Phylogenomics and the rise of the angiosperms.

Angiosperms are the cornerstone of most terrestrial ecosystems and human livelihoods1,2. A robust understanding of angiosperm evolution is required to explain their rise to ecological dominance. So far, the angiosperm tree of life has been determined primarily by means of analyses of the plastid genome3,4. Many studies have drawn on this foundational work, such as classification and first insights into angiosperm diversification since their Mesozoic origins5-7. However, the limited and biased sampling of both taxa and genomes undermines confidence in the tree and its implications. Here, we build the tree of life for almost 8,000 (about 60%) angiosperm genera using a standardized set of 353 nuclear genes8. This 15-fold increase in genus-level sampling relative to comparable nuclear studies9 provides a critical test of earlier results and brings notable change to key groups, especially in rosids, while substantiating many previously predicted relationships. Scaling this tree to time using 200 fossils, we discovered that early angiosperm evolution was characterized by high gene tree conflict and explosive diversification, giving rise to more than 80% of extant angiosperm orders. Steady diversification ensued through the remaining Mesozoic Era until rates resurged in the Cenozoic Era, concurrent with decreasing global temperatures and tightly linked with gene tree conflict. Taken together, our extensive sampling combined with advanced phylogenomic methods shows the deep history and full complexity in the evolution of a megadiverse clade.

Fire facilitates ground layer plant diversity in a Miombo ecosystem.

BACKGROUND AND AIMS: Little is known about the response of ground layer plant communities to fire in Miombo ecosystems, which is a global blind spot of ecological understanding. We aim to (i) assess the impact of three experimentally imposed fire treatments on ground layer species composition, and compare it with patterns observed for trees; and (ii) analyse the effect of fire treatments on species richness to assess how responses differ among plant functional groups. METHODS: At a 60-year-long fire experiment in Zambia, we quantified the richness and diversity of ground layer plants in terms of taxa and functional groups across three experimental fire treatments of late dry-season fire, early dry-season fire, and fire exclusion. Data were collected in five repeat surveys from the onset of the wet season to the early dry season. KEY RESULTS: Of the 140 ground layer species recorded across the three treatments, fire-maintained treatments contributed most of the richness and diversity, with the least number of unique species found at the No-fire treatment. The Early-fire treatment was more similar in composition to the No-fire treatment than to the Late-fire treatment. C4 grass and geoxyle richness were highest in the Late-fire treatment, and there were no shared sedge species between the Late-fire and other treatments. At a plot level, the average richness in the Late-fire treatment was twice that of the fire exclusion treatment. CONCLUSIONS: Heterogeneity in fire seasonality and intensity supports diversity of a unique flora by providing a diversity of local environments. African ecosystems face rapid expansion of land and fire management schemes for carbon offsetting and sequestration. We demonstrate that analyses of the impacts of such schemes predicated on the tree flora alone will highly likely underestimate impacts on biodiversity. A research priority must be a new understanding of the Miombo ground layer flora integrated into policy and land management.

Envisaging a global infrastructure to exploit the potential of digitised collections.

Tens of millions of images from biological collections have become available online over the last two decades. In parallel, there has been a dramatic increase in the capabilities of image analysis technologies, especially those involving machine learning and computer vision. While image analysis has become mainstream in consumer applications, it is still used only on an artisanal basis in the biological collections community, largely because the image corpora are dispersed. Yet, there is massive untapped potential for novel applications and research if images of collection objects could be made accessible in a single corpus. In this paper, we make the case for infrastructure that could support image analysis of collection objects. We show that such infrastructure is entirely feasible and well worth investing in.

Global analysis of Poales diversification - parallel evolution in space and time into open and closed habitats.

Poales are one of the most species-rich, ecologically and economically important orders of plants and often characterise open habitats, enabled by unique suites of traits. We test six hypotheses regarding the evolution and assembly of Poales in open and closed habitats throughout the world, and examine whether diversification patterns demonstrate parallel evolution. We sampled 42% of Poales species and obtained taxonomic and biogeographic data from the World Checklist of Vascular Plants database, which was combined with open/closed habitat data scored by taxonomic experts. A dated supertree of Poales was constructed. We integrated spatial phylogenetics with regionalisation analyses, historical biogeography and ancestral state estimations. Diversification in Poales and assembly of open and closed habitats result from dynamic evolutionary processes that vary across lineages, time and space, most prominently in tropical and southern latitudes. Our results reveal parallel and recurrent patterns of habitat and trait transitions in the species-rich families Poaceae and Cyperaceae. Smaller families display unique and often divergent evolutionary trajectories. The Poales have achieved global dominance via parallel evolution in open habitats, with notable, spatially and phylogenetically restricted divergences into strictly closed habitats.

A Taxonomically-verified and Vouchered Checklist of the Vascular Plants of the Republic of Guinea.

The Checklist of the Vascular Plants of the Republic of Guinea (CVPRG) is a specimen-based, expert-validated knowledge product, which provides a concise synthesis and overview of current knowledge on 3901 vascular plant species documented from Guinea (Conakry), West Africa, including their accepted names and synonyms, as well as their distribution and status within Guinea (indigenous or introduced, endemic or not). The CVPRG is generated automatically from the Guinea Collections Database and the Guinea Names Backbone Database, both developed and maintained at the Royal Botanic Gardens, Kew, in collaboration with the staff of the National Herbarium of Guinea. A total of 3505 indigenous vascular plant species are reported of which 3328 are flowering plants (angiosperms); this represents a 26% increase in known indigenous angiosperms since the last floristic overview. Intended as a reference for scientists documenting the diversity and distribution of the Guinea flora, the CVPRG will also inform those seeking to safeguard the rich plant diversity of Guinea and the societal, ecological and economic benefits accruing from these biological resources.

Phylogenomics sheds new light on the drivers behind a long-lasting systematic riddle: the figwort family Scrophulariaceae.

The figwort family, Scrophulariaceae, comprises c. 2000 species whose evolutionary relationships at the tribal level have proven difficult to resolve, hindering our ability to understand their origin and diversification. We designed a specific probe kit for Scrophulariaceae, targeting 849 nuclear loci and obtaining plastid regions as by-products. We sampled c. 87% of the genera described in the family and use the nuclear dataset to estimate evolutionary relationships, timing of diversification, and biogeographic patterns. Ten tribes, including two new tribes, Androyeae and Camptolomeae, are supported, and the phylogenetic positions of Androya, Camptoloma, and Phygelius are unveiled. Our study reveals a major diversification at c. 60 million yr ago in some Gondwanan landmasses, where two different lineages diversified, one of which gave rise to nearly 81% of extant species. A Southern African origin is estimated for most modern-day tribes, with two exceptions, the American Leucophylleae, and the mainly Australian Myoporeae. The rapid mid-Eocene diversification is aligned with geographic expansion within southern Africa in most tribes, followed by range expansion to tropical Africa and multiple dispersals out of Africa. Our robust phylogeny provides a framework for future studies aimed at understanding the role of macroevolutionary patterns and processes that generated Scrophulariaceae diversity.

The phylogeny and global biogeography of Primulaceae based on high-throughput DNA sequence data.

The angiosperm family Primulaceae is morphologically diverse and distributed nearly worldwide. However, phylogenetic uncertainty has obstructed the identification of major morphological and biogeographic transitions within the clade. We used target capture sequencing with the Angiosperms353 probes, taxon-sampling encompassing nearly all genera of the family, tree-based sequence curation, and multiple phylogenetic approaches to investigate the major clades of Primulaceae and their relationship to other Ericales. We generated dated phylogenetic trees and conducted broad-scale biogeographic analyses as well as stochastic character mapping of growth habit. We show that Ardisia, a pantropical genus and the largest in the family, is not monophyletic, with at least 19 smaller genera nested within it. Neotropical members of Ardisia and several smaller genera form a clade, an ancestor of which arrived in the Neotropics and began diversifying about 20 Ma. This Neotropical clade is most closely related to Elingamita and Tapeinosperma, which are most diverse on islands of the Pacific. Both Androsace and Primula are non-monophyletic by the inclusion of smaller genera. Ancestral state reconstructions revealed that there have either been parallel transitions to an herbaceous habit in Primuloideae, Samolus, and at least three lineages of Myrsinoideae, or a common ancestor of nearly all Primulaceae was herbaceous. Our results provide a robust estimate of phylogenetic relationships across Primulaceae and show that a revised classification of Myrsinoideae and several other clades within the family is necessary to render all genera monophyletic.

A monograph of the African and Madagascan species of Cyperus sect. Incurvi (Cyperaceae).

Cyperus sect. Incurvi (Cyperaceae) contains 31 species worldwide, with important continental radiations in Australasia, Tropical Africa and Madagascar, and the Neotropics. Here, a monograph of the African and Madagascan species of Cyperus sect. Incurvi is presented, including descriptions, illustrations, synonymy, notes on habitat and ecology, geographic distribution ranges and conservation assessments. Our results identify eight species of Cyperus sect. Incurvi endemic to Madagascar, and a further three species native to Tropical Africa. Seven species of Cyperus sect. Incurvi have been typified herein. Six rare Madagascan endemics are assessed as threatened with extinction.

Chromosome size matters: genome evolution in the cyperid clade.

BACKGROUND AND AIMS: While variation in genome size and chromosome numbers and their consequences are often investigated in plants, the biological relevance of variation in chromosome size remains poorly known. Here, we examine genome and mean chromosome size in the cyperid clade (families Cyperaceae, Juncaceae and Thurniaceae), which is the largest vascular plant lineage with predominantly holocentric chromosomes. METHODS: We measured genome size in 436 species of cyperids using flow cytometry, and augment these data with previously published datasets. We then separately compared genome and mean chromosome sizes (2C/2n) amongst the major lineages of cyperids and analysed how these two genomic traits are associated with various environmental factors using phylogenetically informed methods. KEY RESULTS: We show that cyperids have the smallest mean chromosome sizes recorded in seed plants, with a large divergence between the smallest and largest values. We found that cyperid species with smaller chromosomes have larger geographical distributions and that there is a strong inverse association between mean chromosome size and number across this lineage. CONCLUSIONS: The distinct patterns in genome size and mean chromosome size across the cyperids might be explained by holokinetic drive. The numerous small chromosomes might function to increase genetic diversity in this lineage where crossovers are limited during meiosis.

Comparison of Magnoliaceae Plastomes: Adding Neotropical Magnolia to the Discussion.

Chloroplast genomes are considered to be highly conserved. Nevertheless, differences in their sequences are an important source of phylogenetically informative data. Chloroplast genomes are increasingly applied in evolutionary studies of angiosperms, including Magnoliaceae. Recent studies have focused on resolving the previously debated classification of the family using a phylogenomic approach and chloroplast genome data. However, most Neotropical clades and recently described species have not yet been included in molecular studies. We performed sequencing, assembly, and annotation of 15 chloroplast genomes from Neotropical Magnoliaceae species. We compared the newly assembled chloroplast genomes with 22 chloroplast genomes from across the family, including representatives from each genus and section. Family-wide, the chloroplast genomes presented a length of about 160 kb. The gene content in all species was constant, with 145 genes. The intergenic regions showed a higher level of nucleotide diversity than the coding regions. Differences were higher among genera than within genera. The phylogenetic analysis in Magnolia showed two main clades and corroborated that the current infrageneric classification does not represent natural groups. Although chloroplast genomes are highly conserved in Magnoliaceae, the high level of diversity of the intergenic regions still resulted in an important source of phylogenetically informative data, even for closely related taxa.

Plastid phylogenomics of the Sansevieria Clade of Dracaena (Asparagaceae) resolves a recent radiation.

Best known as low maintenance houseplants, sansevierias are a diverse group of flowering plants native to Africa, Madagascar, the Arabian Peninsula, and the Indian subcontinent. Traditionally recognised as a distinct genus, Sansevieria was recently merged with the larger genus Dracaena based on molecular phylogenetic data. Within the Sansevieria Clade of Dracaena, taxonomic uncertainties remain despite attempts to unravel the relationships between the species. To investigate the evolutionary relationships, morphological evolution and biogeographical history in the group, we aim to reconstruct a robust dated phylogenetic hypothesis. Using genome skimming, a chloroplast genome (cpDNA) dataset and a nuclear ribosomal (nrDNA) dataset were generated. The sampling included representatives of all sections and informal groups previously described in Sansevieria based on morphology. Analysis of the cpDNA dataset using a maximum likelihood approach resulted in a well-supported phylogeny. The time-calibrated phylogeny indicated a recent radiation with five main clades emerging in the Pliocene. Two strongly supported clades align with previously defined groups, i.e., Sansevieria section Dracomima, characterised by the Dracomima-type inflorescence, and the Zeylanica informal group, native to the Indian subcontinent. Other previously defined groups were shown to be polyphyletic; a result of convergent evolution of the identifying characters. Switches between flat and cylindrical leaves occurred multiple times in the evolution of the Sansevieria Clade. Similarly, the Cephalantha-type inflorescence has originated multiple times from an ancestor with a Sansevieria-type inflorescence. Analysis of the nrDNA dataset resulted in a phylogenetic hypothesis with low resolution, yet it supported the same two groups confirmed by the cpDNA dataset. This study furthers our understanding of the evolution of the Sansevieria Clade, which will benefit taxonomic and applied research, and aid conservation efforts.

The evolutionary history of the Caribbean magnolias (Magnoliaceae): Testing species delimitations and biogeographical hypotheses using molecular data.

The Caribbean islands provide an ideal setting for studying biodiversity, given their complex geological and environmental history, and their historical and current geographical proximity to the American mainland. Magnolia, a flagship tree genus that has 15 endemic and threatened taxa (12 species and 3 subspecies) on the Caribbean islands, offers an excellent case study to empirically test Caribbean biogeographical hypotheses. We constructed phylogenetic hypotheses to: (1) reveal their evolutionary history, (2) test the current largely morphology-based classification and assess species limits, and (3) investigate major biogeographic hypotheses proposed for the region. Nuclear and chloroplast DNA sequence data of all 15 Caribbean Magnolia taxa are included, supplemented by a selection of American mainland species, and species representing most major clades of the Magnoliaceae family. We constructed phylogenetic hypotheses in a time-calibrated Bayesian framework, supplemented with haplotype network analyses and ancestral range estimations. Genetic synapomorphies in the studied markers confirm the species limits of 14 out of 15 morphologically recognizable Caribbean Magnolia taxa. There is evidence for four colonization events of Magnolia into the Caribbean from the American mainland, which most likely occurred by overwater dispersal, given age estimates of maximum 16 mya for their presence on the Caribbean islands.

Joining forces in Ochnaceae phylogenomics: a tale of two targeted sequencing probe kits.

PREMISE: Both universal and family-specific targeted sequencing probe kits are becoming widely used for reconstruction of phylogenetic relationships in angiosperms. Within the pantropical Ochnaceae, we show that with careful data filtering, universal kits are equally as capable in resolving intergeneric relationships as custom probe kits. Furthermore, we show the strength in combining data from both kits to mitigate bias and provide a more robust result to resolve evolutionary relationships. METHODS: We sampled 23 Ochnaceae genera and used targeted sequencing with two probe kits, the universal Angiosperms353 kit and a family-specific kit. We used maximum likelihood inference with a concatenated matrix of loci and multispecies-coalescence approaches to infer relationships in the family. We explored phylogenetic informativeness and the impact of missing data on resolution and tree support. RESULTS: For the Angiosperms353 data set, the concatenation approach provided results more congruent with those of the Ochnaceae-specific data set. Filtering missing data was most impactful on the Angiosperms353 data set, with a relaxed threshold being the optimum scenario. The Ochnaceae-specific data set resolved consistent topologies using both inference methods, and no major improvements were obtained after data filtering. Merging of data obtained with the two kits resulted in a well-supported phylogenetic tree. CONCLUSIONS: The Angiosperms353 data set improved upon data filtering, and missing data played an important role in phylogenetic reconstruction. The Angiosperms353 data set resolved the phylogenetic backbone of Ochnaceae as equally well as the family specific data set. All analyses indicated that both Sauvagesia L. and Campylospermum Tiegh. as currently circumscribed are polyphyletic and require revised delimitation.

Cyperus prophyllatus: An endangered aquatic new species of Cyperus L. (Cyperaceae) with a exceptional spikelet disarticulation pattern among about 950 species, including molecular phylogenetic, anatomical and (micro)morphological data.

Cyperus prophyllatus, an endangered new species of Cyperus (Cyperaceae) from an aquatic ecosystem of the Atlantic Forest, Espírito Santo State, southeastern Brazil, is described and illustrated. The spikelet morphology of Cyperus prophyllatus is unique among the c. 950 species of Cyperus in having both a conspicuous spikelet prophyll and a corky rachilla articulation, which remain persistent at the base of the spikelet after disarticulation. Our molecular phylogenetic data support the placement of C. prophyllatus in the C3 Cyperus Grade and more precisely in the clade representing Cyperus sect. Oxycaryum, which also includes C. blepharoleptos and C. gardneri. Anatomical and (micro)morphological analyses corroborate the phylogenetic results, provide a better understanding of ecology and taxonomy, as well as reveal compatibility of structures with survival and dispersion in aquatic environments. A distribution map, table with distinctive characters of allied species, and conservation status are made available.

Delimiting the genera of the Ficinia Clade (Cypereae, Cyperaceae) based on molecular phylogenetic data.

Generic delimitations in the Ficinia Clade of tribe Cypereae are revisited. In particular, we aim to establish the placement of annual species currently included in Isolepis of which the phylogenetic position is uncertain. Phylogenetic inference is based on two nuclear markers (ETS, ITS) and five plastid markers (the genes matK, ndhF, rbcL and rps16, the trnL intron and trnL-F spacer) data, analyzed using model based methods. Topologies based on nuclear and plastid data show incongruence at the backbone. Therefore, the results are presented separately. The monophyly of the smaller genera (Afroscirpoides, Dracoscirpoides, Erioscirpus, Hellmuthia, Scirpoides) is confirmed. However, Isolepis is paraphyletic as Ficinia is retrieved as one of its clades. Furthermore, Ficinia is paraphyletic if I. marginata and allies are excluded. We take a pragmatic approach based on the nuclear topology, driven by a desire to minimize taxonomic changes, to recircumscribe Ficinia to include the annual Isolepis species characterized by cartilaginous glumes and formally include all the Isolepis species inferred outside the core Isolepis clade. Consequently, the circumscription of Isolepis is narrowed to encompass only those species retrieved as part of the core Isolepis clade. Five new combinations are made (Ficinia neocapensis, Ficinia hemiuncialis, Ficinia incomtula, Ficinia leucoloma, Ficinia minuta). We present nomenclatural summary at genus level, identification keys and diagnostic features.

Introgression across evolutionary scales suggests reticulation contributes to Amazonian tree diversity.

Hybridization has the potential to generate or homogenize biodiversity and is a particularly common phenomenon in plants, with an estimated 25% of plant species undergoing interspecific gene flow. However, hybridization in Amazonia's megadiverse tree flora was assumed to be extremely rare despite extensive sympatry between closely related species, and its role in diversification remains enigmatic because it has not yet been examined empirically. Using members of a dominant Amazonian tree family (Brownea, Fabaceae) as a model to address this knowledge gap, our study recovered extensive evidence of hybridization among multiple lineages across phylogenetic scales. More specifically, using targeted sequence capture our results uncovered several historical introgression events between Brownea lineages and indicated that gene tree incongruence in Brownea is best explained by reticulation, rather than solely by incomplete lineage sorting. Furthermore, investigation of recent hybridization using ~19,000 ddRAD loci recovered a high degree of shared variation between two Brownea species that co-occur in the Ecuadorian Amazon. Our analyses also showed that these sympatric lineages exhibit homogeneous rates of introgression among loci relative to the genome-wide average, implying a lack of selection against hybrid genotypes and persistent hybridization. Our results demonstrate that gene flow between multiple Amazonian tree species has occurred across temporal scales, and contrasts with the prevailing view of hybridization's rarity in Amazonia. Overall, our results provide novel evidence that reticulate evolution influenced diversification in part of the Amazonian tree flora, which is the most diverse on Earth.

First molecular phylogenetic insights into the evolution of Eriocaulon (Eriocaulaceae, Poales).

Eriocaulon is a genus of c. 470 aquatic and wetland species of the monocot plant family Eriocaulaceae. It is widely distributed in Africa, Asia and America, with centres of species richness in the tropics. Most species of Eriocaulon grow in wetlands although some inhabit shallow rivers and streams with an apparent adaptive morphology of elongated submerged stems. In a previous molecular phylogenetic hypothesis, Eriocaulon was recovered as sister of the African endemic genus Mesanthemum. Several regional infrageneric classifications have been proposed for Eriocaulon. This study aims to critically assess the existing infrageneric classifications through phylogenetic reconstruction of infrageneric relationships, based on DNA sequence data of four chloroplast markers and one nuclear marker. There is little congruence between our molecular results and previous morphology-based infrageneric classifications. However, some similarities can be found, including Fyson's sect. Leucantherae and Zhang's sect. Apoda. Further phylogenetic studies, particularly focusing on less well sampled regions such as the Neotropics, will help provide a more global overview of the relationships in Eriocaulon and may enable suggesting the first global infrageneric classification.

Revision of the Afro-Madagascan genus Costularia (Schoeneae, Cyperaceae): infrageneric relationships and species delimitation.

A recent molecular phylogenetic study revealed four distinct evolutionary lineages in the genus Costularia s.l. (Schoeneae, Cyperaceae, Poales). Two lineages are part of the Oreobolus clade of tribe Schoeneae: the first being a much-reduced genus Costularia s.s., and the second a lineage endemic to New Caledonia for which a new genus Chamaedendron was erected. The other two lineages were shown to be part of the Tricostularia clade of tribe Schoeneae. Based on morphological and molecular data, the genus Costularia is here redelimited to represent a monophyletic entity including 15 species, which is restricted in distribution to southeastern Africa (Malawi, Mozambique, South Africa, Swaziland, Zimbabwe), Madagascar, the Mascarenes (La Réunion, Mauritius), and the Seychelles (Mahé). Molecular phylogenetic data based on two nuclear markers (ETS, ITS) and a chloroplast marker (trnL-F) resolve the studied taxa as monophyletic where multiple accessions could be included (except for Costularia laxa and Costularia purpurea, which are now considered conspecific), and indicate that the genus dispersed once to Africa, twice to the Mascarenes, and once to the Seychelles. Two endemic species from Madagascar are here described and illustrated as new to science, as is one additional species endemic to La Réunion. Two taxa previously accepted as varieties of Costularia pantopoda are here recognised at species level (Costularia baronii and Costularia robusta). We provide a taxonomic revision including an identification key, species descriptions and illustrations, distribution maps and assessments of conservation status for all species.

Response of xerophytic plants to glacial cycles in southern South America.

BACKGROUND AND AIM: Quaternary glaciations strongly affected the distribution of species from arid and semi-arid environments, as temperature drops were accompanied by strong fluctuations in rainfall. In this study, we examined the response of xerophytic species to glacial cycles, determining the genetic patterns and climatic niche of Echinopsis chiloensis var. chiloensis, an endemic columnar cactus of arid and semi-arid regions of Chile. METHODS: We analysed 11 polymorphic microsatellites for 130 individuals from 13 populations distributed across the entire distribution of the species. We examined genetic diversity and structure, identified possible patterns of isolation by distance (IBD) and tested two competing population history scenarios using Approximate Bayesian Computation. The first scenario assumes a constant population size while the second includes a bottleneck in the southern population. The latter scenario assumed that the southernmost populations experienced a strong contraction during glaciation, followed by a postglacial expansion; by contrast, the area of the northernmost populations remained as a stable refugium. We also used ecological niche modelling (ENM) to evaluate the location and extension of suitable areas during the Last Glacial Maximum (LGM) and the mid-Holocene. KEY RESULTS: We found a decline in genetic diversity towards high latitudes and a significant IBD pattern that together with ENM predictions suggest that E. chiloensis var. chiloensis experienced range contraction northwards during wet-cold conditions of the LGM, followed by expansion during aridification of the mid-Holocene. In addition to IBD, we detected the presence of a strong barrier to gene flow at 32°30'S, which according to coalescence analysis occurred 44 kyr BP. The resulting genetic clusters differed in realized climatic niche, particularly in the variables related to precipitation. CONCLUSIONS: Our results suggest that the cactus E. chiloensis var. chiloensis experienced range contraction and fragmentation during the wet-cold conditions of the LGM, which may have facilitated ecological differentiation between northern and southern populations, promoting incipient speciation.