Plant speciation in the face of recurrent climate changes in the Alps

Abstract

The main, continuous mountain range of the European Alpine System (i.e., the Alps) hosts a diversified pool of species whose evolution has long been investigated. The legacy of past climate changes on the distribution of high-elevation plants as well as taxa differentially adapted to the mosaic of edaphic conditions (i.e., surmised ecotypes on calcareous, siliceous, serpentine bedrocks) and the origin of new species are here discussed based on available evidence from endemic taxa across the Alps. The integration of main spatial and ecological patterns within and among species supports speciation driven by spatial isolation in main glacial refugia where plant populations survived during cold phases and hindered by intense gene flow along main expansion pathways during warm phases. Despite patterns of genetic differentiation matching environmental heterogeneity, processes underlying the dynamics of distribution ranges likely promoted recurrent homogenization of incipient divergence and generally hindered the completion of speciation (except for cases of hybrid speciation). Even intense selective pressures on toxic bedrocks such as serpentine seemingly fail to support the completion of speciation. Accordingly, typical scenarios of ecological speciation whereby local adaptation to environmental heterogeneity initiates and supports long-term reduction of gene flow may rarely be at the origin of stable species in the Alps. Although consistent with neutral processes whereby spatial isolation driven by past climate changes promoted reproductive isolation and yielded limited diversification, mechanisms at the origin of new species across heterogeneous landscapes of the Alps remain insufficiently known. Necessary advances to reliably understand the evolution of biodiversity in the Alps and identify possible museums or cradles of variation in face of climate changes are discussed.

Out of the Balkans and Anatolia to the Western Alps? Surprising phylogenetic implications for two endemicAlyssum(Brassicaceae) species:A. cognensesp. nov. andA. rossetii

“…Wide variation in climatic conditions, geological substrates, soils, topography and elevation over short distances generates a wide diversity of niches and can promote speciation through ecological and allopatric pathways (Boucher, Zimmermann & Conti, 2016;Perrigo, Hoorn & Antonelli, 2020;Tordoni et al, 2020). Pleistocene glaciations also had significant effects on European mountain plant diversity and speciation (Hewitt, 2004;Kadereit, 2017;Parisod, 2022). In the Alps, massive and repeated glaciations led to range reduction, fragmentation and population extinction, which significantly decreased species diversity.…”

“…On the other hand, long-term population persistence may have occurred in glacial refugia, which were mostly located at the periphery of the Alpine ice sheet (Hewitt, 2004;Schönswetter et al, 2005). Geographical isolation in refugia promoted speciation, and with lower dispersal ability, ecological specialization and topographical barriers, may have led to increased rates of endemism (Casazza et al, 2008;Smyčka et al, 2017;Parisod, 2022). Indeed, a high concentration of local endemics is found in the south-eastern and south-western Alps, which were less affected by glaciations and both served as centres for glacial survival and speciation (Casazza et al, 2008;Schmitt, 2009;Aeschimann, Rasolofo & Theurillat, 2011;Tordoni et al, 2020).…”

Adaptive differentiation on serpentine soil in diploid versus autotetraploid populations of Biscutella laevigata (Brassicaceae)

“…Hence, with only significant isolation by distance being detected among tetraploids, genetic differentiation related to NS versus S soils is extremely weak. Even when the ploidy level is accounted for, genetic variation is significantly partitioned among populations of B. laevigata that all appear considerably isolated from one another and selective pressures inherent to S may thus ineffectively reach stable edaphic differentiation (Parisod 2022).…”

“…In particular, to what extent WGD is a nearly-neutral process or promotes the evolution Adaptive differentiation on serpentine soil in diploid versus autotetraploid populations of Biscutella laevigata (Brassicaceae) Tala Bürki 1 , Valentin Pulver 1 , Sandra Grünig 1,2 , Martin Čertner 2,3,4 and Christian Parisod ✉ 1,2 of novel adaptive traits fostering species radiation remains debated (Mayrose et al 2011, Soltis et al 2014. Extant polyploids often differ from their diploid progenitors in morphological, physiological, and ecological characteristics (Otto and Whitton 2000, Ramsey and Schemske 2002, Leitch and Leitch 2008, Nei 2013, but to what extent WGD potentially contributes to a widening of the ecological niche and expansion to new environments in the resulting autopolyploid lineage is still poorly known (Parisod andBroennimann 2016, Baduel et al 2018). In particular, direct evidence of an impact of WGD on adaptation in natural populations or even of the extent to which naturally-occurring autopolyploids are locally adapted is scarce (Ramsey 2011, Martin andHusband 2013).…”

Ecological and evolutionary drivers of phenotypic and genetic variation in the European crabapple (Malus sylvestris (L.) Mill.), a wild relative of the cultivated apple

“…Climate influence demography such as population expansion and contraction, the extent of gene flow among populations, and ultimately the extent of genetic divergence among populations (Edwards et al, 2022). For instance, changes in the climate since the last glacial maximum (LGM) 20,000 years ago have driven the genetic composition of the European crabapple and many other tree species (Comes & Kadereit, 1998;Kremer et al, 2002;Pyhäjärvi et al, 2008;Cornille et al, 2013a;Gugger et al, 2013;Riordan et al, 2016;Lander et al, 2021;Yamada et al, 2021;Parisod, 2021). Climate can also shape phenotypic variation among populations.…”