RESUMEN
Introgression is an important source of genetic variation that can determine species adaptation to environmental conditions. Yet, definitive evidence of the genomic and adaptive implications of introgression in nature remains scarce. The widespread hybrid zones of Darwin's primroses (Primula elatior, Primula veris, and Primula vulgaris) provide a unique natural laboratory for studying introgression in flowering plants and the varying permeability of species boundaries. Through analysis of 650 genomes, we provide evidence of an introgressed genomic region likely to confer adaptive advantage in conditions of soil toxicity. We also document unequivocal evidence of chloroplast introgression, an important precursor to species-wide chloroplast capture. Finally, we provide the first evidence that the S-locus supergene, which controls heterostyly in primroses, does not introgress in this clade. Our results contribute novel insights into the adaptive role of introgression and demonstrate the importance of extensive genomic and geographical sampling for illuminating the complex nature of species boundaries.
Asunto(s)
Magnoliopsida , Primula , Primula/genética , Genoma , Genómica , Magnoliopsida/genética , Cromosomas , Hibridación GenéticaRESUMEN
Medicinal plants and their bioactive molecules are integral components of nature and have supported the health of human societies for millennia. However, the prevailing view of medicinal biodiversity solely as an ecosystem-decoupled natural resource of commercial value prevents people from fully benefiting from the capacity of nature to provide medicines and from assessing the vulnerability of this capacity to the global environmental crisis. Emerging scientific and technological developments and traditional knowledge allow for appreciating medicinal plant resources from a planetary health perspective. In this Personal View, we highlight and integrate current knowledge that includes medicinal, biodiversity, and environmental change research in a transdisciplinary framework to evaluate natural medicinal resources and their vulnerability in the anthropocene. With Europe as an application case, we propose proxy spatial indicators for establishing the capacity, potential societal benefits, and economic values of native medicinal plant resources and the exposure of these resources to global environmental change. The proposed framework and indicators aim to be a basis for transdisciplinary research on medicinal biodiversity and could guide decisions in addressing crucial multiple Sustainable Development Goals, from accessible global health care to natural habitat protection and restoration.
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Ecosistema , Plantas Medicinales , Humanos , Conservación de los Recursos Naturales , Biodiversidad , Recursos NaturalesRESUMEN
Biodiversity hotspots, such as the Caucasus mountains, provide unprecedented opportunities for understanding the evolutionary processes that shape species diversity and richness. Therefore, we investigated the evolution of Primula sect. Primula, a clade with a high degree of endemism in the Caucasus. We performed phylogenetic and network analyses of whole-genome resequencing data from the entire nuclear genome, the entire chloroplast genome, and the entire heterostyly supergene. The different characteristics of the genomic partitions and the resulting phylogenetic incongruences enabled us to disentangle evolutionary histories resulting from tokogenetic vs cladogenetic processes. We provide the first phylogeny inferred from the heterostyly supergene that includes all species of Primula sect. Primula. Our results identified recurrent admixture at deep nodes between lineages in the Caucasus as the cause of non-monophyly in Primula. Biogeographic analyses support the 'out-of-the-Caucasus' hypothesis, emphasizing the importance of this hotspot as a cradle for biodiversity. Our findings provide novel insights into causal processes of phylogenetic discordance, demonstrating that genome-wide analyses from partitions with contrasting genetic characteristics and broad geographic sampling are crucial for disentangling the diversification of species-rich clades in biodiversity hotspots.
Asunto(s)
Primula , Filogenia , Primula/genética , Estudio de Asociación del Genoma Completo , Biodiversidad , Especiación GenéticaRESUMEN
The complex nature of species boundaries has been a central topic in evolutionary biology ever since Darwin. Despite numerous separate studies on reproductive isolation and hybridization, their relationship remains underinvestigated. Are the strengths and asymmetries of reproductive barriers reflected in the extent and directionalities of interspecific genetic exchange? We combined field, experimental, and molecular data to quantify strengths and asymmetries of sympatric reproductive barriers and hybridization between florally heteromorphic primroses. We also assessed whether generalist pollinators discriminate between different floral cues and contribute to reproductive isolation, a long-debated topic. Sympatric reproductive isolation is high but incomplete, and most phenotypic intermediates are genetic F1 hybrids, whereas backcrosses are rare, revealing low interspecific gene flow. Species integrity rests on multiple barriers, but ethological isolation is among the strongest, demonstrating that even generalist pollinators crucially contribute to the maintenance of species boundaries. Furthermore, reproductive barriers are weaker for Primula veris and short-styled plants, results corroborated by molecular data. Thus, in florally heteromorphic systems, both species- and morph-dependent asymmetries affect permeability of species boundaries. Our study illustrates how the interactions between complex floral syndromes and pollinators shape species boundaries in unique, previously undescribed ways.
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Primula , Aislamiento Reproductivo , Evolución Biológica , Flores/genética , Hibridación Genética , Polinización , SimpatríaRESUMEN
Strategies for 21st-century environmental management and conservation under global change require a strong understanding of the biological mechanisms that mediate responses to climate- and human-driven change to successfully mitigate range contractions, extinctions, and the degradation of ecosystem services. Biodiversity responses to past rapid warming events can be followed in situ and over extended periods, using cross-disciplinary approaches that provide cost-effective and scalable information for species' conservation and the maintenance of resilient ecosystems in many bioregions. Beyond the intrinsic knowledge gain such integrative research will increasingly provide the context, tools, and relevant case studies to assist in mitigating climate-driven biodiversity losses in the 21st century and beyond.
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Biodiversidad , Cambio Climático/historia , Conservación de los Recursos Naturales , Extinción Biológica , Animales , Archivos , Historia Antigua , PaleontologíaRESUMEN
Knowledge of global patterns of biodiversity, ranging from intraspecific genetic diversity (GD) to taxonomic and phylogenetic diversity, is essential for identifying and conserving the processes that shape the distribution of life. Yet, global patterns of GD and its drivers remain elusive. Here we assess existing biodiversity theories to explain and predict the global distribution of GD in terrestrial mammal assemblages. We find a strong positive covariation between GD and interspecific diversity, with evolutionary time, reflected in phylogenetic diversity, being the best predictor of GD. Moreover, we reveal the negative effect of past rapid climate change and the positive effect of inter-annual precipitation variability in shaping GD. Our models, explaining almost half of the variation in GD globally, uncover the importance of deep evolutionary history and past climate stability in accumulating and maintaining intraspecific diversity, and constitute a crucial step towards reducing the Wallacean shortfall for an important dimension of biodiversity.
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Evolución Biológica , Cambio Climático , Variación Genética , Mamíferos/genética , Animales , Ecosistema , Mamíferos/clasificación , FilogeniaRESUMEN
The Mediterranean realm, comprising the Mediterranean and Macaronesian regions, has long been recognized as one of the world's biodiversity hotspots, owing to its remarkable species richness and endemism. Several hypotheses on biotic and abiotic drivers of species diversification in the region have been often proposed but rarely tested in an explicit phylogenetic framework. Here, we investigate the impact of both species-intrinsic and -extrinsic factors on diversification in the species-rich, cosmopolitan Limonium, an angiosperm genus with center of diversity in the Mediterranean. First, we infer and time-calibrate the largest Limonium phylogeny to date. We then estimate ancestral ranges and diversification dynamics at both global and regional scales. At the global scale, we test whether the identified shifts in diversification rates are linked to specific geological and/or climatic events in the Mediterranean area and/or asexual reproduction (apomixis). Our results support a late Paleogene origin in the proto-Mediterranean area for Limonium, followed by extensive in situ diversification in the Mediterranean region during the late Miocene, Pliocene, and Pleistocene. We found significant increases of diversification rates in the "Mediterranean lineage" associated with the Messinian Salinity Crisis, onset of Mediterranean climate, Plio-Pleistocene sea-level fluctuations, and apomixis. Additionally, the Euro-Mediterranean area acted as the major source of species dispersals to the surrounding areas. At the regional scale, we infer the biogeographic origins of insular endemics in the oceanic archipelagos of Macaronesia, and test whether woodiness in the Canarian Nobiles clade is a derived trait linked to insular life and a biotic driver of diversification. We find that Limonium species diversity on the Canary Islands and Cape Verde archipelagos is the product of multiple colonization events followed by in situ diversification, and that woodiness of the Canarian endemics is indeed a derived trait but is not associated with a significant shift to higher diversification rates. Our study expands knowledge on how the interaction between abiotic and biotic drivers shape the uneven distribution of species diversity across taxonomic and geographical scales.
RESUMEN
Plumbaginaceae is characterized by a history of multiple taxonomic rearrangements and lacks a broad molecular phylogenetic framework. Limonium is the most species-rich genus of the family with ca. 600 species and cosmopolitan distribution. Its center of diversity is the Mediterranean region, where ca. 70% of all Limonium species are endemic. In this study, we sample 201 Limonium species covering all described infrageneric entities and spanning its wide geographic range, along with 64 species of other Plumbaginaceae genera, representing 23 out of 29 genera of the family. Additionally, 20 species of the sister family Polygonaceae were used as outgroup. Sequences of three chloroplast (trnL-F, matK, and rbcL) and one nuclear (ITS) loci were used to infer the molecular phylogeny employing maximum likelihood and Bayesian analyses. According to our results, within Plumbaginoideae, Plumbago forms a non-monophyletic assemblage, with Plumbago europaea sister to Plumbagella, while the other Plumbago species form a clade sister to Dyerophytum. Within Limonioideae, Ikonnikovia is nested in Goniolimon, rejecting its former segregation as genus distinct from Goniolimon. Limonium is divided into two major clades: Limonium subg. Pteroclados s.l., including L. sect. Pteroclados and L. anthericoides, and L. subg. Limonium. The latter is divided into three well-supported subclades: the monospecific L. sect. Limoniodendron sister to a clade comprising a mostly non-Mediterranean subclade and a Mediterranean subclade. Our results set the foundation for taxonomic proposals on sections and subsections of Limonium, namely: (a) the newly described L. sect. Tenuiramosum, created to assign L. anthericoides at the sectional rank; (b) the more restricted circumscriptions of L. sect. Limonium (= L. sect. Limonium subsect. Genuinae) and L. sect. Sarcophyllum (for the Sudano-Zambezian/Saharo-Arabian clade); (c) the more expanded circumscription of L. sect. Nephrophyllum (including species of the L. bellidifolium complex); and (d) the new combinations for L. sect. Pruinosum and L. sect. Pteroclados subsect. Odontolepideae and subsect. Nobiles.
RESUMEN
Understanding the effects of past climatic fluctuations on the distribution and population-size dynamics of cold-adapted species is essential for predicting their responses to ongoing global climate change. In spite of the heterogeneity of cold-adapted species, two main contrasting hypotheses have been proposed to explain their responses to Late Quaternary glacial cycles, namely, the interglacial contraction versus the interglacial expansion hypotheses. Here, we use the cold-adapted plant Primula farinosa to test two demographic models under each of the two alternative hypotheses and a fifth, null model. We first approximate the time and extent of demographic contractions and expansions during the Late Quaternary by projecting species distribution models across the last 72 ka. We also generate genome-wide sequence data using a Reduced Representation Library approach to reconstruct the spatial structure, genetic diversity, and phylogenetic relationships of lineages within P. farinosa. Finally, by integrating the results of climatic and genomic analyses in an Approximate Bayesian Computation framework, we propose the most likely model for the extent and direction of population-size changes in $P$. farinosa through the Late Quaternary. Our results support the interglacial expansion of $P$. farinosa, differing from the prevailing paradigm that the observed distribution of cold-adapted species currently fragmented in high altitude and latitude regions reflects the consequences of postglacial contraction processes.
Asunto(s)
Adaptación Fisiológica/fisiología , Clima , Frío , Variación Genética , Cubierta de Hielo , Filogenia , Primula/genética , Teorema de Bayes , Genoma de Planta/genética , Primula/fisiologíaRESUMEN
Ongoing rapid climate change is predicted to cause local extinction of plant species in mountain regions. However, some plant species could have persisted during Quaternary climate oscillations without shifting their range, despite the limited evidence from fossils. Here, we tested two candidate mechanisms of persistence by comparing the macrorefugia and microrefugia (MR) hypotheses. We used the rare and endemic Saxifraga florulenta as a model taxon and combined ensembles of species distribution models (SDMs) with a high-resolution paleoclimatic and topographic dataset to reconstruct its potential current and past distribution since the last glacial maximum. To test the macrorefugia hypothesis, we verified whether the species could have persisted in or shifted to geographic areas defined by its realized niche. We then identified potential MR based on climatic and topographic properties of the landscape and applied refined scenarios of MR dynamics and functions over time. Last, we quantified the number of known occurrences that could be explained by either the macrorefugia or MR model. A consensus of two or three SDM techniques predicted absence between 14-10, 3-4 and 1 ka bp, which did not support the macrorefugia model. In contrast, we showed that S. florulenta could have contracted into MR during periods of absence predicted by the SDMs and later re-colonized suitable areas according to the macrorefugia model. Assuming a limited and realistic seed dispersal distance for our species, we explained a large number of the current occurrences (61-96%). Additionally, we showed that MR could have facilitated range expansions or shifts of S. florulenta. Finally, we found that the most recent and the most stable MR were the ones closest to current occurrences. Hence, we propose a novel paradigm to explain plant persistence by highlighting the importance of supporting functions of MR when forecasting the fate of plant species under climate change.
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Ecosistema , Dispersión de las Plantas , Saxifragaceae/fisiología , Altitud , Cambio Climático , Francia , Italia , Modelos BiológicosRESUMEN
The plant family Labiatae (Lamiaceae) is known for its fine medicinal and aromatic herbs like lavender, mint, oregano, sage and thyme and is a rich source of essential oils for the food, pharmaceutical and cosmetic industry. Besides its great economic importance, the Labiatae family contributes significantly to the endemic flora of Greece and Turkey. Owing to its economic and biological significance and to the difficult identification based on morphological characters of several of its taxa, the Labiatae family is an ideal case for developing DNA barcodes. The purpose of this study is to evaluate the utility of DNA barcoding on a local scale in discriminating Labiatae species in Chios Island (Greece) and the adjacent Çesme-Karaburun Peninsula (Turkey). We chose three cpDNA regions (matK, rbcL, trnH-psbA) that were proposed by previous studies and tested them either as single region or as multiregion barcodes based on the criteria determined by Consortium for the Barcode of Life (CBOL). Our results show that matK and trnH-psbA taken as useful in discriminating species of the Labiatae, for the species we examined, as any multiregion combination. matK and trnH-psbA could serve as single-region barcodes for Labiatae species contributing to the conservation and the trade control of valuable plant resources.