The European Alps are highly rich in species, but their future may be threatened by ongoing changes in human land use and climate. Here, we reconstructed vegetation, temperature, human impact and livestock over the past ~12,000 years from Lake Sulsseewli, based on sedimentary ancient plant and mammal DNA, pollen, spores, chironomids, and microcharcoal. We assembled a highly-complete local DNA reference library (PhyloAlps, 3923 plant taxa), and used this to obtain an exceptionally rich sedaDNA record of 366 plant taxa. Vegetation mainly responded to climate during the early Holocene, while human activity had an additional influence on vegetation from 6 ka onwards. Land-use shifted from episodic grazing during the Neolithic and Bronze Age to agropastoralism in the Middle Ages. Associated human deforestation allowed the coexistence of plant species typically found at different elevational belts, leading to levels of plant richness that characterise the current high diversity of this region. Our findings indicate a positive association between low intensity agropastoral activities and precipitation with the maintenance of the unique subalpine and alpine plant diversity of the European Alps.
There is still limited consensus on the evolutionary history of species-rich temperate alpine floras due to a lack of comparable and high-quality phylogenetic data covering multiple plant lineages. Here we reconstructed when and how European alpine plant lineages diversified, i.e., the tempo and drivers of speciation events. We performed full-plastome phylogenomics and used multi-clade comparative models applied to six representative angiosperm lineages that have diversified in European mountains (212 sampled species, 251 ingroup species total). Diversification rates remained surprisingly steady for most clades, even during the Pleistocene, with speciation events being mostly driven by geographic divergence and bedrock shifts. Interestingly, we inferred asymmetrical historical migration rates from siliceous to calcareous bedrocks, and from higher to lower elevations, likely due to repeated shrinkage and expansion of high elevation habitats during the Pleistocene. This may have buffered climate-related extinctions, but prevented speciation along elevation gradients as often documented for tropical alpine floras.
While soil ecosystems undergo important modifications due to global change, the effect of soil properties on plant distributions is still poorly understood. Plant growth is not only controlled by soil physico-chemistry but also by microbial activities through the decomposition of organic matter and the recycling of nutrients essential for plants. A growing body of evidence also suggests that plant functional traits modulate species' response to environmental gradients. However, no study has yet contrasted the importance of soil physico-chemistry, microbial activities and climate on plant species distributions, while accounting for how plant functional traits can influence speciesspecific responses. Using hierarchical effects in a multi-species distribution model, we investigate how four functional traits related to resource acquisition (plant height, leaf carbon to nitrogen ratio, leaf dry matter content and specific leaf area) modulate the response of 44 plant species to climatic variables, soil physico-chemical properties and microbial decomposition activity (i.e. exoenzymatic activities) in the French Alps. Our hierarchical trait-based model allowed to predict well 41 species according to the TSS statistic. In addition to climate, the combination of soil C/N, as a measure of organic matter quality, and exoenzymatic activity, as a measure of microbial decomposition activity, strongly improved predictions of plant distributions. Plant traits played an important role. In particular, species with conservative traits performed better under limiting nutrient conditions but were outcompeted by exploitative plants in more favorable environments. We demonstrate tight associations between microbial decomposition activity, plant functional traits associated to different resource acquisition strategies and plant distributions. This highlights the importance of plant-soil linkages for mountain plant distributions. These results are crucial for biodiversity modelling in a world where both climatic and soil systems are undergoing profound and rapid transformations.
Low-coverage whole genome shotgun sequencing (or genome skimming) has emerged as a cost-effective method for acquiring genomic data in nonmodel organisms. This method provides sequence information on chloroplast genome (cpDNA), mitochondrial genome (mtDNA) and nuclear ribosomal regions (rDNA), which are over-represented within cells. However, numerous bioinformatic challenges remain to accurately and rapidly obtain such data in organisms with complex genomic structures and rearrangements, in particular for mtDNA in plants or for cpDNA in some plant families. Here we introduce the pipeline ORTHOSKIM, which performs in silico capture of targeted sequences from genomic and transcriptomic libraries without assembling whole organelle genomes. ORTHOSKIM proceeds in three steps: (i) global sequence assembly, (ii) mapping against reference sequences and (iii) target sequence extraction; importantly it also includes a range of quality control tests. Different modes are implemented to capture both coding and noncoding regions of cpDNA, mtDNA and rDNA sequences, along with predefined nuclear sequences (e.g., ultraconserved elements) or collections of single-copy orthologue genes. Moreover, aligned DNA matrices are produced for phylogenetic reconstructions, by performing multiple alignments of the captured sequences. While ORTHOSKIM is suitable for any eukaryote, a case study is presented here, using 114 genome-skimming libraries and four RNA sequencing libraries obtained for two plant families, Primulaceae and Ericaceae, the latter being a well-known problematic family for cpDNA assemblies. ORTHOSKIM recovered with high success rates cpDNA, mtDNA and rDNA sequences, well suited to accurately infer evolutionary relationships within these families. ORTHOSKIM is released under a GPL-3 licence and is available at: https://github.com/cpouc hon/ORTHO SKIM.
Ranunculaceae comprise ca. 2,500 species (ca. 55 genera) that display a broad range of floral diversity, particularly at the level of the perianth. Petals, when present, are often referred to as “elaborate” because they have a complex morphology. In addition, the petals usually produce and store nectar, which gives them a crucial functional role in the interaction with pollinators. Its morphological diversity and species richness make this family a particularly suitable model group for studying the evolution of complex morphologies. Our aims are (1) to reconstruct the ancestral form of the petal and evolutionary stages at the scale of Ranunculaceae, (2) to test the hypothesis that there are morphogenetic regions on the petal that are common to all species and that interspecific morphological diversity may be due to differences in the relative proportions of these regions during development. We scored and analyzed traits (descriptors) that characterize in detail the complexity of mature petal morphology in 32 genera. Furthermore, we described petal development using high resolution X-Ray computed tomography (HRX-CT) in six species with contrasting petal forms (Ficaria verna, Helleborus orientalis, Staphisagria picta, Aconitum napellus, Nigella damascena, Aquilegia vulgaris). Ancestral state reconstruction was performed using a robust and dated phylogeny of the family, allowing us to produce new hypotheses for petal evolution in Ranunculaceae. Our results suggest a flat ancestral petal with a short claw for the entire family and for the ancestors of all tribes except Adonideae. The elaborate petals that are present in different lineages have evolved independently, and similar morphologies are the result of convergent evolution.
Within the huge diversity of genus Passiflora, series Laurifoliae constitutes a strikingly uniform group, widely distributed in neotropical rain forests, at low to moderate elevations. Given its morphological and ecological unity, Killip mentionned it as an «exceedingly difficult» group. The lack of clear morphological criteria has not helped in delimiting it, and the confusion has grown with the addition of new species and criteria. As a preliminary step in the study of diversity within series Laurifoliae, we re-examine its morphological delimitation, assessing how its current 29 species (including the highly similar P. pachyantha and P. killipiana) conform to 20 criteria from different authors. Three criteria (indumentum on vegetative parts, stipule glands, membranous limen) appear to be irrelevant, because they are either too variable or rarely recorded in the species descriptions. Using the 17 remaining ones, 24 typical species show very limited variations, five of them differing by only one criterion. Among them, we retain terete to angular stem, setaceous or linear stipules soon deciduous, petiolar glands in one pair, leaves oblong, neither peltate nor lobate, three glandular bract over 1 cm long and free, flowers pendent, with two campanulate outer series of filaments (most other series much reduced or aborted). Five species, P. guazumaefolia, P. kikiana, P. odontophylla, P. ischnoclada, and P. maliformis, differ by three to nine traits, not found in the typical representatives of the series, so they can be excluded from it. Passiflora kikiana should be classified into series Kermesinae. For the four other ones, a satisfactory solution implies a more global study, involving other series.
There is still limited consensus on the evolutionary history of the species-rich temperate alpine floras due to a lack of comparable and high-quality phylogenetic data covering multiple plant lineages. Here we reconstructed when and how European alpine plant lineages diversified, i.e., the tempo and drivers of speciation events. We performed full-plastome phylogenomics and used multi-clade comparative models applied to six representative angiosperm lineages that have diversified in the European mountains. The diversification rates remained surprisingly steady for most clades, even during Pleistocene glaciations, with speciation events being mostly driven by geographic divergence and bedrock shifts. Interestingly, we inferred asymmetrical historical migration rates from siliceous to calcareous bedrocks, and from higher to lower elevations, likely due to repeated shrinkage and expansion of high elevation habitats during the Pleistocene. This may have buffered climate-related extinctions, but prevented plant speciation along elevation gradients as are often documented for tropical alpine floras.
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