Genetic Drift Linked to Heterogeneous Landscape and Ecological Specialization Drives Diversification in the Alpine Endemic Columbine Aquilegia thalictrifolia

Abstract

The European Alpine system is an extensive mountain range, whose heterogeneous landscape together with Quaternary climatic oscillations significantly affected organismal diversity and distribution in Europe. The model genus Aquilegia represents a textbook example of a rapid and recent radiation through the Northern hemisphere, with the majority of the European taxa occuring in the Alpine system. However, the processes governing genetic differentiation of the genus in this complex geographic area are still widely unexplored. In this work, we used 9 microsatellite loci to study the genetic structure and diversity of 11 populations of Aquilegia thalictrifolia Schott & Kotschy, an alpine taxon characterized by a marked ecological specificity. We found that, despite the endemic and fragmented distribution, A. thalictrifolia has overall high levels of heterozygosity, which is consistent to the substantial inbreeding depression that characterizes the genus. Strong spatial genetic structuring of populations suggests a historical prevalence of genetic drift over gene flow, with natural barriers and ecological niche hindering migration. An analytical comparison of fixation and population differentiation indexes allowed us to infer hypotheses of the postglacial history and more recent demographic events that have influenced the genetics of the species. Overall, our results indicate allopatry as a major force of differentiation in the European scenario, likely to underlie the development of taxonomic boundaries in a broader geographic context. This adds to previous notions on the primary evolutionary forces shaping the Aquilegia radiation in Europe.

Levels and patterns of genetic diversity differ between two closely related endemicArabidopsisspecies

“…Overall, we observe that the genetic variation level in the two endemic species is lower than for the other Arabidopsis species with wide distribution range and the same mating system (self-incompatibility). For comparison, the narrow endemic Aquilegia thalictrifolia, distributed in a few valleys of the Italian South-Eastern Alps, also displayed a higher average Hexp (0.68 ± 0.19), which is twice as high as for the two Arabidopsis endemics (Lega et al 2014). In A. cebennensis π, θw and Hexp were low and almost similar for the three subpopulations, and similar to what was estimated for the whole species.…”

Geography and Environment Shape Landscape Genetics of Mediterranean Alpine Species Silene ciliata Poiret. (Caryophyllaceae)

“… Geng et al (2009) found short-distance genetic structure patterns related to limited gene dispersal along with substantial levels of gene flow and slow rates of genetic drift between topographically separated populations. Many other authors reported genetic structure at larger landscape scales (e.g., Aægisdóttir et al, 2009 ; Lega et al, 2014 ) related to natural barriers to gene flow. In our case, we detected both coarse-scale mountain range clustering and finer-scale short distance population differentiation.…”

Is phenotypic canalization involved in the decline of the endemic Aquilegia thalictrifolia? Rethinking relationships between fluctuating asymmetry and species conservation status

“…AT12 and AT13; Lega et al . ). This may be due to events that occurred during the population's history (e.g.…”

“…However, in spite of the narrow distribution, the critical conservation status and the presence of self‐compatibility, A. thalictrifolia maintains a high level of heterozygosity (Lega et al . ). Moreover, it grows at the base of wet cliffs mainly in unvegetated areas, a habitat considered highly stable, not affected by rapid successional dynamics of vegetation and only occasionally disturbed by rock falls.…”