History and evolution of the afroalpine fora: in the footsteps of Olov Hedberg

The monumental work of Olov Hedberg provided deep insights into the spectacular and fragmented tropical alpine flora of the African sky islands. Here we review recent molecular and niche modelling studies and re-examine Hedberg’s hypotheses and conclusions. Colonisation started when mountain uplift established the harsh diurnal climate with nightly frosts, accelerated throughout the last 5 Myr (Plio-Pleistocene), and resulted in a flora rich in local endemics. Recruitment was dominated by long-distance dispersals (LDDs) from seasonally cold, remote areas, mainly in Eurasia. Colonisation was only rarely followed by substantial diversification. Instead, most of the larger genera and even species colonised the afroalpine habitat multiple times independently. Conspicuous parallel evolution occurred among mountains, e.g., of gigantism in Lobelia and Dendrosenecio and dwarf shrubs in Alchemilla. Although the alpine habitat was ~ 8 times larger and the treeline was ~ 1000 m lower than today during the Last Glacial Maximum, genetic data suggest that the flora was shaped by strong intermountain isolation interrupted by rare LDDs rather than ecological connectivity. The new evidence points to a much younger and more dynamic island scenario than envisioned by Hedberg: the afroalpine flora is unsaturated and fragile, it was repeatedly disrupted by the Pleistocene climate oscillations, and it harbours taxonomic and genetic diversity that is unique but severely depauperated by frequent bottlenecks and cycles of colonisation, extinction, and recolonisation. The level of intrapopulation genetic variation is alarmingly low, and many afroalpine species may be vulnerable to extinction because of climate warming and increasing human impact.publishedVersio

I Olov Hedbergs fotspor: Plantenes evolusjon i det afrikanske høyfjellet

Floraen i det tropiske afrikanske høyfjellet er spektakulær og rik på endemiske (stedegne) arter, og ikke minst er forekomstene av plantearter ekstremt fragmentert på grunn av lange avstander mellom de enkelte fjellene (fig. 1). Denne særegne floraen ble dyptpløyende analysert av Olov Hedberg i hans monumentale verk fra 1957 (Hedberg 1957) og i påfølgende arbeider (f.eks. Hedberg 1961, Hedberg 1969). Studier basert på molekylære data og nisjemodellering har senere gitt sterk støtte til flere av hans hypoteser, men også ledet til ny og overraskende innsikt. Plantenes innvandring til det afrikanske høyfjellet startet allerede da fjellhevingen skapte det spesielle tropisk-alpine døgnklimaet med frost hver natt og høye dagtemperaturer året rundt. Antallet arter økte deretter betydelig gjennom de siste 5 millioner år (plio-pleistocen) og faktisk helt fram til vår tid. En stor del av floraen oppstod etter langdistansespredning fra fjerne, kalde områder, hovedsakelig i Eurasia. Plantenes innvandring ble bare i noen få tilfeller fulgt av betydelig diversifisering (f.eks. hos marikåpe Alchemilla) – tvert imot har slekter som er artsrike i det afrikanske høyfjellet, ofte vist seg å ha spredt seg uavhengig dit gjentatte ganger (f.eks. starr Carex), noe til og med enkeltarter som vår egen fjellskrinneblom Arabis alpina har gjort. De nye studiene tyder på at den afrikanske høyfjellsfloraen har utvikletseg under et mye yngre og mer dynamisk øy-scenario enn det Hedberg så for seg: Den framstår som umettet og sårbar for framtidige klima- og arealendringer på grunn av katastrofale forstyrrelser under klimasvingningene gjennom de siste par millioner år. Den rommer artsmangfold og genetisk diversitet som er unikt, men sterkt svekket av genetiske «flaskehalser» og sykluser av innvandring, utdøing og gjeninnvandring. Det er usedvanlig lite genetisk variasjon i dagens populasjoner, noe som kan bety at mange arter står i fare for å dø ut på grunn av klimaoppvarming og økende menneskelig påvirkning

Repeatedly Northwards and Upwards: Southern African Grasslands Fuel the Colonization of the African Sky Islands in Helichrysum (Compositae)

The Afromontane and Afroalpine areas constitute some of the main biodiversity hotspots of Africa. They are particularly rich in plant endemics, but the biogeographic origins and evolutionary processes leading to this outstanding diversity are poorly understood. We performed phylogenomic and biogeographic analyses of one of the most species-rich plant genera in these mountains, Helichrysum (Compositae-Gnaphalieae). Most previous studies have focused on Afroalpine elements of Eurasian origin, and the southern African origin of Helichrysum provides an interesting counterexample. We obtained a comprehensive nuclear dataset from 304 species (≈50% of the genus) using target-enrichment with the Compositae1061 probe set. Summary-coalescent and concatenation approaches combined with paralog recovery yielded congruent, well-resolved phylogenies. Ancestral range estimations revealed that Helichrysum originated in arid southern Africa, whereas the southern African grasslands were the source of most lineages that dispersed within and outside Africa. Colonization of the tropical Afromontane and Afroalpine areas occurred repeatedly throughout the Miocene-Pliocene. This timing coincides with mountain uplift and the onset of glacial cycles, which together may have facilitated both speciation and intermountain gene flow, contributing to the evolution of the Afroalpine flora.This work received financial support from the Spanish Ministry of Science, Innovation and Universities (PID2019-105583GB-C22/AEI/10.13039/501100011033) and the Catalan government (“Ajuts a grups consolidats” 2021SGR00315 and FI grant to C.B.-G. 2022FI_B 00150). The Ph.D. thesis was carried out under the Ph.D. program “Plant Biology and Biotechnology” of the Autonomous University of Barcelona (UAB). Additional support was provided by the Czech Science Foundation GAČR project no. 20-10878S to R.S. and F.K. and long-term research development project (RVO 67985939) of the Czech Academy of Sciences. Additional funds were obtained from the Norwegian Programme for Development, Research and Higher Education (NUFU; project AFROALP-II, no 2007/1058) and the Research Council of Norway (project SpeciationClock, no 274607) to C.B.Abstract 1. Introduction 2. Materials and Methods 2.1. Taxon Sampling 2.2. DNA Extraction, Library Preparation, Target Capture, and Sequencing 2.3. Molecular Data Processing and Phylogenetic Analyses 2.4. Divergence Time Estimation 2.5. Ancestral Range Estimation 3. Results 3.1. Alignment Processing and Filtering 3.2. Phylogenetic Analyses 3.3. Divergence Time and Ancestral Range Estimation 3.4. Number, Type, and Directionality Estimation of Biogeographical Events 4. Discussion 4.1. Utility of Target-Enrichment Strategies in Reconstructing the Radiation of Helichrysum 4.2. The Early History of Helichrysum and Colonization of Madagascar 4.3. Repeatedly Northwards 4.4. Repeatedly Upwards 5. Conclusions Supplementary Materials Author Contributions Funding Data Availability Statement Acknowledgments Conflicts of Interest Reference

Center of origin and evolutionary history in the high Andean genus Oritrophium (Astereae, Asteraceae)

Páramo, the most species-rich tropical mountain ecosystem, is relatively well-researched in terms of the diversity and evolutionary sources of its flora, yet we know very little about the diversification within this environment. This study aims to unravel the evolutionary history of Oritrophium, an endemic genus of alpine habitats in North and South America, with a disjunct and bi-modal distribution of its species diversity. We aim to disentangle the center of origin and radiation of the genus, and mechanisms structuring its genetic diversity at inter- and intra-specific level. We sampled 19 species (85% from the total) and extended the sampling at population level for the two widely distributed species, O.limnophilum and O.peruvianum, comprising 19 and 24 populations, respectively. Using nuclear ribosomal internal transcribed spacer (ITS) and trnL-trnF chloroplast DNA region, we reconstructed dated phylogenies to test the monophyly of the genus and unravel possible historical forces underlying its diversification. We also performed an ancestral area estimation to reconstruct the biogeographic history of the genus. At the population level, we constructed haplotype networks and run spatial analyses of molecular variance to explore possible mechanisms that operate on structuring the diversity at intraspecific level. Oritrophium resulted polyphyletic, with two species being closely related to Erigeron and three other species ambiguously related to Erigeron, Diplostephium, Linochilus, and/or Hinterhubera. The remaining 14 species formed a clade, Oritrophiums.s., that likely originated during the Early Pliocene in the Andes of northwestern Bolivia to southern Ecuador, the center of the genus' diversity. The group likely diversified with the emergence of the Páramo during the Late Pliocene and further dispersed mainly from South-to-North in the Pleistocene. This migration involved both, long-distance dispersal from the Central Andes to Mexico and gradual migration of the species along the Andes. Accordingly, Oritrophium s.s. appears as the first record of a long-distance dispersal from the Páramo of South America to North America. The dispersal pattern within South America was mirrored by the intraspecific population diversity and structure of the investigated species.Fil: Salomón, Luciana. Karlova Univerzita (cuni); República ChecaFil: Nicola, Marcela Viviana. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Botánica Darwinion. Academia Nacional de Ciencias Exactas, Físicas y Naturales. Instituto de Botánica Darwinion; ArgentinaFil: Kandziora, Martha. Karlova Univerzita (cuni); República ChecaFil: Kolář, Filip. Karlova Univerzita (cuni); República Checa. Czech Academy of Sciences. Institute of Botany; República ChecaFil: Sklenář, Petr. Karlova Univerzita (cuni); República Chec

Phenomap - Challenges and Successes in Bringing Together Multiple Data Projects to Build New Visualizations of Phenotypic Information and Specimen Records

Connecting biodiversity data across databases is not as easy as one might think. Different databases use different identifiers and taxonomies and connecting these data often results in loss of information and precision. Here we present some of the challenges we faced with integrating multiple biodiversity data sets, including specimen data from the scientific collections, during a hackathon hosted by the Phenoscape project in December of 2017. The hackathon brought together a diverse group of participants, including biologists and software developers, to explore ways of using the computable phenotype data in the Phenoscape Knowledgebase (KB) (Edmunds et al. 2015). The KB contains ontology-annotated data that links evolutionary phenotypes from the comparative literature to model organism phenotypes enabling, e.g., the retrieval of candidate genes for evolutionary phenotypes and the generation of synthetic supermatrices of presence/absence characters. During this hackathon, our team explored how to link phenotype data in the KB to museum specimen data in iDigBio (Matsunaga et al. 2013) with the hope of creating visualizations including world maps showing species distributions with different character states and their phylogenetic relationships. We visualized lineage relationships by querying the Open Tree of Life (OT) (Hinchliff et al. 2015) website using data integrated by another group at the hackathon that linked KB and OT taxonomic identifiers. Phenoscape uses terms from anatomy, quality, and taxonomy ontologies to annotate characters and taxonomic information from the phylogenetic literature along with specimen information. When populating the KB, specimen identifiers such as occurrence identifiers, collector’s number, and catalog numbers were preserved if present in the literature. We found that these identifiers, although standard in the biodiversity domain, were mostly insufficient to uniquely identify the source specimen in iDigBio. As an alternative, we instead mapped all the occurrences of taxa using string matches of the genus and species from Vertebrate Taxonomy Ontology identifiers. Without specimen identifiers that are consistent across databases, we lost the ability to explore spatial and temporal variation of characters within genera and were only able to explore phenotypes and geographic distributions among genera. We look forward to discussing these issues with the collections community represented at this meeting by the Society for the Preservation of Natural History Collections (SPNHC). We developed an R Shiny application that integrates characters and taxa from Phenoscape with specimen records from iDigBio and phylogenies from OT, to visualize phenotypic characters and taxon distributions in three interactive panels. The app allows a user to visualize OT phylogenies and place presence/absence character data on the tree. Specifically, users can: select taxa or specific characters to visualize their geographic distributions, navigate a phylogeny browser which displays character and specimen data available for taxa under consideration, and view a heatmap of characters available for character and taxon combinations. Because of our challenges joining data, our distribution map leaves users with the impression that all individuals in a genus exhibit a character whereas the KB was populated with data describing individuals. We hope that with improved data standards and their use by more people, constructing applications like ours will become easier

The enigmatic tropical alpine flora on the African sky islands is young, disturbed, and unsaturated

Significance Resilience is required to withstand or mitigate the effect of human-induced climate change. Today whole ecosystems are affected by climate change, but our understanding of their evolution and natural response is limited, often restricted to individual populations or species. The enigmatic flora on the tops of the African sky islands is isolated and unique, showing striking adaptations to the harsh tropical alpine conditions. Here we analyze genome data from a large fraction of afroalpine plants and show that this remarkable flora has a dynamic history with frequent colonizations and extinctions, most likely caused by previous natural climate changes during the ice-age cycles. The flora will be particularly vulnerable to human-induced climate warming, reducing alpine habitat into successively smaller areas

History and evolution of the afroalpine fora: in the footsteps of Olov Hedberg

The monumental work of Olov Hedberg provided deep insights into the spectacular and fragmented tropical alpine flora of the African sky islands. Here we review recent molecular and niche modelling studies and re-examine Hedberg’s hypotheses and conclusions. Colonisation started when mountain uplift established the harsh diurnal climate with nightly frosts, accelerated throughout the last 5 Myr (Plio-Pleistocene), and resulted in a flora rich in local endemics. Recruitment was dominated by long-distance dispersals (LDDs) from seasonally cold, remote areas, mainly in Eurasia. Colonisation was only rarely followed by substantial diversification. Instead, most of the larger genera and even species colonised the afroalpine habitat multiple times independently. Conspicuous parallel evolution occurred among mountains, e.g., of gigantism in Lobelia and Dendrosenecio and dwarf shrubs in Alchemilla. Although the alpine habitat was ~ 8 times larger and the treeline was ~ 1000 m lower than today during the Last Glacial Maximum, genetic data suggest that the flora was shaped by strong intermountain isolation interrupted by rare LDDs rather than ecological connectivity. The new evidence points to a much younger and more dynamic island scenario than envisioned by Hedberg: the afroalpine flora is unsaturated and fragile, it was repeatedly disrupted by the Pleistocene climate oscillations, and it harbours taxonomic and genetic diversity that is unique but severely depauperated by frequent bottlenecks and cycles of colonisation, extinction, and recolonisation. The level of intrapopulation genetic variation is alarmingly low, and many afroalpine species may be vulnerable to extinction because of climate warming and increasing human impact

Leaps and bounds: geographical and ecological distance constrained the colonisation of the Afrotemperate by Erica

Background The coincidence of long distance dispersal (LDD) and biome shift is assumed to be the result of a multifaceted interplay between geographical distance and ecological suitability of source and sink areas. Here, we test the influence of these factors on the dispersal history of the flowering plant genus Erica (Ericaceae) across the Afrotemperate. We quantify similarity of Erica climate niches per biogeographic area using direct observations of species, and test various colonisation scenarios while estimating ancestral areas for the Erica clade using parametric biogeographic model testing. Results We infer that the overall dispersal history of Erica across the Afrotemperate is the result of infrequent colonisation limited by geographic proximity and niche similarity. However, the Drakensberg Mountains represent a colonisation sink, rather than acting as a “stepping stone” between more distant and ecologically dissimilar Cape and Tropical African regions. Strikingly, the most dramatic examples of species radiations in Erica were the result of single unique dispersals over longer distances between ecologically dissimilar areas, contradicting the rule of phylogenetic biome conservatism. Conclusions These results highlight the roles of geographical and ecological distance in limiting LDD, but also the importance of rare biome shifts, in which a unique dispersal event fuels evolutionary radiation