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 investigate the evolutionary potential of populations, the constraints of evolution, its repeatability and therefore its predictability. 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 support a previously formulated hypothesis of parallel polytopic divergence of montane and alpine ecotypes. We detect a large proportion of differentially expressed genes (DEGs) underlying divergence within each replicate ecotype pair, with a strikingly low number of shared DEGs across pairs. Functional enrichment of DEGs reveals that the traits affected by significant expression divergence are largely consistent across ecotype pairs, in strong contrast to the nonshared genetic basis. The remarkable redundancy of differential gene expression indicates a polygenic architecture for the diverged adaptive traits. 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 in Arabidopsis arenosa

“…This is in congruence with findings in Senecio lautus (James et al 2021b,c), in which similar phenotypes with large divergence times within-population pairs have arisen via mutational changes in different genes, although many of these genes shared the same biological functions. However, even in the system of a recent postglacial alpine-montane divergence, such as Heliosperma pusillum (Trucchi et al 2017;Szukala et al 2022), similar phenotypes were also achieved via selection on different genes in the same functional pathways. In such polygenic systems, we expect genetic redundancy, that is, mutations in different genes (possibly within the same pathway) can lead to similar phenotypes and thus to phenotypic parallelism (Hermisson and Pennings 2017;Höllinger et al 2019;Barghi et al 2020).…”

Parallel Differentiation and Plastic Adjustment of Leaf Anatomy in Alpine Arabidopsis arenosa Ecotypes

“…On the one hand, phenotypic plasticity may reduce the power of natural selection, hindering specialization via genetic differentiation [ 51 ]. On the other hand, enhanced plasticity may enable the colonization of new environments, fostering adaptation [ 29 ]. Arabidopsis arenosa represents an excellent system to test for the role of plasticity in response to habitat differentiation, and future studies could test for adaptive advantages, or disadvantages, of the extent of plasticity.…”

“…As small populations often bear limited/low genetic variation, the source of adaptive variation is reduced, and genetic drift is increased due to a smaller number of individuals leading to stochastic changes [ 27 , 28 ]. However, not only particular traits per se , but also the ability to adjust them plastically can be under selection and differ between ecotypes [ 29 , 30 ].…”

“…Grown under the same environmental conditions, genetically determined differences between populations remain, while environmentally induced plastic differences diminish [ 39 ]. Comparing traits of one ecotype in the native versus the foreign environment also allows concluding on its potential to plastically adjust a trait, which may be particularly important for phylogenetically young populations or ecotypes [ 29 ].…”

A simple conceptual framework and nomenclature for studying repeated, parallel and convergent evolution

“…Second, vague or imprecise terms are likely to impact early career researchers and newcomers to the field, who are sedimenting their knowledge, creating a superfluous barrier to their understanding. For instance, in biodiversity genomics parallel evolution has been used to refer to 'parallel changes at the molecular sequence level' (Natarajan et al, 2015), 'parallel replacements/substitutions' (Natarajan et al, 2015;Mendes et al, 2016;Lee et al, 2018), 'parallel evolution and fixation of mutations' (Stern, 2013), 'parallel selection on standing genetic variation' (Pease et al, 2016), 'parallel adaptation' (Stoltzfus & McCandlish, 2017;Bohutínská et al, 2021;Konečná et al, 2021;Szukala et al, 2022), 'parallel evolution of phenotypes' (Colosimo et al, 2005;Szukala et al, 2022), among other terms. Third, because nuances in the terms are likely field-specific (when considering developmental biology, physiology, ecology, genomics as di erent fields within biology), they may obstruct multidisciplinary e orts.…”