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The subterranean ecosystem exerts strong selection pressures on the organisms that thrive in it. In response, obligate cave-dwellers have developed a series of morphological, physiological, and behavioral adaptations, such as eye reduction, appendage elongation, low metabolic rates or intermittent activity patterns, collectively referred to as troglomorphism. Traditionally, studies on cave organisms have been hampered by the difficulty of sampling (i.e., small population sizes, temporal heterogeneity in specimen occurrence, challenges imposed by the difficult-to-access nature of caves). Here, we circumvent this limitation by implementing a museomics approach. Specifically, we aim at comparing the genetic population structures of five cave spider species demonstrating contrasting life histories and levels of troglomorphism across different caves in the northern Dinarides (Balkans, Europe). We applied a genome-wide hybridization-capture approach (i.e., HyRAD) to capture DNA from 117 historical samples. By comparing the population genetic structures among five species and by studying isolation by distance, we identified deeper population structuring and more pronounced patterns of isolation by distance in the highly troglomorphic Parastalita stygia and Stalita pretneri ground dwellers, while the three web-building Troglohyphantes species, two of which can occasionally be found in surface habitats, showed less structured populations compatible with higher dispersal ability. The spatial distribution of genetic groups revealed common phylogeographic breaks among lineages across the studied species, which hint at the importance of environmental features in driving dispersal potential and shaping underground diversity.

The Alps played an important role in the biogeography of European plants and acted as a refugium for numerous species during the interglacial cycles. We investigated Nuphar pumila, one of the most emblematic glacial relicts of the Alps, by carrying out exhaustive literature and field surveys to collect relevant data on its distribution and threats. We further evaluated the level of introgression with the closely related N. lutea based on microsatellite data from natural populations across the Alps as well as from all ex situ collections and reintroductions in Switzerland. According to our results, more than 60% of the known N. pumila populations went extinct, and the species currently presents 37 natural populations in the investigated area. A large number of populations were affected by eutrophication (69%) and hybridization with N. lutea (53%). Priority should be given to the in situ conservation of genetically pure populations, while ex situ cultures should be applied to nearly extinct populations and the genetically pure individuals still present in hybrid populations. N. pumila is an excellent representative of the wetland/aquatic glacial relicts that are particularly affected by the combination of climate change and habitat degradation. International integration of research and conservation programs is needed to limit the decline of such rare species in the Alps.

Supplementary information of paper

Plants protect themselves against herbivore attacks through a myriad of physical structures and toxic secondary metabolites. Together with abiotic factors, herbivores are expected to modulate plant defence strategies within plant assemblages. Because the abundance of insect herbivore decreases in colder environments, the palatability of plants in communities at higher elevation should shift in response to both abiotic and biotic factors.We inventoried grasshopper communities to document changes in herbivore abundance along elevation gradients and quantified associated shifts in plant palatability. We measured plant palatability by measuring the growth of Spodoptera littoralis generalist caterpillars fed with the leaves of 172 plant species. We related plant palatability to leaf traits and elevation at the species and community levels.In congruence with the decrease in grasshopper abundance with elevation, we found that the mean palatability level of plant communities increases with elevation. In addition, plant palatability was negatively associated with the community-weighted mean of leaf dry matter content. At the species level, plants with high carbon-to-nitrogen ratio were less palatable, while we found no effect of species mean elevation on plant palatability.Synthesis. Our results suggest that plant communities at higher elevation are composed of species that are generally more palatable for insect herbivores. Shift in plant palatability with elevation may thus be the outcome of a relaxation of the in situ herbivore pressure and changes in abiotic conditions.

Field studies and conceptual work on hybridization-mediated extinction risk in climate relicts are extremely rare. Nuphar pumila (Nymphaeaceae) is one of the most emblematic climate relicts in Europe with few isolated populations in the Alpine arc. The extent of introgression with related lowland and generalist species Nupharlutea has never been studied using molecular methods. All biogeographical regions where N.pumila naturally occurs in the neighbourhood of the Alpine arc were sampled and studied using nuclear microsatellite markers. Furthermore, we used forward-in-time simulations and Approximate Bayesian Computation to check whether an introgression scenario fits with the observed admixture patterns and estimated the demographic parameters associated with this process. Our study confirms ongoing hybridization between N.pumila and N.lutea and validates it by the use of population models. More than 40 % of investigated N.pumila individuals were admixed and hybrids were found in over 60 % of studied populations. The introgression is bidirectional and is most likely a result of very recent gene flow. Our work provides strong evidence for rapid extinction risk and demographic swamping between specialized climatic relicts and closely related generalists. The remaining pure populations of N.pumila are rare in the Alpine arc and deserve high conservation priority.

Traits that mediate species interactions are evolutionarily shaped by biotic and abiotic drivers, yet we know relatively little about the relative importance of these factors. Herbivore pressure, along with resource availability and ‘third-party’ mutualists, are hypothesized to play a major role in the evolution of plant defence traits. Here, we used the model system Plantago lanceolata, which grows along steep elevation gradients in the Swiss Alps, to investigate the effect of elevation, herbivore pressure, mycorrhizal inoculation and temperature on plant resistance. Over a 1200 m elevation gradient, the levels of herbivory and iridoid glycosides (IGs) declined with increasing elevation. By planting seedlings at three different elevations, we further showed that both low-elevation growing conditions and mycorrhizal inoculation resulted in increased plant resistance to herbivores. Finally, using a temperature-controlled experiment comparing high- and low-elevation ecotypes, we showed that high-elevation ecotypes are less resistant to herbivory, and that lower temperatures impair IGs deployment after herbivore attack. We thus propose that both lower herbivore pressure, and colder temperatures relax the defense syndrome of high elevation plants.