Genomic analyses suggest parallel ecological divergence in Heliosperma pusillum (Caryophyllaceae)

Abstract

Summary The mosaic distribution of interbreeding taxa with contrasting ecology and morphology offers an opportunity to study microevolutionary dynamics during ecological divergence. We investigate here the evolutionary history of an alpine and a montane ecotype of Heliosperma pusillum (Caryophyllaceae) in the south‐eastern Alps.From six pairs of geographically close populations of the two ecotypes (120 individuals) we obtained a high‐coverage restriction site associated DNA sequencing (RADseq) dataset that was used for demographic inference to test the hypothesis of parallel evolution of the two ecotypes.The data are consistent with repeated ecological divergence in H. pusillum, uncovering up to five polytopic origins of one ecotype from the other. A complex evolutionary history is evidenced, with local isolation‐with‐migration in two population pairs and intra‐ecotype migration in two others. In all cases, the time of divergence or secondary contact was inferred as postglacial. A metagenomic analysis on exogenous contaminant RAD sequences suggests divergent microbial communities between the ecotypes.The lack of shared genomic regions of high divergence across population pairs illustrates the action of drift and/or local selection in shaping genetic divergence across repeated cases of ecological divergence.

Parallel alpine differentiation inArabidopsis arenosa

“…Such foothill-to-alpine colonisation is also in line with overall expectations about the postglacial history of alpine flora in general (46) and of parallel alpine ecotypic differentiation within a species in particular (47)(48)(49). Interestingly, the exactly opposite alpine-to-foothill colonisation holds for the only other comparable example of multi-parallel differentiation in alpine plants, Heliosperma (14,18), making the comparisons among these systems more challenging.…”

“…This contrasts to remarkably divergent phenotypic outcomes of independent shifts along the gradient of elevation in the other multi-parallel plant system, Heliosperma (14). In this species, however, genetic drift in a small population of the derived (lower-elevation) ecotype was the likely driver of inter-population phenotypic divergence (18). In contrast, genetic drift likely had little impact on structuring diversity in alpine A. arenosa, as indicated by comparable genetic diversity across ecotypes and homogeneous population diversity in A. arenosa in general (27).…”

Meta‐analysis of chromosome‐scale crossover rate variation in eukaryotes and its significance to evolutionary genomics

“…Shared outliers and/or correlated differentiation are then often interpreted as indication that divergent natural selection has targeted the same genes in multiple population pairs, and hence as evidence of parallel evolution at the molecular level. However, such analyses are frequently performed with low physical marker resolution (recent examples: Egger, Roesti, Böhne, Roth, & Salzburger, ; Perreault‐Payette et al., ; Ravinet et al., ; Raeymaekers et al., ; Rougemont et al., ; Stuart et al., ; Trucchi, Frajman, Haverkamp, Schönswetter, & Paun, ). Consequently, single markers are highly unlikely to coincide with polymorphisms under direct selection.…”

Genetic and epigenetic variations associated with adaptation to heterogeneous habitat conditions in a deciduous shrub

“…This was also supported by MMRR showing potential effect of habitat environment on genetic differentiation. Although strong gene flow has homogenized the genetic differentiation across the genome, adaptive loci will remain due to similar pressure (Trucchi, Frajman, Haverkamp, Schönswetter, & Paun, 2017). Only several plastic functional traits were investigated, and very limited loci were detected by AFLP.…”