited for the experimental inquiry of adaptation both in natural and manipulated conditions. Moreover, the island-like distribution of serpentines across landscapes provides abundant natural replicates, offering power to evolutionary genomic inference. Exciting recent insights into the genomic basis of serpentine adaptation point to a partly shared basis that involves sampling from common allele pools available from retained ancestral polymorphism or via gene flow. However, a lack of integrated studies deconstructing complex adaptations and linking candidate alleles with fitness consequences leaves room for much deeper exploration. Thus, we still seek the crucial direct link between the phenotypic effect of candidate alleles and their measured adaptive value – a prize that is exceedingly rare to achieve in any study of adaptation. We expect that closing this gap is not far off using the promising model systems described here.