Polygenic routes lead to parallel altitudinal adaptation in Heliosperma pusillum (Caryophyllaceae)

Abstract

Understanding how organisms adapt to the environment is a major goal of modern biology. Parallel evolution - the independent evolution of similar phenotypes in different populations - provides a powerful framework to explore this question. Here, we quantified the degree of gene expression and functional parallelism across replicated ecotype formation in Heliosperma pusillum (Caryophyllaceae) and gained insights into the architecture of adaptive traits. Population structure analyses and demographic modelling confirm the previously formulated hypothesis of parallel polytopic divergence of montane and alpine ecotypes. We detect a large proportion of differentially expressed genes (DEGs) underlying adaptation of each replicate ecotype pair, with a strikingly low amount of shared DEGs across pairs. Functional enrichment of DEGs reveals that the traits affected by divergent gene expression are the same across ecotype pairs, in strong contrast to the non-shared genetic basis. The remarkable redundancy of differential gene expression indicates that diverged adaptive traits are highly polygenic. We conclude that polygenic traits appear key to opening multiple routes for adaptation, widening the adaptive potential of organisms.

Genomic basis and phenotypic manifestation of (non-)parallel serpentine adaptation inArabidopsis arenosa

“…This shows the important role of genetic redundancy in rapid adaptations with a polygenic basis (Boyle et al, 2017; Barghi et al, 2020; Láruson et al, 2020). That genetic redundancy is an important factor underlying parallel adaptation towards complex environmental challenges that have been also shown in other systems such as in alpine Heliosperma pusillum (Trucchi et al, 2017; Szukala et al, 2021) or dune Senecio lauttus (James, Allsopp, et al, 2021), but also from more narrowly defined environments – metal-polluted mines in Silene uniflora (Papadopulos et al, 2021) or temperature adaptations in Drosophila simulans (Barghi et al, 2019). In summary, given the expected polygenic basis of adaptation, it is unlikely that limited gene-level parallelism simply reflects genetic architecture but rather represents an effect of genetic redundancy.…”

Parallel adaptation to lower altitudes is associated with enhanced plasticity in Heliosperma pusillum (Caryophyllaceae)

“…Among the constitutive genes identified in each pair, 26 genes (Supplementary Table S1) were shared by both ecotype pairs (more than chance expectations; hypergeometric p < 3e-24). Finally, eight of these genes (Supplementary Table S1) were also found to be DE in both ecotype pairs in a non-native, common garden environment in a previous study (Szukala et al, 2022), despite the different growing conditions and developmental stage.…”

“…Rchb. (Caryophyllaceae; Trucchi et al, 2017;Szukala et al, 2022). This species forms altitudinal ecotypes previously shown to bear cross-generations phenotypic differentiation (Bertel et al, 2016b(Bertel et al, , 2018.…”

“…1,300 m). Importantly, genomic and transcriptomic studies (Trucchi et al, 2017;Szukala et al, 2022) have demonstrated, among others with coalescent methods, that pairs of geographically clustered montane and alpine ecotypes in the south-eastern Alps have diverged at least four times independently, representing a case of parallel evolution and can thus be regarded as natural evolutionary replicates.…”

“…This variability is likely at least in part due to plasticity, given that reduced genetic variation was found in the small and strongly confined montane populations (Fig. 2f; Trucchi et al, 2017;Szukala et al, 2022).…”