Parallel adaptation in natural populations

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When and under which circumstances does evolution repeat itself? Evolution is driven by a deterministic forces like directional selection but also by chance, what brings an intriguing question about its predictability. Because evolution is a historical process, we have limited possibilities how to experimentally test for such question in its full complexity, i.e. in natural environments. Distinct lineages that independently evolved under similar conditions (i.e. underwent parallel adaptation) represent rare cases of such an experiment that had happened in nature. Thus, knowing how predictable is parallel evolution in such natural experiments should inform about how deterministic is evolution in general. That can provide insights into predictive evolution of crops, pathogens or species under climate change.

        

We study the probability of parallel adaptive evolution on genome level, by resequencing genomes of independently adapted lineages of different Brassicaceae species to the same selective agens. We focus on parallel alpine adaptation in Arabidopsis arenosa and A. halleri and in Caradmine amara, adaptation to whole genome duplication in C. amara, A. arenosa and A. lyrata or substrate adaptation in A. arenosa and A. lyrata. In addition to discoveries of particular loci reused by natural selection, we aim to understand the evolutionary mechanisms determining if genomic parallelism happens and at which level it is manifested (single nucleotide polymorphism - SNP, gene or functional pathway).

Our recent project focused on seven independently adapted alpine lineages in Arabidopsis. We demonstrated that the probability of gene reuse decreased with divergence between compared lineages, likely because less alleles are shared among distantly related lineages. This means that more divergent lineages have less variation available for gene reuse and, subsequently, are less likely to evolve parallel genetic solutions to similar challenges. In general, our results suggest that genetic basis of adaptive evolution could be better predictable in closely related lineages with shared pool of adaptive alleles while it becomes subject of change in distantly related lineages.

To explore parallel adaptation at the gene expression level, we also sequenced transcriptomes of four foothill - alpine population pairs of independent origin. We found that non-random number of genes indeed exhibit differences in gene expression between foothill and alpine populations across multiple mountain regions. This suggests alpine plants found similar solutions to alpine stress multiple times even in terms of gene expression, in particular in genes involved in biotic stress response. As a parallel project, in collaboration with Innsbruck University, we also investigate parallelism at the metabolomic level (Gas chromatography and mass spectrometry analysis) to compare metabolomic profiles, i.e. flavonoid content and hormonal profiling, across the same set of populations.

Funding: Junior researcher project of Czech Science Foundation (17-20357Y) & Junior group leader research project of Charles University in Prague (Primus/SCI/35)

Team members involved: Magdalena Bohutínská, Jakub Vlček, Guillaume Wos, Paolo Bartolić

Key collaborators on this work are

Tanja Slotte (Univ. Stockholm)

Graham Coop (UC Davis, USA)

Levi Yant (JIC Norwich)

Karol Marhold (Slovak Academy of Sciences, Slovakia)

 

Parallel origin of alpine ecotypes of Arabidopsis arenosa in distinct mountain ranges