Phylogenomic analysis reveals five independently evolved African forage grass clades in the genus Urochloa.

BACKGROUND AND AIMS: The grass genus Urochloa (Brachiaria) sensu lato includes forage crops that are important for beef and dairy industries in tropical and sub-tropical Africa, South America and Oceania/Australia. Economically important species include U. brizantha, U. decumbens, U. humidicola, U. mutica, U. arrecta, U. trichopus, U. mosambicensis and Megathyrsus maximus, all native to the African continent. Perennial growth habits, large, fast growing palatable leaves, intra- and interspecific morphological variability, apomictic reproductive systems and frequent polyploidy are widely shared within the genus. The combination of these traits probably favoured the selection for forage domestication and weediness, but trait emergence across Urochloa cannot be modelled, as a robust phylogenetic assessment of the genus has not been conducted. We aim to produce a phylogeny for Urochloa that includes all important forage species, and identify their closest wild relatives (crop wild relatives). Finally, we will use our phylogeny and available trait data to infer the ancestral states of important forage traits across Urochloa s.l. and model the evolution of forage syndromes across the genus. METHODS: Using a target enrichment sequencing approach (Angiosperm 353), we inferred a species-level phylogeny for Urochloa s.l., encompassing 54 species (~40 % of the genus) and outgroups. Phylogenies were inferred using a multispecies coalescent model and maximum likelihood method. We determined the phylogenetic placement of agriculturally important species and identified their closest wild relatives, or crop wild relatives, based on well-supported monophyly. Further, we mapped key traits associated with Urochloa forage crops to the species tree and estimated ancestral states for forage traits along branch lengths for continuous traits and at ancestral nodes in discrete traits. KEY RESULTS: Agricultural species belong to five independent clades, including U. brizantha and U. decumbens lying in a previously defined species complex. Crop wild relatives were identified for these clades supporting previous sub-generic groupings in Urochloa based on morphology. Using ancestral trait estimation models, we find that five morphological traits that correlate with forage potential (perennial growth habits, culm height, leaf size, a winged rachis and large seeds) independently evolved in forage clades. CONCLUSIONS: Urochloa s.l. is a highly diverse genus that contains numerous species with agricultural potential, including crop wild relatives that are currently underexploited. All forage species and their crop wild relatives naturally occur on the African continent and their conservation across their native distributions is essential. Genomic and phenotypic diversity in forage clade species and their wild relatives need to be better assessed both to develop conservation strategies and to exploit the diversity in the genus for improved sustainability in Urochloa cultivar production.

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.

Madagascar's extraordinary biodiversity: Evolution, distribution, and use.

Madagascar's biota is hyperdiverse and includes exceptional levels of endemicity. We review the current state of knowledge on Madagascar's past and current terrestrial and freshwater biodiversity by compiling and presenting comprehensive data on species diversity, endemism, and rates of species description and human uses, in addition to presenting an updated and simplified map of vegetation types. We report a substantial increase of records and species new to science in recent years; however, the diversity and evolution of many groups remain practically unknown (e.g., fungi and most invertebrates). Digitization efforts are increasing the resolution of species richness patterns and we highlight the crucial role of field- and collections-based research for advancing biodiversity knowledge and identifying gaps in our understanding, particularly as species richness corresponds closely to collection effort. Phylogenetic diversity patterns mirror that of species richness and endemism in most of the analyzed groups. We highlight humid forests as centers of diversity and endemism because of their role as refugia and centers of recent and rapid radiations. However, the distinct endemism of other areas, such as the grassland-woodland mosaic of the Central Highlands and the spiny forest of the southwest, is also biologically important despite lower species richness. The documented uses of Malagasy biodiversity are manifold, with much potential for the uncovering of new useful traits for food, medicine, and climate mitigation. The data presented here showcase Madagascar as a unique "living laboratory" for our understanding of evolution and the complex interactions between people and nature. The gathering and analysis of biodiversity data must continue and accelerate if we are to fully understand and safeguard this unique subset of Earth's biodiversity.

Madagascar's extraordinary biodiversity: Threats and opportunities.

Madagascar's unique biota is heavily affected by human activity and is under intense threat. Here, we review the current state of knowledge on the conservation status of Madagascar's terrestrial and freshwater biodiversity by presenting data and analyses on documented and predicted species-level conservation statuses, the most prevalent and relevant threats, ex situ collections and programs, and the coverage and comprehensiveness of protected areas. The existing terrestrial protected area network in Madagascar covers 10.4% of its land area and includes at least part of the range of the majority of described native species of vertebrates with known distributions (97.1% of freshwater fishes, amphibians, reptiles, birds, and mammals combined) and plants (67.7%). The overall figures are higher for threatened species (97.7% of threatened vertebrates and 79.6% of threatened plants occurring within at least one protected area). International Union for Conservation of Nature (IUCN) Red List assessments and Bayesian neural network analyses for plants identify overexploitation of biological resources and unsustainable agriculture as the most prominent threats to biodiversity. We highlight five opportunities for action at multiple levels to ensure that conservation and ecological restoration objectives, programs, and activities take account of complex underlying and interacting factors and produce tangible benefits for the biodiversity and people of Madagascar.

Biogeographic history of a large clade of ectomycorrhizal fungi, the Russulaceae, in the Neotropics and adjacent regions.

The biogeography of neotropical fungi remains poorly understood. Here, we reconstruct the origins and diversification of neotropical lineages in one of the largest clades of ectomycorrhizal fungi in the globally widespread family Russulaceae. We inferred a supertree of 3285 operational taxonomic units, representing worldwide internal transcribed spacer sequences. We reconstructed biogeographic history and diversification and identified lineages in the Neotropics and adjacent Patagonia. The ectomycorrhizal Russulaceae have a tropical African origin. The oldest lineages in tropical South America, most with African sister groups, date to the mid-Eocene, possibly coinciding with a boreotropical migration corridor. There were several transatlantic dispersal events from Africa more recently. Andean and Central American lineages mostly have north-temperate origins and are associated with North Andean uplift and the general north-south biotic interchange across the Panama isthmus, respectively. Patagonian lineages have Australasian affinities. Diversification rates in tropical South America and other tropical areas are lower than in temperate areas. Neotropical Russulaceae have multiple biogeographic origins since the mid-Eocene involving dispersal and co-migration. Discontinuous distributions of host plants may explain low diversification rates of tropical lowland ectomycorrhizal fungi. Deeply diverging neotropical fungal lineages need to be better documented.

Modelling the tempo and mode of lineage dispersal.

Lineage dispersal is a basic macroevolutionary process shaping the distribution of biodiversity. Probabilistic approaches in biogeography, epidemiology, and macroecology often model dispersal as a background process to explain extant or infer past distributions. We propose framing questions around the mode, timing, rate, and direction of lineage dispersal itself, from a lineage- or geography-centric perspective. We review available methods for modelling lineage dispersal. Likelihood- and simulation-based approaches to modelling dispersal have made progress in accounting for the variation of lineage dispersal over space, time, and branches of a phylogeny and its interaction with diversification. Methodological improvements, guided by a focus on model adequacy, will lead to more realistic models that can answer fundamental questions about the tempo and mode of lineage dispersal.

Fire and grazing determined grasslands of central Madagascar represent ancient assemblages.

The ecology of Madagascar's grasslands is under-investigated and the dearth of ecological understanding of how disturbance by fire and grazing shapes these grasslands stems from a perception that disturbance shaped Malagasy grasslands only after human arrival. However, worldwide, fire and grazing shape tropical grasslands over ecological and evolutionary timescales, and it is curious Madagascar should be a global anomaly. We examined the functional and community ecology of Madagascar's grasslands across 71 communities in the Central Highlands. Combining multivariate abundance models of community composition and clustering of grass functional traits, we identified distinct grass assemblages each shaped by fire or grazing. The fire-maintained assemblage is primarily composed of tall caespitose species with narrow leaves and low bulk density. By contrast, the grazer-maintained assemblage is characterized by mat-forming, high bulk density grasses with wide leaves. Within each assemblage, levels of endemism, diversity and grass ages support these as ancient assemblages. Grazer-dependent grasses can only have co-evolved with a now-extinct megafauna. Ironically, the human introduction of cattle probably introduced a megafaunal substitute facilitating modern day persistence of a grazer-maintained grass assemblage in an otherwise defaunated landscape, where these landscapes now support the livelihoods of millions of people.

Continued Adaptation of C4 Photosynthesis After an Initial Burst of Changes in the Andropogoneae Grasses.

C$_{4}$ photosynthesis is a complex trait that sustains fast growth and high productivity in tropical and subtropical conditions and evolved repeatedly in flowering plants. One of the major C$_{4}$ lineages is Andropogoneae, a group of $\sim $1200 grass species that includes some of the world's most important crops and species dominating tropical and some temperate grasslands. Previous efforts to understand C$_{4}$ evolution in the group have compared a few model C$_{4}$ plants to distantly related C$_{3}$ species so that changes directly responsible for the transition to C$_{4}$ could not be distinguished from those that preceded or followed it. In this study, we analyze the genomes of 66 grass species, capturing the earliest diversification within Andropogoneae as well as their C$_{3}$ relatives. Phylogenomics combined with molecular dating and analyses of protein evolution show that many changes linked to the evolution of C$_{4}$ photosynthesis in Andropogoneae happened in the Early Miocene, between 21 and 18 Ma, after the split from its C$_{3}$ sister lineage, and before the diversification of the group. This initial burst of changes was followed by an extended period of modifications to leaf anatomy and biochemistry during the diversification of Andropogoneae, so that a single C$_{4}$ origin gave birth to a diversity of C$_{4}$ phenotypes during 18 million years of speciation events and migration across geographic and ecological spaces. Our comprehensive approach and broad sampling of the diversity in the group reveals that one key transition can lead to a plethora of phenotypes following sustained adaptation of the ancestral state. [Adaptive evolution; complex traits; herbarium genomics; Jansenelleae; leaf anatomy; Poaceae; phylogenomics.].

One-third of the plastid genes evolved under positive selection in PACMAD grasses.

MAIN CONCLUSION: We demonstrate that rbcL underwent strong positive selection during the C 3 -C 4 photosynthetic transitions in PACMAD grasses, in particular the 3' end of the gene. In contrast, selective pressures on other plastid genes vary widely and environmental drivers remain to be identified. Plastid genomes have been widely used to infer phylogenetic relationships among plants, but the selective pressures driving their evolution have not been systematically investigated. In our study, we analyse all protein-coding plastid genes from 113 species of PACMAD grasses (Poaceae) to evaluate the selective pressures driving their evolution. Our analyses confirm that the gene encoding the large subunit of RubisCO (rbcL) evolved under strong positive selection after C3-C4 photosynthetic transitions. We highlight new codons in rbcL that underwent parallel changes, in particular those encoding the C-terminal part of the protein. C3-C4 photosynthetic shifts did not significantly affect the evolutionary dynamics of other plastid genes. Instead, while two-third of the plastid genes evolved under purifying selection or neutrality, 25 evolved under positive selection across the PACMAD clade. This set of genes encode for proteins involved in diverse functions, including self-replication of plastids and photosynthesis. Our results suggest that plastid genes widely adapt to changing ecological conditions, but factors driving this evolution largely remain to be identified.