Long-term demographic processes of species leave behind traces in various forms, such as spatial genetic structure in extant populations and fossil remains in the ground. Combining these complementary sources of evidence from a dense sampling across the entire natural range of Swiss stone pine helped us to unravel the glacial history of this timberline species.
Above: Field site with a view: Swiss stone pine forest on Riederfurka above Aletsch glacier, with a historic monument in the foreground and geological monuments in the distance (photo: Felix Gugerli).
Imagine walking along the upper end of forest occurrence in the Alps or a similar high-elevation mountain system. Looking around, you will likely recognize certain imprints of former glacial activity, visible as remnant moraines and rocks showing glacier polish. These typical features of today’s alpine landscape remind us that this habitat was formerly ice-covered but has since been (re-)colonized by forest trees and their associated plants, fungi and animals. You might wonder how slow-growing, long-lived trees could swiftly cope with the long-term dynamics of past glacial–interglacial cycles by shifting their range to benign habitats outside their alpine terrain—and back again following the retreating ice cover.
Swiss stone pine (Pinus cembra), the emblematic tree species of the timberline ecotone, on the verge of the Aletsch glacier (Switzerland)—yet the largest, but also quickly melting body of ice in the European Alps (photo: César Morales-Molino).
Swiss stone pine (Pinus cembra) is an emblematic tree species with diverse and fascinating growth forms that reflect long-lasting endurance of extreme alpine weather conditions. This species occurs in a beautiful, almost mystical alpine landscape in the European Alps and in scattered places in the Carpathian Mountains, and it displays an intriguing interaction with nutcrackers that hoard its seed for winter food. How could such a species cope with moving to and fro its current habitat in response to shifting climates and glaciers? And how could we best decipher this demographic history using the material at hand? The extant trees reveal their population history through their genealogy: It is common routine to unveil demographic processes using genetic markers (phylogeography, demographic modelling). Similarly hidden information can be retrieved from remains of former occurrences, e.g., in lake sediments or even buried underneath now retreating glaciers: Here, we find fossil pollen deposits, or occasional macrofossils that provide evidence of immediate presence of a given species near the place of discovery. However, both approaches have their limitations: Genetic inference lacks precise dating or localization of the migration routes and of refugial areas, and palaeoecology does not disclose intraspecific differentiation to inform about which genetic lineage occurred at a given site in the past.
Cover article: (Open Access)
Gugerli, F., Brodbeck, S., Lendvay, B., Dauphin, B., Bagnoli, F., Tinner, W., Van Der Knaap, W.O., Höhn, M., Vendramin, G.G., Morales-Molino, C. & Schwörer, C. (2023) A range-wide postglacial history of Swiss stone pine based on molecular markers and palaeoecologicalevidence. Journal of Biogeography, 50, 1049–1062. https://doi.org/10.1111/jbi.14586
There are clear benefits if geneticists and palaeoecologists are teaming up. Both disciplines contribute their relevant share when it comes to deciphering the history of a species in a spatio-temporal context and provide complementary insights into the past. Doing this in a wonderful study system such as Swiss stone pine forest makes the (field)work even more appealing. However, sampling often comes with strenuous ascents to high-elevation forests, possibly hauling coring equipment to picturesque mountain lakes. But efforts are well compensated once floating on a coring platform or strolling among bizarre trees to collect needle samples for DNA extractions, with nervous nutcrackers croaking above your head fearing food theft. Not to mention the beautiful view to high-elevation, still glacier-covered mountains nearby. Such work resembles forensics: digging in the “dirt” to uncover the past through palaeoecological evidence in the ground, while conducting molecular-genetic lab work to derive testimonies left behind on the “crime scene”.
The European nutcracker (Nucifraga caryocatactes) is the predominant seed disperser of P. cembra. Cached seed that are not recovered and remain in the ground may subsequently germinate and establish to form the new Swiss stone pine generation (photo: Eike Lena Neuschulz).
Admittedly, the fun part stops once back in the labs—seemingly endless hours of identifying and counting pollen or macrofossils, thousands of pipette tips wasted. But the reward comes back once analyses shape the data piles into meaningful heaps and structures. In the case of Swiss stone pine: We found a remarkably distinct spatial structure of two lineages comprising five genetic clusters, but rather evenly distributed genetic diversity, implying that demographic changes over long periods did not have a marked (negative) effect on genetic diversity. To our surprise, the separation of the two main lineages did not coincide with the pronounced geographical disjunction between the Alps and the Carpathian Mountains, but it appeared in the Central Alps, in an area previously recognized as a bio- and phylogeographic contact zone. This finding suggests a more ancient split of these lineages, and indeed, demographic inference estimated the divergence back to more than 200,000 years ago. This period coincides with a particularly long warm stage (MIS7 interglacial). Such warm periods, but also the very cold phases in-between (glacial stadials), led to geographical isolation, whereas the largest range expansions occurred in the course of cool transitional periods (interstadials) like the Bølling/Allerød during the last deglaciation. While fossil evidence does not reach as far back in time to document the ancient split of lineages, the palaeoecological records compiled allowed us to narrow down refugial areas occupied by Swiss stone pine during the Last Glacial Maximum (LGM) to the Po plain of northern Italy and expanding into Friuli and Slovenia, another area in the Carpathian forelands, in the Hungarian plain, and possibly in the Bohemian massif. The footprints of respective re-colonization routes, inferred from dated palaeoecological findings, match well with the genetic structure identified in extant Swiss stone pine populations—evidence of the added value when combining datasets and looking across disciplinary boundaries.
While these outcomes are interesting per se, they are not the end of the story yet. Is it possible to obtain a refined picture of palaeoecological records? What was the genetic make-up of the refugial populations? Can we track the evolution of genetic clusters along their migration routes? Are there changes in allele frequencies at adaptive loci? Further research avenues consist of coring sediments in places where it has not been done, but where LGM or even older occurrences may be possible, and if not done so, distinguishing Pinus pollen in existing and new samples to the species level to separate P. cembra from P. sylvestris/uncinata. Analyses of DNA retrieved from macrofossils may shed light onto the genetic composition of ancient populations, including environmentally driven changes in adaptive genetic variation.
Coring platform on an alpine lake (Lai da Vons, Switzerland), with Swiss stone pine overseeing that sediment coring is done accurately (photo: Christoph Schwörer).
But the most pressing question remains yet unanswered: What is the fate of Swiss stone pine in view of a seemingly super interglacial as a consequence of anthropogenic climate warming? These trees are among the oldest in European mountain forests, as such reflecting demographic stasis, but they are deemed to respond quickly to rapidly changing climate by moving uphill. Unless demographic (dispersal) or adaptive processes keep up the pace of climate warming, we anticipate a gradual decline through competitive exclusion and possibly local extinction of Swiss stone pine—a worrying perspective for this magnificent timberline forest ecosystem and the species it is composed of.
Felix Gugerli, Senior Scientist, Biodiversity & Conservation Biology, Swiss Federal Research Institute WSL, Birmensdorf, Switzerland
César Morales-Molino, Postdoctoral researcher, Grupo de Ecología y Restauración Forestal, Departamento de Ciencias de la Vida, Facultad de Ciencias, Universidad de Alcalá, Alcalá de Henares, Spain
Christoph Schwörer, Group leader, Institute of Plant Sciences and Oeschger Centre for Climate Change Research, University of Bern, Bern, Switzerland