Impact of the climatic changes in the Pliocene-Pleistocene transition on Irano-Turanian species. The radiation of genus Jurinea (Compositae).

The Irano-Turanian region is one of the world's richest floristic regions and the centre of diversity for numerous xerophytic plant lineages. However, we still have limited knowledge on the timing of evolution and biogeographic history of its flora, and potential drivers of diversification remain underexplored. To fill this knowledge gap, we focus on the Eurasian genus Jurinea (ca. 200 species), one of the largest plant radiations that diversified in the region. We applied a macroevolutionary integrative approach to explicitly test diversification hypotheses and investigate the relative roles of geography vs. ecology and niche conservatism vs. niche lability in speciation processes. To do so, we gathered a sample comprising 77% of total genus richness and obtained data about (1) its phylogenetic history, recovering 502 nuclear loci sequences; (2) growth forms; (3) ecological niche, compiling data of 21 variables for more than 2500 occurrences; and (4) paleoclimatic conditions, to estimate climatic stability. Our results revealed that climate was a key factor in the evolutionary dynamics of Jurinea. The main diversification and biogeographic events that occurred during past climate changes, which led to colder and drier conditions, are the following: (1) the origin of the genus (10.7 Ma); (2) long-distance dispersals from the Iranian Plateau to adjacent regions (∼7-4 Ma); and (3) the diversification shift during Pliocene-Pleistocene Transition (ca. 3 Ma), when net diversification rate almost doubled. Our results supported the pre-adaptation hypothesis, i.e., the evolutionary success of Jurinea was linked to the retention of the ancestral niche adapted to aridity. Interestingly, the paleoclimatic analyses revealed that in the Iranian Plateau long-term climatic stability favoured old-lineage persistence, resulting in current high species richness of semi-arid and cold adapted clades; whereas moderate climate oscillations stimulated allopatric diversification in the lineages distributed in the Circumboreal region. In contrast, growth form lability and high niche disparity among closely related species in the Central Asian clade suggest adaptive radiation to mountain habitats. In sum, the radiation of Jurinea is the result of both adaptive and non-adaptive processes influenced by climatic, orogenic and ecological factors.

Climate Stability Index maps, a global high resolution cartography of climate stability from Pliocene to 2100.

Climate changes are top biodiversity shapers, both during the past and future. Mapping the most climatic stable and unstable zones on Earth could improve our understanding of biodiversity distribution and evolution. Here, we present a set of maps based on a global scale, high resolution (ca. 5 km) new Climate Stability Index (CSI). The CSI considers bioclimatic variables for two different time ranges: (1) from Pliocene (3.3 Ma) to the present (CSI-past map set), using 12 time periods of PaleoClim representing warm and cold cycles; and (2) from present to the year 2100 (CSI-future), using nine general circulation models of climate change of four periods available from WorldClim. We calculated standard deviation of the variables and selected an uncorrelated set for summing, normalizing and obtaining the CSI maps. Our approach is useful for fields such as biogeography, earth sciences, agriculture, or sociology. However, CSI is an index that can be re-calculated according to particular criteria and objectives (e.g. temperature variables); maps are, therefore, customizable to every user.

Centaurea Subsect. Phalolepis (Compositae, Cardueae): A Case Study of Mountain-Driven Allopatric Speciation in the Mediterranean Peninsulas.

Centaurea subsection Phalolepis has been thoroughly analyzed in previous studies using microsatellites in four centers of speciation: Anatolia, Greece, the Italian Peninsula and the Iberian Peninsula. Evidence suggests a correlation between taxon diversity and mountains. This group constituted a good case study for examining the mountain-geobiodiversity hypothesis (MGH), which explains the possible reasons for the many radiations occurring in mountains across the world. We combined all the datasets and carried out analyses of their genetic structure to confirm the species of subsect. Phalolepis are grouped according to a geographic pattern. We then checked whether climatic fluctuations favored the "species pump" hypothesis in the mountains by using the Climatic Stability Index (CSI). Finally, the relief of the terrain was tested against the rate of allopatric speciation by region by means of Terrain Ruggedness Index and environmental gradients through our new Climate Niche Breadth Index. Our results supported the MGH hypothesis and confirmed that the main triggers, namely altitudinal zonation, climatic oscillations and rugged terrain, must be present for the development of a radiation.

Global distribution patterns and niche modelling of the invasive Kalanchoe × houghtonii (Crassulaceae).

Invasive alien species are currently considered one of the main threats to global biodiversity. One of the most rapidly expanding invasive plants in recent times is Kalanchoe × houghtonii (Crassulaceae), an artificial hybrid created in the 1930s in the United States by experimental crossings between K. daigremontiana and K. tubiflora, two species endemic to Madagascar. Thanks to its large colonizing capacity (mainly derived from the production of asexual plantlets), K. × houghtonii soon escaped from cultivation and quickly spread in many parts of the world. However, its actual range is not well known due to the lack of a formal description until recent times (2006) and its strong morphological resemblance with one of its parentals (K. daigremontiana). The present study was aimed, in the first instance, to delimit the present distribution area of K. × houghtonii at the global scale by gathering and validating all its occurrences and to track its colonization history. Currently, K. × houghtonii can be found on all continents except Antarctica, although it did not reach a global distribution until the 2000s. Its potential distribution, estimated with MaxEnt modelling software, is mainly centered in subtropical regions, from 20° to 40° of both northern and southern latitudes, mostly in areas with a high anthropogenic activity. Unexpectedly, concomitant to a poleward migration, future niche models suggest a considerable reduction of its range by up to one-third compared to the present, which might be related with the Crassulaceaean Acid Metabolism (CAM) of K. × houghtonii. Further research may shed light as to whether a decrease in potential habitats constitutes a general pattern for Crassulaceae and CAM plants.

Incorporating differences between genetic diversity of trees and herbaceous plants in conservation strategies.

Reviews that summarize the genetic diversity of plant species in relation to their life history and ecological traits show that forest trees have more genetic diversity at population and species levels than annuals or herbaceous perennials. In addition, among-population genetic differentiation is significantly lower in trees than in most herbaceous perennials and annuals. Possible reasons for these differences between trees and herbaceous perennials and annuals have not been discussed critically. Several traits, such as high rates of outcrossing, long-distance pollen and seed dispersal, large effective population sizes (Ne ), arborescent stature, low population density, longevity, overlapping generations, and occurrence in late successional communities, may make trees less sensitive to genetic bottlenecks and more resistant to habitat fragmentation or climate change. We recommend that guidelines for genetic conservation strategies be designed differently for tree species versus other types of plant species. Because most tree species fit an LH scenario (low [L] genetic differentiation and high [H] genetic diversity), tree seeds could be sourced from a few populations distributed across the species' range. For the in situ conservation of trees, translocation is a viable option to increase Ne . In contrast, rare herbaceous understory species are frequently HL (high differentiation and low diversity) species. Under the HL scenario, seeds should be taken from many populations with high genetic diversity. In situ conservation efforts for herbaceous plants should focus on protecting habitats because the typically small populations of these species are vulnerable to the loss of genetic diversity. The robust allozyme genetic diversity databases could be used to develop conservation strategies for species lacking genetic information. As a case study of reforestation with several tree species in denuded areas on the Korean Peninsula, we recommend the selection of local genotypes as suitable sources to prevent adverse effects and to insure the successful restoration in the long term.

Incorporación de diferencias de diversidad genética entre árboles y plantas herbáceas en estrategias de conservación Resumen Las revisiones que resumen la diversidad genética de las plantas en relación con sus características ecológicas y biológicas muestran que los árboles forestales tienen más diversidad genética a nivel de población y de especie que las plantas anuales o las perennes herbáceas. Sumado a esto, la diferenciación genética entre poblaciones es significativamente más baja en los árboles que en la mayoría de las perennes herbáceas y las anuales. Hasta la fecha no se han discutido críticamente las posibles explicaciones de estas diferencias entre los árboles y las perennes herbáceas y las plantas anuales. Varias características, como las tasas altas de alogamia, la dispersión a gran distancia de polen y semillas, el gran tamaño de la población efectiva (Ne ), la estatura arbórea, la baja densidad poblacional, la longevidad, el solapamiento de generaciones y la presencia dentro de comunidades sucesionales tardías, pueden generar en los árboles una menor sensibilidad a los cuellos de botella genéticos y una mayor resistencia a la fragmentación del hábitat o al cambio climático. Recomendamos que las directrices para las estrategias de conservación genética estén diseñadas de manera diferente para las especies arbóreas que para otro tipo de plantas. Ya que la mayoría de las especies arbóreas encajan dentro de un escenario LH (baja [L] diferenciación genética y alta [H] diversidad genética), las semillas de los árboles podrían tomarse de unas cuantas poblaciones dispersas a lo largo del área de distribución de la especie. Por lo anterior, para la conservación in situ de los árboles, la translocación es una opción viable para incrementar la Ne . Al contrario de esta situación, las especies herbáceas raras del sotobosque con frecuencia son especies HL (alta diferenciación y baja diversidad). En el escenario HL, las semillas deberían ser recolectadas de muchas poblaciones con diversidad genética alta y los esfuerzos de conservación in situ para las plantas herbáceas deberían enfocarse en la protección del hábitat ya que las poblaciones típicamente pequeñas de estas especies son vulnerables a la pérdida de la diversidad genética. Las robustas bases de datos de diversidad genética aloenzimática podrían usarse para desarrollar estrategias de conservación para las especies que carecen de información genética. Como caso de estudio de reforestación con varias especies arbóreas en áreas deforestadas de la Península de Corea, recomendamos la selección de genotipos locales como fuente adecuada para prevenir los efectos adversos y para asegurar la restauración exitosa a largo plazo.

An empirical assessment of a single family-wide hybrid capture locus set at multiple evolutionary timescales in Asteraceae.

PREMISE: Hybrid capture with high-throughput sequencing (Hyb-Seq) is a powerful tool for evolutionary studies. The applicability of an Asteraceae family-specific Hyb-Seq probe set and the outcomes of different phylogenetic analyses are investigated here. METHODS: Hyb-Seq data from 112 Asteraceae samples were organized into groups at different taxonomic levels (tribe, genus, and species). For each group, data sets of non-paralogous loci were built and proportions of parsimony informative characters estimated. The impacts of analyzing alternative data sets, removing long branches, and type of analysis on tree resolution and inferred topologies were investigated in tribe Cichorieae. RESULTS: Alignments of the Asteraceae family-wide Hyb-Seq locus set were parsimony informative at all taxonomic levels. Levels of resolution and topologies inferred at shallower nodes differed depending on the locus data set and the type of analysis, and were affected by the presence of long branches. DISCUSSION: The approach used to build a Hyb-Seq locus data set influenced resolution and topologies inferred in phylogenetic analyses. Removal of long branches improved the reliability of topological inferences in maximum likelihood analyses. The Astereaceae Hyb-Seq probe set is applicable at multiple taxonomic depths, which demonstrates that probe sets do not necessarily need to be lineage-specific.

Climatic niche characteristics of native and invasive Lilium lancifolium.

One of the topics currently under discussion in biological invasions is whether the species' climatic niche has been conserved or, alternatively, has diverged during invasions. Here, we explore niche dynamic processes using the complex invasion history model of Lilium lancifolium, which is the first tested case of a native species (Korea) with two hypothesized spatial (regional and intercontinental) and temporal arrivals: (1) as an archaeophyte in East Asia (before AD 1500); and (2) as a neophyte in Europe, North America, Australia, and New Zealand (after AD 1500). Following a niche examination through both environmental and geographical spaces, the species in the archaeophyte range has apparently filled the ancestral native niche and, rather, would have increased it considerably. The species as a neophyte shows a closer climatic match with the archaeophyte range than with the native one. This pattern of niche similarity suggests that the neophyte range was probably colonized by a subset of archaeophyte propagules adapted to local climate that promoted the species' establishment. Overall, niche conservatism is proposed at each colonization step, from native to archaeophyte, and from archaeophyte to neophyte ranges. We detected signals of an advanced invasion stage within the archaeophyte range and traces of an early introduction stage in neophyte ranges.

Phylogeny, origin and dispersal of Saussurea (Asteraceae) based on chloroplast genome data.

Saussurea is one of the largest genera of the tribe Cardueae of Asteraceae, comprising about 460 species from the Northern Hemisphere with most species distributed in QTPss and adjacent areas. Here, we established a well-supported phylogenetic framework for Saussurea based on whole chloroplast genomes of 136 taxa plus 16 additional taxa of Cardueae using Bayesian inference and Maximum Likelihood. Our phylogenetic results are inconsistent with previous subgeneric classifications of Saussurea. We nearly completely delimited subgen. Eriocoryne, and found that subgen. Theodorea, subgen. Saussurea section Laguranthera and Rosulascentes are closely related to each other. Based on our phylogenetic results, we performed biogeographic analyses and inferred that the genus Saussurea arose during early-middle Miocene within the Hengduan Mountains. We expect that landscape heterogeneity within the QTPss and adjacent areas, such as the Hengduan Mountains, played an important role in the evolution of Saussurea. Following its evolutionary origin, the genus underwent rapid diversification in situs and dispersed northwards in several migrational patterns. Both continuous uplift of the QTPss and adjacent areas as well as global cooling since mid-Miocene probably led to geographic expansion and diffusion of Saussurea, with the latter, in particular, resulting in the northward dispersal.

Nuclear and plastid DNA phylogeny of tribe Cardueae (Compositae) with Hyb-Seq data: A new subtribal classification and a temporal diversification framework.

Classification of tribe Cardueae in natural subtribes has always been a challenge due to the lack of support of some critical branches in previous phylogenies based on traditional Sanger markers. With the aim to propose a new subtribal delimitation, we applied a Hyb-Seq approach to a set of 76 Cardueae species representing all subtribes and informal groups defined in the tribe, targeting 1061 nuclear conserved orthology loci (COS) designed for Compositae and obtaining chloroplast coding regions as by-product of off-target reads. For the extraction of the target nuclear data, we used two strategies, PHYLUCE and HybPiper, and 776 and 1055 COS loci were recovered with each of them, respectively. Additionally, 87 chloroplast genes were assembled and annotated. With three datasets, phylogenetic relationships were reconstructed using both concatenation and coalescent approaches. Phylogenetic analyses of the nuclear datasets fully resolved virtually all nodes with very high support. Nuclear and plastid tree topologies are mostly congruent with a very limited number of incongruent nodes. Based on the well-solved phylogenies obtained, we propose a new taxonomic scheme of 12 monophyletic and morphologically consistent subtribes: Carlininae, Cardopatiinae, Echinopsinae, Dipterocominae (new), Xerantheminae (new), Berardiinae (new), Staehelininae (new), Onopordinae (new), Carduinae (redelimited), Arctiinae (new), Saussureinae (new), and Centaureinae. In addition, we further updated the temporal framework for origin and diversification of these subtribes. Our results highlight the power of Hyb-Seq over Sanger sequencing of a few DNA markers in solving phylogenetic relationships of traditionally difficult groups.

Author Correction: Identifying long-term stable refugia for relict plant species in East Asia.

In the original version of this Article, an incorrect sample size was provided for the number of relict species (443 instead of 442) and the number of relict forests (423 instead of 422). These errors have been corrected in both the PDF and HTML versions of the Article.

Identifying long-term stable refugia for relict plant species in East Asia.

Today East Asia harbors many "relict" plant species whose ranges were much larger during the Paleogene-Neogene and earlier. The ecological and climatic conditions suitable for these relict species have not been identified. Here, we map the abundance and distribution patterns of relict species, showing high abundance in the humid subtropical/warm-temperate forest regions. We further use Ecological Niche Modeling to show that these patterns align with maps of climate refugia, and we predict species' chances of persistence given the future climatic changes expected for East Asia. By 2070, potentially suitable areas with high richness of relict species will decrease, although the areas as a whole will probably expand. We identify areas in southwestern China and northern Vietnam as long-term climatically stable refugia likely to preserve ancient lineages, highlighting areas that could be prioritized for conservation of such species.

Exploring data processing strategies in NGS target enrichment to disentangle radiations in the tribe Cardueae (Compositae).

Target enrichment is a cost-effective sequencing technique that holds promise for elucidating evolutionary relationships in fast-evolving lineages. However, potential biases and impact of bioinformatic sequence treatments in phylogenetic inference have not been thoroughly explored yet. Here, we investigate this issue with an ultimate goal to shed light into a highly diversified group of Compositae (Asteraceae) constituted by four main genera: Arctium, Cousinia, Saussurea, and Jurinea. Specifically, we compared sequence data extraction methods implemented in two easy-to-use workflows, PHYLUCE and HybPiper, and assessed the impact of two filtering practices intended to reduce phylogenetic noise. In addition, we compared two phylogenetic inference methods: (1) the concatenation approach, in which all loci were concatenated in a supermatrix; and (2) the coalescence approach, in which gene trees were produced independently and then used to construct a species tree under coalescence assumptions. Here we confirm the usefulness of the set of 1061 COS targets (a nuclear conserved orthology loci set developed for the Compositae) across a variety of taxonomic levels. Intergeneric relationships were completely resolved: there are two sister groups, Arctium-Cousinia and Saussurea-Jurinea, which are in agreement with a morphological hypothesis. Intrageneric relationships among species of Arctium, Cousinia, and Saussurea are also well defined. Conversely, conflicting species relationships remain for Jurinea. Methodological choices significantly affected phylogenies in terms of topology, branch length, and support. Across all analyses, the phylogeny obtained using HybPiper and the strictest scheme of removing fast-evolving sites was estimated as the optimal. Regarding methodological choices, we conclude that: (1) trees obtained under the coalescence approach are topologically more congruent between them than those inferred using the concatenation approach; (2) refining treatments only improved support values under the concatenation approach; and (3) branch support values are maximized when fast-evolving sites are removed in the concatenation approach, and when a higher number of loci is analyzed in the coalescence approach.

Comparison of genetic variation between northern and southern populations of Lilium cernuum (Liliaceae): Implications for Pleistocene refugia.

The so-called "Baekdudaegan" (BDDG), a mountain range that stretches along the Korean Peninsula, has been recently proposed as a major "southern" glacial refugium for boreal or temperate plant species based on palaeoecological and, especially, genetic data. Genetic studies comparing genetic variation between population occurring on the BDDG and more northern ones (i.e. in NE China and/or in Russian Far East) are, however, still too few to draw firm conclusions on the role of the BDDG as a refugium and a source for possible northward post-glacial recolonizations. In order to fill this gap, we selected a boreal/temperate herb, Lilium cernuum, and compared levels of allozyme-based genetic diversity of five populations from NE China with five populations from South Korea (home of its hypothesized refuge areas). As a complementary tool, we used the maximum entropy algorithm implemented in MaxEnt to infer the species' potential distribution for the present time, which was projected to different past climate scenarios for the Last Glacial Maximum (LGM). Permutation tests revealed that Korean populations harbored significantly higher levels of within-population genetic variation than those from NE China (expected heterozygosity = 0.173 vs. 0.095, respectively). Our results suggest that the lowered levels of genetic diversity in NE Chinese populations might be due to founder effects associated with post-glacial migration from southern regions. Congruent with genetic data, past distribution models showed higher probability of occurrence in southern ranges than in northern ones during the LGM. In addition, a positive correlation was detected between the expected heterozygosity and environmental LGM suitability. From a conservation perspective, our results further suggest that the southern populations in South Korea may be particularly worthy of protection.

Potential effects of climate change on geographic distribution of the Tertiary relict tree species Davidia involucrata in China.

This study, using species distribution modeling (involving a new approach that allows for uncertainty), predicts the distribution of climatically suitable areas prevailing during the mid-Holocene, the Last Glacial Maximum (LGM), and at present, and estimates the potential formation of new habitats in 2070 of the endangered and rare Tertiary relict tree Davidia involucrata Baill. The results regarding the mid-Holocene and the LGM demonstrate that south-central and southwestern China have been long-term stable refugia, and that the current distribution is limited to the prehistoric refugia. Given future distribution under six possible climate scenarios, only some parts of the current range of D. involucrata in the mid-high mountains of south-central and southwestern China would be maintained, while some shift west into higher mountains would occur. Our results show that the predicted suitable area offering high probability (0.5‒1) accounts for an average of only 29.2% among the models predicted for the future (2070), making D. involucrata highly vulnerable. We assess and propose priority protected areas in light of climate change. The information provided will also be relevant in planning conservation of other paleoendemic species having ecological traits and distribution ranges comparable to those of D. involucrata.