Differences in dispersal abilities and habitat specialization determine the postglacial range expansion of three high-elevation plants
Above: Steep limestone cliffs in the Pre-Pyrenees, a glacial refugium for the study species.
When I first visited the Pyrenees as a child from the Mediterranean lowlands, I got fascinated by the accordion-like folded landscape, the green and dense meadows, and the amount of unknown colorful flowers which painted the entire picture. In the coming years, I began to understand what processes and conditions produced that landscape and vegetation, and the original fascination slowly turned into questions. Inspired by classical and more recent literature about glacial refugia for plants from the European Alps, the question started to burn inside me: what about the Pyrenees? What happened in these mountains that create an almost perfect border between the Mediterranean and the template climate? As claimed in some classical studies, did mountain plants in the Pyrenees have more possibilities of surviving the cold stages than their counterparts in the Alps? And looking in the opposite temporal direction, what possibilities do they have to cope with climate change in the near future? To date, the lack of a critical mass of molecular data for Pyrenean mountain plants does not allow us to answer these questions, and that is the reason why we started the project in which our publication is framed.
Cover image article: (Free to read online for a year.)
Carnicero, P., Wessely, J., Moser, D., Font, X., Dullinger, S. & Schönswetter, P. (2022). Postglacial range expansion of high-elevation plants is restricted by dispersal ability and habitat specialization. Journal of Biogeography, 49, 1739– 1752. https://doi.org/10.1111/jbi.
In this project entitled Conserving intraspecific diversity in a warmer world, we aimed at tackling the above mentioned questions and to understand the impact of past and current changes in the diversity within species. Nine species endemic to the Pyrenees were selected for this purpose, and in this first publication of the project, we present the results for three species with preference for carbonate bedrock. In the general trend of searching for individual examples, which could be a proxy for a wider group of ecologically similar species, I expected these three species to be good models to explain what happened to other species with similar bedrock preference. Nothing further from the truth. Our results showed two different responses to the end of the cold stage: one expanded rapidly, while the other two showed postglacial stasis; they remained in the areas where they survived the cold stages, with only a few colonizations of areas previously under the ice. Why?
When we were seeking an answer to this incongruent pattern, we went back to basic questions that a biologist should never forget: where and how do our study species live, disperse, reproduce, etc.? And these indeed brought us to a reasonable explanation. Salix pyrenaica, the species, which rapidly expanded and colonized previously glaciated areas, is a very good disperser and often able to find a place to grow provided a carbonate bedrock. In a way, we can call Salix pyrenaica a generalist of carbonate bedrocks. This ecological trait allowed it to rapidly and efficiently explore the newly available terrain after glaciation, by dispersing many fruits, and a considerable amount of them finding a proper spot to grow. Instead, Cirsium glabrum and Silene borderei showed a much more static picture. The areas where, according to our genetic and climatic data, they survived the cold stages are almost a perfect match to the areas where they occur nowadays. In contrast, they barely occur in potentially suitable areas that were under the glaciers during the ice ages. Silene borderei has no particular adaptations for long-distance dispersal, but Cirsium glabrum does. While it is true that Silene borderei indeed showed a more static postglacial history than Cirsium glabrum, something still has to explain why both expanded so little after the glaciations as compared to Salix pyrenaica. In contrast to the latter, Cirsium glabrum and Silene borderei are microsite-specialists in terms of habitat selection, which imposes a severe drawback in terms of colonization of new areas: even if dispersing seeds efficiently, only a very small portion of them will find a suitable habitat to grow, rendering the colonization of new areas an extremely slow process.
Schematic representing the impact of habitat specialization in range expansion. In the left panel, a generalist like Salix pyrenaica showing multiple successful dispersal events. In the right panel, for a micro-site specialist like Cirsium glabrum, most of the dispersal events will not succeed.
How close do these results bring us to inferring where the glacial refugia for high-elevation species in the Pyrenees actually were? Despite the uncertainties conferred by the above mentioned results, we are in the position of formulating some statements and, of course, new questions. On the one hand, Salix pyrenaica shows the expected behavior of contraction-expansion of glacial refugia: survival of a harsh period in refugia, and posterior expansion from there. Unfortunately, this expansion seems to have been so fast and involved a high degree of exchange of genes between expanding populations, that the signal for identifying the refugia in detail is too weak. In this case, we can state that there were at least two refugia in the east and the west. Instead, for Cirsium glabrum and Silene borderei we can clearly state that the eastern and western Pre-Pyrenees played an important role for the survival of the species during the ice age. The Pre-Pyrenees have already been suggested as a main refugium for species with carbonate bedrock preference, and our results confirm this.
In conclusion, our results show that species-specific ecological traits play a major role in the recent history of the studied species. Thus, for species like Cirsium glabrum and Silene borderei, refugia remained their permanentdistributions, while others, like Salix pyrenaica, started remarkable range expansions from the refugia. Ecological traits therefore strongly impact which species have narrow or widespread distributions. Future molecular data coming from our and other projects will provide further evidence to confirm, reject or reformulate the general applicability of the hypotheses formulated here.
Pau Carnicero, PhD, Department of Botany, University of Innsbruck
I would like to thank Peter Schönswetter for his relevant feedback on this blog post.