Anatomy of a mega-radiation: Biogeography and niche evolution in Astragalus.

PREMISE: Astragalus (Fabaceae), with more than 3000 species, represents a globally successful radiation of morphologically highly similar species predominant across the northern hemisphere. It has attracted attention from systematists and biogeographers, who have asked what factors might be behind the extraordinary diversity of this important arid-adapted clade and what sets it apart from close relatives with far less species richness. METHODS: Here, for the first time using extensive phylogenetic sampling, we asked whether (1) Astragalus is uniquely characterized by bursts of radiation or whether diversification instead is uniform and no different from closely related taxa. Then we tested whether the species diversity of Astragalus is attributable specifically to its predilection for (2) cold and arid habitats, (3) particular soils, or to (4) chromosome evolution. Finally, we tested (5) whether Astragalus originated in central Asia as proposed and (6) whether niche evolutionary shifts were subsequently associated with the colonization of other continents. RESULTS: Our results point to the importance of heterogeneity in the diversification of Astragalus, with upshifts associated with the earliest divergences but not strongly tied to any abiotic factor or biogeographic regionalization tested here. The only potential correlate with diversification we identified was chromosome number. Biogeographic shifts have a strong association with the abiotic environment and highlight the importance of central Asia as a biogeographic gateway. CONCLUSIONS: Our investigation shows the importance of phylogenetic and evolutionary studies of logistically challenging "mega-radiations." Our findings reject any simple key innovation behind high diversity and underline the often nuanced, multifactorial processes leading to species-rich clades.

Phylogenomic analyses of Sapindales support new family relationships, rapid Mid-Cretaceous Hothouse diversification, and heterogeneous histories of gene duplication.

Sapindales is an angiosperm order of high economic and ecological value comprising nine families, c. 479 genera, and c. 6570 species. However, family and subfamily relationships in Sapindales remain unclear, making reconstruction of the order's spatio-temporal and morphological evolution difficult. In this study, we used Angiosperms353 target capture data to generate the most densely sampled phylogenetic trees of Sapindales to date, with 448 samples and c. 85% of genera represented. The percentage of paralogous loci and allele divergence was characterized across the phylogeny, which was time-calibrated using 29 rigorously assessed fossil calibrations. All families were supported as monophyletic. Two core family clades subdivide the order, the first comprising Kirkiaceae, Burseraceae, and Anacardiaceae, the second comprising Simaroubaceae, Meliaceae, and Rutaceae. Kirkiaceae is sister to Burseraceae and Anacardiaceae, and, contrary to current understanding, Simaroubaceae is sister to Meliaceae and Rutaceae. Sapindaceae is placed with Nitrariaceae and Biebersteiniaceae as sister to the core Sapindales families, but the relationships between these families remain unclear, likely due to their rapid and ancient diversification. Sapindales families emerged in rapid succession, coincident with the climatic change of the Mid-Cretaceous Hothouse event. Subfamily and tribal relationships within the major families need revision, particularly in Sapindaceae, Rutaceae and Meliaceae. Much of the difficulty in reconstructing relationships at this level may be caused by the prevalence of paralogous loci, particularly in Meliaceae and Rutaceae, that are likely indicative of ancient gene duplication events such as hybridization and polyploidization playing a role in the evolutionary history of these families. This study provides key insights into factors that may affect phylogenetic reconstructions in Sapindales across multiple scales, and provides a state-of-the-art phylogenetic framework for further research.

Lineage-specific vs. universal: A comparison of the Compositae1061 and Angiosperms353 enrichment panels in the sunflower family.

PREMISE: Phylogenetic studies in the Compositae are challenging due to the sheer size of the family and the challenges they pose for molecular tools, ranging from the genomic impact of polyploid events to their very conserved plastid genomes. The search for better molecular tools for phylogenetic studies led to the development of the family-specific Compositae1061 probe set, as well as the universal Angiosperms353 probe set designed for all flowering plants. In this study, we evaluate the extent to which data generated using the family-specific kit and those obtained with the universal kit can be merged for downstream analyses. METHODS: We used comparative methods to verify the presence of shared loci between probe sets. Using two sets of eight samples sequenced with Compositae1061 and Angiosperms353, we ran phylogenetic analyses with and without loci flagged as paralogs, a gene tree discordance analysis, and a complementary phylogenetic analysis mixing samples from both sample sets. RESULTS: Our results show that the Compositae1061 kit provides an average of 721 loci, with 9-46% of them presenting paralogs, while the Angiosperms353 set yields an average of 287 loci, which are less affected by paralogy. Analyses mixing samples from both sets showed that the presence of 30 shared loci in the probe sets allows the combination of data generated in different ways. DISCUSSION: Combining data generated using different probe sets opens up the possibility of collaborative efforts and shared data within the synantherological community.

Biodiversity at the global scale: the synthesis continues.

Traditionally, the generation and use of biodiversity data and their associated specimen objects have been primarily the purview of individuals and small research groups. While deposition of data and specimens in herbaria and other repositories has long been the norm, throughout most of their history, these resources have been accessible only to a small community of specialists. Through recent concerted efforts, primarily at the level of national and international governmental agencies over the last two decades, the pace of biodiversity data accumulation has accelerated, and a wider array of biodiversity scientists has gained access to this massive accumulation of resources, applying them to an ever-widening compass of research pursuits. We review how these new resources and increasing access to them are affecting the landscape of biodiversity research in plants today, focusing on new applications across evolution, ecology, and other fields that have been enabled specifically by the availability of these data and the global scope that was previously beyond the reach of individual investigators. We give an overview of recent advances organized along three lines: broad-scale analyses of distributional data and spatial information, phylogenetic research circumscribing large clades with comprehensive taxon sampling, and data sets derived from improved accessibility of biodiversity literature. We also review synergies between large data resources and more traditional data collection paradigms, describe shortfalls and how to overcome them, and reflect on the future of plant biodiversity analyses in light of increasing linkages between data types and scientists in our field.

Comparative analyses of Mikania (Asteraceae: Eupatorieae) plastomes and impact of data partitioning and inference methods on phylogenetic relationships.

We assembled new plastomes of 19 species of Mikania and of Ageratina fastigiata, Litothamnus nitidus, and Stevia collina, all belonging to tribe Eupatorieae (Asteraceae). We analyzed the structure and content of the assembled plastomes and used the newly generated sequences to infer phylogenetic relationships and study the effects of different data partitions and inference methods on the topologies. Most phylogenetic studies with plastomes ignore that processes like recombination and biparental inheritance can occur in this organelle, using the whole genome as a single locus. Our study sought to compare this approach with multispecies coalescent methods that assume that different parts of the genome evolve at different rates. We found that the overall gene content, structure, and orientation are very conserved in all plastomes of the studied species. As observed in other Asteraceae, the 22 plastomes assembled here contain two nested inversions in the LSC region. The plastomes show similar length and the same gene content. The two most variable regions within Mikania are rpl32-ndhF and rpl16-rps3, while the three genes with the highest percentage of variable sites are ycf1, rpoA, and psbT. We generated six phylogenetic trees using concatenated maximum likelihood and multispecies coalescent methods and three data partitions: coding and non-coding sequences and both combined. All trees strongly support that the sampled Mikania species form a monophyletic group, which is further subdivided into three clades. The internal relationships within each clade are sensitive to the data partitioning and inference methods employed. The trees resulting from concatenated analysis are more similar among each other than to the correspondent tree generated with the same data partition but a different method. The multispecies coalescent analysis indicate a high level of incongruence between species and gene trees. The lack of resolution and congruence among trees can be explained by the sparse sampling (~ 0.45% of the currently accepted species) and by the low number of informative characters present in the sequences. Our study sheds light into the impact of data partitioning and methods over phylogenetic resolution and brings relevant information for the study of Mikania diversity and evolution, as well as for the Asteraceae family as a whole.

Angiosperms at the edge: Extremity, diversity, and phylogeny.

A hallmark of flowering plants is their ability to invade some of the most extreme and dynamic habitats, including cold and dry biomes, to a far greater extent than other land plants. Recent work has provided insight to the phylogenetic distribution and evolutionary mechanisms which have enabled this success, yet needed is a synthesis of evolutionary perspectives with plant physiological traits, morphology, and genomic diversity. Linking these disparate components will not only lead to better understand the evolutionary parallelism and diversification of plants with these two strategies, but also to provide the framework needed for directing future research. We summarize the primary physiological and structural traits involved in response to cold- and drought stress, outline the phylogenetic distribution of these adaptations, and describe the recurring association of these changes with rapid diversification events that occurred in multiple lineages over the past 15 million years. Across these threefold facets of dry-cold correlation (traits, phylogeny, and time) we stress the contrast between (a) the amazing diversity of solutions flowering plants have developed in the face of extreme environments and (b) a broad correlation between cold and dry adaptations that in some cases may hint at deep common origins.

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.

Phylogenomics Yields New Insight Into Relationships Within Vernonieae (Asteraceae).

Asteraceae, or the sunflower family, is the largest family of flowering plants and is usually considered difficult to work with, not only due to its size, but also because of the abundant cases of polyploidy and ancient whole-genome duplications. Traditional molecular systematics studies were often impaired by the low levels of variation found in chloroplast markers and the high paralogy of traditional nuclear markers like ITS. Next-generation sequencing and novel phylogenomics methods, such as target capture and Hyb-Seq, have provided new ways of studying the phylogeny of the family with great success. While the resolution of the backbone of the family is in progress with some results already published, smaller studies focusing on internal clades of the phylogeny are important to increase sampling and allow morphological, biogeography, and diversification analyses, as well as serving as basis to test the current infrafamilial classification. Vernonieae is one of the largest tribes in the family, accounting for approximately 1,500 species. From the 1970s to the 1990s, the tribe went through several reappraisals, mainly due to the splitting of the mega genus Vernonia into several smaller segregates. Only three phylogenetic studies focusing on the Vernonieae have been published to date, both using a few molecular markers, overall presenting low resolution and support in deepest nodes, and presenting conflicting topologies when compared. In this study, we present the first attempt at studying the phylogeny of Vernonieae using phylogenomics. Even though our sampling includes only around 4% of the diversity of the tribe, we achieved complete resolution of the phylogeny with high support recovering approximately 700 nuclear markers obtained through target capture. We also analyzed the effect of missing data using two different matrices with different number of markers and the difference between concatenated and gene tree analysis.

A fully resolved backbone phylogeny reveals numerous dispersals and explosive diversifications throughout the history of Asteraceae.

The sunflower family, Asteraceae, comprises 10% of all flowering plant species and displays an incredible diversity of form. Asteraceae are clearly monophyletic, yet resolving phylogenetic relationships within the family has proven difficult, hindering our ability to understand its origin and diversification. Recent molecular clock dating has suggested a Cretaceous origin, but the lack of deep sampling of many genes and representative taxa from across the family has impeded the resolution of migration routes and diversifications that led to its global distribution and tremendous diversity. Here we use genomic data from 256 terminals to estimate evolutionary relationships, timing of diversification(s), and biogeographic patterns. Our study places the origin of Asteraceae at ∼83 MYA in the late Cretaceous and reveals that the family underwent a series of explosive radiations during the Eocene which were accompanied by accelerations in diversification rates. The lineages that gave rise to nearly 95% of extant species originated and began diversifying during the middle Eocene, coincident with the ensuing marked cooling during this period. Phylogenetic and biogeographic analyses support a South American origin of the family with subsequent dispersals into North America and then to Asia and Africa, later followed by multiple worldwide dispersals in many directions. The rapid mid-Eocene diversification is aligned with the biogeographic range shift to Africa where many of the modern-day tribes appear to have originated. Our robust phylogeny provides a framework for future studies aimed at understanding the role of the macroevolutionary patterns and processes that generated the enormous species diversity of Asteraceae.