Oligocene niche shift, Miocene diversification – cold tolerance and accelerated speciation rates in the St. John’s Worts (Hypericum, Hypericaceae)

Background: Our aim is to understand the evolution of species-rich plant groups that shifted from tropical into cold/temperate biomes. It is well known that climate affects evolutionary processes, such as how fast species diversify, species range shifts, and species distributions. Many plant lineages may have gone extinct in the Northern Hemisphere due to Late Eocene climate cooling, while some tropical lineages may have adapted to temperate conditions and radiated; the hyper-diverse and geographically widespread genus Hypericum is one of these. Results: To investigate the effect of macroecological niche shifts on evolutionary success we combine historical biogeography with analyses of diversification dynamics and climatic niche shifts in a phylogenetic framework. Hypericum evolved cold tolerance c. 30 million years ago, and successfully colonized all ice-free continents, where today ~500 species exist. The other members of Hypericaceae stayed in their tropical habitats and evolved into ~120 species. We identified a 15–20 million year lag between the initial change in temperature preference in Hypericum and subsequent diversification rate shifts in the Miocene. Conclusions: Contrary to the dramatic niche shift early in the evolution of Hypericum most extant species occur in temperate climates including high elevations in the tropics. These cold/temperate niches are a distinctive characteristic of Hypericum. We conclude that the initial release from an evolutionary constraint (from tropical to temperate climates) is an important novelty in Hypericum. However, the initial shift in the adaptive landscape into colder climates appears to be a precondition, and may not be directly related to increased diversification rates. Instead, subsequent events of mountain formation and further climate cooling may better explain distribution patterns and species-richness in Hypericum. These findings exemplify important macroevolutionary patterns of plant diversification during large-scale global climate change

Phylogenetic relationships in the southern African genus Drosanthemum (Ruschioideae, Aizoaceae)

Background. Drosanthemum, the only genus of the tribe Drosanthemeae, is widespread over the Greater Cape Floristic Region in southern Africa. With 114 recognized species, Drosanthemum together with the highly succulent and species-rich tribe Ruschieae constitute the 'core ruschioids' in Aizoaceae. Within Drosanthemum, nine subgenera have been described based on flower and fruit morphology. Their phylogenetic relationships, however, have not yet been investigated, hampering understanding of monophyletic entities and patterns of geographic distribution. Methods. Using chloroplast and nuclear DNA sequence data, we performed network- and tree-based phylogenetic analyses of 73 species of Drosanthemum with multiple accessions for widespread species. A well-curated, geo-referenced occurrence data set comprising the 134 genetically analysed and 863 further accessions was used to describe the distributional ranges of intrageneric lineages and the genus as a whole. Results. Phylogenetic inference supports nine clades within Drosanthemum, seven of which group in two major clades, while the remaining two show ambiguous affinities. The nine clades are generally congruent to previously described subgenera within Drosanthemum, with exceptions such as (pseudo-) cryptic species. In-depth analyses of sequence patterns in each gene region were used to reveal phylogenetic affinities inside the retrieved clades in more detail. We observe a complex distribution pattern including widespread, species-rich clades expanding into arid habitats of the interior (subgenera Drosanthemum p.p., Vespertina, Xamera) that are genetically and morphologically diverse. In contrast, less species-rich, genetically less divergent, and morphologically unique lineages are restricted to the central Cape region and more mesic conditions (Decidua, Necopina, Ossicula, Quastea, Quadrata, Speciosa). Our results suggest that the main lineages arose from an initial rapid radiation, with subsequent diversification in some clades.Raw data, code, analysis output, and species occurrence The zip file contains a ReadMe file and 4 folders: 1_main_data_and_results (the files used to produce the figures in the main text); 2_ML_phylogenetics (raw data, code, and analysis output of ML phylogenetic analyses); 3_MJ_networks (raw data [SNP/sequence motive recoded DNA alignment matrices], and output of median-joining network analyses)

Potent Antifungal Properties of Dimeric Acylphloroglucinols from Hypericum mexicanum and Mechanism of Action of a Highly Active 3′Prenyl Uliginosin B

9openInternationalBothThe success of antifungal therapies is often hindered by the limited number of available drugs. To close the gap in the antifungal pipeline, the search of novel leads is of primary importance, and here the exploration of neglected plants has great promise for the discovery of new principles. Through bioassay-guided isolation, uliginosin B and five new dimeric acylphloroglucinols (uliginosins C-D, and 3′prenyl uliginosins B-D), besides cembrenoids, have been isolated from the lipophilic extract of Hypericum mexicanum. Their structures were elucidated by a combination of Liquid Chromatography - Mass Spectrometry LC-MS and Nuclear Magnetic Resonance (NMR) measurements. The compounds showed strong anti-Candida activity, also against fluconazole-resistant strains, with fungal growth inhibition properties at concentrations ranging from 3 to 32 µM, and reduced or absent cytotoxicity against human cell lines. A chemogenomic screen of 3′prenyl uliginosin B revealed target genes that are important for cell cycle regulation and cytoskeleton assembly in fungi. Taken together, our study suggests dimeric acylphloroglucinols as potential candidates for the development of alternative antifungal therapiesopenTocci, N.; Weil, T.; Perenzoni, D.; Moretto, M.; Nürk, N.; Madriñán, S.; Ferrazza, R.; Guella, G.; Mattivi, F.Tocci, N.; Weil, T.; Perenzoni, D.; Moretto, M.; Nürk, N.; Madriñán, S.; Ferrazza, R.; Guella, G.; Mattivi, F

Preventing species extinctions: A global conservation consortium for Erica

Societal Impact Statement Human-caused habitat destruction and transformation is resulting in a cascade of impacts to biological diversity, of which arguably the most fundamental is species extinctions. The Global Conservation Consortia (GCC) are a means to pool efforts and expertise across national boundaries and between disciplines in the attempt to prevent such losses in focal plant groups. GCC Erica coordinates an international response to extinction threats in one such group, the heaths, or heathers, of which hundreds of species are found only in South Africa's spectacularly diverse Cape Floristic Region. Summary Effectively combating the biodiversity crisis requires coordinated conservation efforts. Botanic Gardens Conservation International (BGCI) and numerous partners have established Global Conservation Consortia (GCC) to collaboratively develop and implement comprehensive conservation strategies for priority threatened plant groups. Through these networks, institutions with specialised collections and staff can leverage ongoing work to optimise impact for threatened plant species. The genus Erica poses a challenge similar in scale to that of the largest other GCC group, Rhododendron, but almost 700 of the around 800 known species of Erica are concentrated in a single biodiversity hotspot, the Cape Floristic Region (CFR) of South Africa. Many species are known to be threatened, suffering the immediate impacts of habitat destruction, invasive species, changes in natural fire regimes and climate change. Efforts to counter these threats face general challenges: disproportionate burden of in situ conservation falling on a minority of the community, limited knowledge of species-rich groups, shortfalls in assessing and monitoring threat, lack of resources for in situ and limitations of knowledge for ex situ conservation efforts and in communicating the value of biological diversity to a public who may never encounter it in the wild. GCC Erica brings together the world's Erica experts, conservationists and the botanical community, including botanic gardens, seed banks and organisations in Africa, Madagascar, Europe, the United States, Australia and beyond. We are collaboratively pooling our unique sets of skills and resources to address these challenges in working groups for conservation prioritisation, conservation in situ, horticulture, seed banking, systematic research and outreach.publishedVersio

Diversification in evolutionary arenas : Assessment and synthesis

Understanding how and why rates of evolutionary diversification vary is a central issue in evolutionary biology and ecology. The concept of adaptive radiation has attracted much interest, but is metaphorical and verbal in nature, making it difficult to quantitatively compare different evolutionary lineages or geographic regions. In addition, the causes of evolutionary stasis are relatively neglected. Here we review the central concepts in the evolutionary diversification literature and bring these together by proposing a general framework for estimating rates of diversification and quantifying their underlying dynamics, which can be applied across clades and regions and across spatial and temporal scales. Our framework describes the diversification rate (d) as a function of the abiotic environment (a), the biotic environment (b) and clade-specific phenotypes or traits (c); thus d~a,b,c. We refer to the four components (a-d) and their interactions collectively as the 'Evolutionary Arena'. We outline analytical approaches to this conceptual model that open up new avenues for research, and present a case study on conifers, for which we parameterise the general model. We also discuss three conceptual examples based on existing literature: the Lupinus radiation in the Andes in the context of emerging ecological opportunity and fluctuating fragmentation due to climatic oscillation; oceanic island radiations in the context of archipelago isolation and island formation and erosion; and biotically driven radiations of the Mediterranean orchid genus Ophrys. The results of the conifer case study are consistent with the long-standing scenario that large niches, lack of competition, and high-rates of niche evolution differentially promote diversification, but these results go further by quantifying the statistical interactions between variables representing these three drivers. The conceptual examples illustrate how using the synthetic Evolutionary Arena framework results in highlighting gaps in current knowledge, and thus help to identify future directions for research on evolutionary radiations. In this way, the Evolutionary Arena framework promotes a more general understanding of variation in evolutionary rates by making quantitative results comparable between case studies, thereby allowing new syntheses of evolutionary and ecological processes to emerge

Botaniske hager går sammen for å stanse utryddelsen av arter: Global Conservation Consortium for Erica (lyng)

Botanic gardens unite to prevent species extinctions: the Global Conservation Consortium for Erica. Michael Pirie et al. describe an international project to prevent extinctions of species of Erica, the heaths or heathers. The ‘Global Conservation Consortium for Erica’ is coordinated at the Bergen University Gardens under the umbrella of Botanic Gardens Conservation International (BGCI). The authors describe the challenges of understanding and protecting species rich plant groups where much of the diversity is concentrated in biodiversity hotspots. Around 700 Erica species are only found in South Africa’s Cape Floristic Region. They explain how GCC Erica will address those challenges, including through both ‘in situ’ and ‘ex situ’ conservation

Merkmalsevolution und historische Biogeography

1 Introduction 1.1 The genus Hypericum 1.1.1 Origin of the name, phytochemistry & economic importance 1.1.2 Biology of Hypericum 1.1.3 Distribution and biogeography 1.2 Objectives of this study 1.2.1 Phylogeny 1.2.2 Character evolution and ecology 1.2.3 Historical biogeography 1.2.4 Diversification 1.3 Methods 1.3.1 Phylogenetic inference 1.3.2 Character evolution 1.3.4 The molecular clock 1.3.5 Biogeography 1.3.6 Diversification rates 2 Cladistic analysis of morphological characters in Hypericum (Hypericaceae) 2.1 Introduction 2.2 Materials & methods 2.2.1 Character coding 2.2.2 Phylogenetic inference 2.3 Results 2.4 Discussion 2.4.1 Character coding 2.4.2 Phylogeny of Hypericaceae 2.4.3 Phylogenetic inference within Hypericum 2.4.4 Character evolution 2.4.5 Biogeography 2.5 Conclusions 3 Molecular phylogeny and character evolution in St. John’s wort (Hypericum) 3.1 Introduction 3.2 Materials & methods 3.2.1 Taxon sampling 3.2.2 Molecular methods 3.2.3 Phylogenetic inference 3.2.4 Character reconstruction 3.3 Results 3.4 Discussion 3.4.1 Phylogeny of Hypericaceae 3.4.2 Character evolution 3.4.3 Phylogeny and classification 3.5 Conclusions 4 Out of the tropics? Historical biogeography of the temperate genus Hypericum 4.1 Introduction 4.2 Methods 4.2.1 Divergence time estimations 4.2.2 Diversification rates 4.2.3 Biogeographic analyses 4.3 Results & discussion 4.3.1 Age estimations 4.3.2 Ancestral area reconstructions: model comparison 4.3.3 Historical biogeography 4.3.4 Diversification rate shifts 4.4 Conclusions 5 Synthesis 5.1 Phylogeny and biogeography 5.2 Character evolution 5.3 Nuclear rDNA internal transcribed spacer, hybridization and concerted evolution 5.4 Evolutionary scenario of Hypericum s. l. Abstract References Acknowledgements Abbreviations Figures & Tables Appendix S1 Active compounds S1.1 Description of Hypericum S1.2 Species taxonomy S2 orphological phylogeny S2.2 Morphological character coding S3.1 Voucher: ITS sequences, direct and cloned S3.2 Character coding for ancestral character reconstructions by Bayesian MCMC optimization on the ITS phylogeny S4 Historical biogeography and diversification rate shift analyses CV & PublicationsSt. John’s wort (Hypericum, Hypericaceae) is a cosmopolitan genus with almost 500 species, including the medically used, facultative apomictic species H. perforatum. It is one of the few large plant genera for which an almost complete alpha taxonomy and classification is available. Hypericum is a temperate plant genus belonging to the clusioid clade of the Malpighiales that otherwise consists of tropical flora elements. In this dissertation, new insights into the evolutionary history of the genus Hypericum are provided. I investigate mechanisms that might have contributed to the observed species richness within this flowering plant group. To infer phylogenetic relationships within Hypericum and related taxa, I used morphological data and nuclear ribosomal DNA internal transcribed spacer (ITS) sequence information. A phylogenetic hypothesis had first to be formulated in order to position the analysis of evolution of the morphological and ecological characteristics, the reconstruction of historical biogeography, as well as the identification of diversification events into a testable framework, that is, into an explicit phylogenetic context. I coded 89 morphological characters for all (598) described taxa to conduct a formal cladistic analysis of the genus. For molecular phylogenetic inference, I used 366 sequences of the ITS region for 206 species representing Hypericum and five other genera of Hypericaceae. I analyzed the data with parsimony and model based methods to generate an explicit phylogenetic hypothesis of the genus. The results indicate that the small genera Lianthus, Triadenum, and Santomasia are nested within Hypericum, included in a clade containing most of the New World species. Sister to Hypericum is the small genus Thornea from Central America. Within Hypericum, three large clades and two smaller grades were found. Ancestral character state reconstructions yielded the recognition of characters, which support major clades within the genus. Shrubs represent the ancestral growth form from which herbs evolved several times. Sclerophylous treelets have radiated convergent in high elevation tropical habitats in Africa and the páramos of South America. To investigate the historical biogeography I conducted maximum likelihood analyses and compared the influence of different parametric models incorporating geological information. These analyses resulted in a revised biogeographic scenario for Hypericum and relatives. A cold adapted Hypericum s. l. lineage evolved with the emergence of temperate habitats on the Northern Hemisphere. This ancestral population was distributed across North America and West Eurasia (at this time the western Tethys region), and subsequently became disjunct and diversified independently in the New and the Old World. Since adaptation to cold climate conditions, species of this lineage stayed within temperate habitats (e. g., high mountains in the tropics). Together with this physiological shift, a significant increase in net diversification is correlated, resulting in eight times higher species richness within this temperate lineage of the Hypericaceae. Thus, the adaptation to cold climate conditions is a physiological key innovation triggering the increased evolutionary turnover in this temperate lineage. These results add to the growing evidence that phylogenetic niche conservatism is an important principle influencing biodiversity, especially during global climate changes.Johanniskraut (Hypericum, Hypericaceae) ist eine kosmopolitische Gattung, die annähernd 500 Arten beinhaltet, darunter die medizinisch verwendete, fakultativ apomiktische H. perforatum. Hypericum ist eine der wenigen großen Gattungen, für welche eine umfassende Taxonomie vorhanden ist. Die Arten kommen vor allem in gemäßigten Zonen vor. Die Gattung gehört phylogenetisch in den Clusioid Klade der Malpighiales, welche ansonsten Arten der tropischen Flora enthält. In dieser Arbeit gebe ich neue Einblicke in die Phylogenese der Gattung Hypericum. Weiterhin untersuche ich Gründe, welche zu dem beschriebenen Artenreichtum in dieser Gattung beigetragen haben können. Morphologische Daten und DNA Sequenzen der internal transcribed spacer (ITS) Region wurden verwendet, um die Verwandtschaftsbeziehungen innerhalb von Hypericum zu untersuchen. Eine phylogenetische Hypothese muss formuliert werden, um die Evolution von morphologischen und ökologischen Besonderheiten, die Rekonstruktion der historischen Biogeographie, sowie die Identifizierung von Diversifizierungs-Ereignissen in eine überprüfbare Rahmenbedingung stellen zu können, das heißt in einen klaren phylogenetischen Zusammenhang. Ich habe für alle (598) beschriebenen Taxa 89 morphologische Merkmale codiert und eine kladistische Analyse für die Gattung durchgeführt. Die molekular- phylogenetischen Analysen basieren auf 366 Sequenzen der ITS Region für 206 Hypericum Arten und Vertreter von fünf weiteren Gattungen der Hypericaceae. Die Daten wurden mithilfe von Parsimonie und modellbasierten Methoden analysiert, um eine Phylogenie der Gattung zu generieren. Die Ergebnisse zeigen, dass die Gattungen Lianthus, Triadenum und Santomasia phylogenetisch Hypericum zugeordnet sind. Die Schwestergruppe zu diesem Klade ist die kleine Gattung Thornea aus Mittelamerika. Innerhalb von Hypericum s. l. wurden drei große monophyletische Gruppen und mehrere kleinere, sukzessiv abzweigende Linien identifiziert. Durch die Rekonstruktion von Merkmalszuständen innerhalb der Gattung lassen sich über morphologische Merkmale die großen Gruppen unterstützen. Die Stammart von Hypericum s. l. waren Sträucher. Kräuter entwickelten sich mehrmals konvergent innerhalb der Gattung. Ein baumartiger Habitus hat sich unabhängig in tropischalpinen Lebensräumen in Afrika und in Südamerika entwickelt. Die historische Biogeographie wurde über ML basierte Analysen rekonstruiert. Dabei wurde der Einfluss verschiedener parametrischer Modelle verglichen. Die Ergebnisse führten zu einem revidierten biogeographischen Szenario für Hypericum und seine Verwandten. Eine kalt- adaptierte Hypericum s. l. Linie entwickelte sich mit der Entstehung gemäßigter Lebensräume in der Nordhemisphäre. Aufgrund der Adaptation an kalte Klimate konnten sich die Arten/Individuen dieser Linie in gemäßigten Lebensräumen über die gesamte Erde ausbreiten. Ein signifikanter Anstieg in Artbildungsraten korreliert mit dieser physiologischen Veränderung, was zu einen achtmal größerem Artenreichtum in dieser gemäßigten Linie der Hypericaceae führt. Das heißt, die Anpassung an gemäßigte Klimabedingungen stellt eine wichtige physiologische Neuerung in der Evolution von Hypericum s. l. dar. Diese Resultate verdeutlichen die Bedeutung von Nischenstabilität als ein wichtiges Prinzip, das Biodiversität vor allem in Zeiten globaler Klimaveränderung beeinflusst

Island woodiness underpins accelerated disparification in plant radiations

The evolution of secondary (insular) woodiness and the rapid disparification of plant growth forms associated with island radiations show intriguing parallels between oceanic islands and tropical alpine sky islands. However, the evolutionary significance of these phenomena remains poorly understood and the focus of debate. We explore the evolutionary dynamics of species diversification and trait disparification across evolutionary radiations in contrasting island systems compared with their nonisland relatives. We estimate rates of species diversification, growth form evolution and phenotypic space saturation for the classical oceanic island plant radiations – the Hawaiian silverswords and Macaronesian Echium – and the well‐studied sky island radiations of Lupinus and Hypericum in the Andes. We show that secondary woodiness is associated with dispersal to islands and with accelerated rates of species diversification, accelerated disparification of plant growth forms and occupancy of greater phenotypic trait space for island clades than their nonisland relatives, on both oceanic and sky islands. We conclude that secondary woodiness is a prerequisite that could act as a key innovation, manifest as the potential to occupy greater trait space, for plant radiations on island systems in general, further emphasizing the importance of combinations of clade‐specific traits and ecological opportunities in driving adaptive radiations

Data from: Are the radiations of temperate lineages in tropical alpine ecosystems pre-adapted?

Aim: Tropical mountains around the world harbour an extraordinarily rich pool of plant species and are hotspots of biodiversity. Climatically, they can be zoned into montane climates at mid-altitudes and tropical alpine climates above the tree line. Around half of the tropical alpine species belong to plant lineages with a temperate ancestry, although these regions are often geographically distant. We test the hypothesis that these temperate lineages are pre-adapted to the tropical alpine climate. Location: New World, with a focus on tropical alpine Andes. Time period: Miocene to present. Major taxa studied: Flowering plants. Methods: We build multidimensional environmental models representing the full space of New World climates. We quantify the environmental similarity between the tropical alpine ecosystem and those of potential source areas, while correcting for regional differences by kernel density smoothers. Based on spatial observations of the genus Hypericum (St John's Wort), we quantify niche overlap and test for niche conservatism following intercontinental dispersal using density-weighted nonparametric tests. A dated species tree, biogeographical estimation, multi-optima Ornstein–Uhlenbeck models and model selection approaches are used to test for niche shifts during establishment in the tropical alpine Andes. Results: The tropical alpine ecosystem is isolated by its climate from adjacent regions and is climatically similar to temperate lowland biomes of both hemispheres. Niche conservatism is evident in the study group, except in the tropical alpine lineage that is characterized by niche expansion and shifts in temperature optima. Main conclusions: Our results reject the pre-adaptation hypothesis and instead suggest pronounced niche evolution during colonization of tropical alpine ecosystems. Establishment involved substantial niche shifts, mainly in temperature-related variables, and resulted in a tremendous proliferation of species in the newly invaded tropical alpine ecosystem