Advances in Legume Systematics 14. Classification of Caesalpinioideae. Part 2: Higher-level classification.

Caesalpinioideae is the second largest subfamily of legumes (Leguminosae) with ca. 4680 species and 163 genera. It is an ecologically and economically important group formed of mostly woody perennials that range from large canopy emergent trees to functionally herbaceous geoxyles, lianas and shrubs, and which has a global distribution, occurring on every continent except Antarctica. Following the recent re-circumscription of 15 Caesalpinioideae genera as presented in Advances in Legume Systematics 14, Part 1, and using as a basis a phylogenomic analysis of 997 nuclear gene sequences for 420 species and all but five of the genera currently recognised in the subfamily, we present a new higher-level classification for the subfamily. The new classification of Caesalpinioideae comprises eleven tribes, all of which are either new, reinstated or re-circumscribed at this rank: Caesalpinieae Rchb. (27 genera / ca. 223 species), Campsiandreae LPWG (2 / 5-22), Cassieae Bronn (7 / 695), Ceratonieae Rchb. (4 / 6), Dimorphandreae Benth. (4 / 35), Erythrophleeae LPWG (2 /13), Gleditsieae Nakai (3 / 20), Mimoseae Bronn (100 / ca. 3510), Pterogyneae LPWG (1 / 1), Schizolobieae Nakai (8 / 42-43), Sclerolobieae Benth. & Hook. f. (5 / ca. 113). Although many of these lineages have been recognised and named in the past, either as tribes or informal generic groups, their circumscriptions have varied widely and changed over the past decades, such that all the tribes described here differ in generic membership from those previously recognised. Importantly, the approximately 3500 species and 100 genera of the former subfamily Mimosoideae are now placed in the reinstated, but newly circumscribed, tribe Mimoseae. Because of the large size and ecological importance of the tribe, we also provide a clade-based classification system for Mimoseae that includes 17 named lower-level clades. Fourteen of the 100 Mimoseae genera remain unplaced in these lower-level clades: eight are resolved in two grades and six are phylogenetically isolated monogeneric lineages. In addition to the new classification, we provide a key to genera, morphological descriptions and notes for all 163 genera, all tribes, and all named clades. The diversity of growth forms, foliage, flowers and fruits are illustrated for all genera, and for each genus we also provide a distribution map, based on quality-controlled herbarium specimen localities. A glossary for specialised terms used in legume morphology is provided. This new phylogenetically based classification of Caesalpinioideae provides a solid system for communication and a framework for downstream analyses of biogeography, trait evolution and diversification, as well as for taxonomic revision of still understudied genera.

Precipitation is the main axis of tropical plant phylogenetic turnover across space and time.

Early natural historians-Comte de Buffon, von Humboldt, and De Candolle-established environment and geography as two principal axes determining the distribution of groups of organisms, laying the foundations for biogeography over the subsequent 200 years, yet the relative importance of these two axes remains unresolved. Leveraging phylogenomic and global species distribution data for Mimosoid legumes, a pantropical plant clade of c. 3500 species, we show that the water availability gradient from deserts to rain forests dictates turnover of lineages within continents across the tropics. We demonstrate that 95% of speciation occurs within a precipitation niche, showing profound phylogenetic niche conservatism, and that lineage turnover boundaries coincide with isohyets of precipitation. We reveal similar patterns on different continents, implying that evolution and dispersal follow universal processes.

Phylogenomic analysis of 997 nuclear genes reveals the need for extensive generic re-delimitation in Caesalpinioideae (Leguminosae).

Subfamily Caesalpinioideae with ca. 4,600 species in 152 genera is the second-largest subfamily of legumes (Leguminosae) and forms an ecologically and economically important group of trees, shrubs and lianas with a pantropical distribution. Despite major advances in the last few decades towards aligning genera with clades across Caesalpinioideae, generic delimitation remains in a state of considerable flux, especially across the mimosoid clade. We test the monophyly of genera across Caesalpinioideae via phylogenomic analysis of 997 nuclear genes sequenced via targeted enrichment (Hybseq) for 420 species and 147 of the 152 genera currently recognised in the subfamily. We show that 22 genera are non-monophyletic or nested in other genera and that non-monophyly is concentrated in the mimosoid clade where ca. 25% of the 90 genera are found to be non-monophyletic. We suggest two main reasons for this pervasive generic non-monophyly: (i) extensive morphological homoplasy that we document here for a handful of important traits and, particularly, the repeated evolution of distinctive fruit types that were historically emphasised in delimiting genera and (ii) this is an artefact of the lack of pantropical taxonomic syntheses and sampling in previous phylogenies and the consequent failure to identify clades that span the Old World and New World or conversely amphi-Atlantic genera that are non-monophyletic, both of which are critical for delimiting genera across this large pantropical clade. Finally, we discuss taxon delimitation in the phylogenomic era and especially how assessing patterns of gene tree conflict can provide additional insights into generic delimitation. This new phylogenomic framework provides the foundations for a series of papers reclassifying genera that are presented here in Advances in Legume Systematics (ALS) 14 Part 1, for establishing a new higher-level phylogenetic tribal and clade-based classification of Caesalpinioideae that is the focus of ALS14 Part 2 and for downstream analyses of evolutionary diversification and biogeography of this important group of legumes which are presented elsewhere.

Mezcala - a new segregate genus of mimosoid legume (Leguminosae, Caesalpinioideae, mimosoid clade) narrowly endemic to the Balsas Depression in Mexico.

Recent results have demonstrated that the genus Desmanthus is non-monophyletic because the genus Kanaloa is nested within it, with a single species, Desmanthusbalsensis placed as sister to the clade comprising Kanaloa plus the remaining species of Desmanthus. Here we transfer D.balsensis to a new segregate genus Mezcala, discuss the morphological features supporting this new genus, present a key to distinguish Mezcala from closely related genera in the Leucaena subclade, and provide a distribution map of M.balsensis.

Hybrid capture of 964 nuclear genes resolves evolutionary relationships in the mimosoid legumes and reveals the polytomous origins of a large pantropical radiation.

PREMISE: Targeted enrichment methods facilitate sequencing of hundreds of nuclear loci to enhance phylogenetic resolution and elucidate why some parts of the "tree of life" are difficult (if not impossible) to resolve. The mimosoid legumes are a prominent pantropical clade of ~3300 species of woody angiosperms for which previous phylogenies have shown extensive lack of resolution, especially among the species-rich and taxonomically challenging ingoids. METHODS: We generated transcriptomes to select low-copy nuclear genes, enrich these via hybrid capture for representative species of most mimosoid genera, and analyze the resulting data using de novo assembly and various phylogenomic tools for species tree inference. We also evaluate gene tree support and conflict for key internodes and use phylogenetic network analysis to investigate phylogenetic signal across the ingoids. RESULTS: Our selection of 964 nuclear genes greatly improves phylogenetic resolution across the mimosoid phylogeny and shows that the ingoid clade can be resolved into several well-supported clades. However, nearly all loci show lack of phylogenetic signal for some of the deeper internodes within the ingoids. CONCLUSIONS: Lack of resolution in the ingoid clade is most likely the result of hyperfast diversification, potentially causing a hard polytomy of six or seven lineages. The gene set for targeted sequencing presented here offers great potential to further enhance the phylogeny of mimosoids and the wider Caesalpinioideae with denser taxon sampling, to provide a framework for taxonomic reclassification, and to study the ingoid radiation.

Locating evolutionary precursors on a phylogenetic tree.

Conspicuous innovations in the history of life are often preceded by more cryptic genetic and developmental precursors. In many cases, these appear to be associated with recurring origins of very similar traits in close relatives (parallelisms) or striking convergences separated by deep time (deep homologies). Although the phylogenetic distribution of gain and loss of traits hints strongly at the existence of such precursors, no models of trait evolution currently permit inference about their location on a tree. Here we develop a new stochastic model, which explicitly captures the dependency implied by a precursor and permits estimation of precursor locations. We apply it to the evolution of extrafloral nectaries (EFNs), an ecologically significant trait mediating a widespread mutualism between plants and ants. In legumes, a species-rich clade with morphologically diverse EFNs, the precursor model fits the data on EFN occurrences significantly better than conventional models. The model generates explicit hypotheses about the phylogenetic location of hypothetical precursors, which may help guide future studies of molecular genetic pathways underlying nectary position, development, and function.

Placing the woody tropical genera of Polygonaceae: A hypothesis of character evolution and phylogeny.

PREMISE OF THE STUDY: Taxonomic groups have often been recognized on the basis of geographic distinctions rather than accurately representing evolutionary relationships. This has been particularly true for temperate and tropical members from the same family. Polygonaceae exemplifies this problem, wherein the woody tropical genera were segregated from temperate members of the family and placed in the subfamily Polygonoideae as two tribes: Triplarideae and Coccolobeae. Modern phylogenetic studies, especially when inferred from many lines of evidence, can elucidate more probable hypotheses of relationships. This study builds on previous work in the family and aims to test the traditional classification of the tropical woody taxa, which have been understudied and undersampled compared to their temperate relatives. • METHODS: A phylogenetic study was undertaken with expanded sampling of the tropical genera with data from five plastid markers (psbA-trnH, psaI-accD, matK, ndhF, and rbcL), nuclear ribosomal DNA (ITS) and morphology. • KEY RESULTS: Results support the placement of nine of 12 genera of the Triplarideae and Coccolobeae within Eriogonoideae, in which these genera form a paraphyletic assemblage giving rise to Eriogoneae. The remaining woody tropical genera excluded from Eriogonoideae occur in the paleotropics. • CONCLUSIONS: Traditional characters used to delimit Coccolobeae and Triplarideae are not useful for defining monophyletic groups. The six-tepal condition is derived from the five-tepal condition, and unisexual flowers have arisen multiple times in different sexual systems. Ruminate endosperm has arisen multiple times in the family, suggesting this character is highly plastic.

Development of nuclear gene-derived molecular markers linked to legume genetic maps.

The systematic identification of the orthologous features of related organisms greatly facilitates comparative genomics, including research on genome evolution and comparative genetic mapping. In this study, we selected 274 unique gene sequences for the development of PCR-based genetic markers across fifteen legume genomes, representing six crop or model legume species from the phaseoloid and inverted repeat loss clades (IRLC). DNA sequence analysis demonstrated that 129 of the amplified fragments represented single copy loci across most target diploid genomes. The majority of these markers are intron-spanning (70.5%) and linked to legume genetic maps (85.3%). The markers were grouped into four main categories: (1) intron-spanning relatively conserved, (2) intron-spanning diverged, (3) exon-derived conserved, and (4) exon-derived diverged. The extent of sequence divergence within each category indicates that the corresponding markers may have utility for assessing phylogenetic relationships at different, but overlapping, taxonomic levels. We tested marker performance on genomes that had not been previously sampled, representing 95 different species that span the diversity of the Fabaceae. Phylogenetic analyses support the orthology of amplified sequences, with the notable exception of an ambiguous affiliation of Lotus relative to the IRLC and phaseoloid clades.

Circularity and Independence in Phylogenetic Tests of Ecological Hypotheses.

It has been asserted that in order to avoid circularity in phylogenetic tests of ecological hypotheses, one must exclude from the cladistic analysis any characters that might be correlated with that hypothesis. The argument assumes that selective correlation leads to lack of independence among characters and may thus bias the analysis. This argument conflates the idea of independence between the ecological hypothesis and the phylogeny with independence among characters used to construct the tree. We argue that adaptation or selection does not necessarily result in the non-independence of characters, and that characters for a cladistic analysis should be evaluated as homology statements rather than functional ones. As with any partitioning of data, character exclusion may lead to weaker phylogenetic hypotheses, and the practice of mapping characters onto a tree, rather than including them in the analysis, should be avoided. Examples from pollination biology are used to illustrate some of the theoretical and practical problems inherent in character exclusion.

CHROMOSOME STUDIES IN ASTERACEAE FROM THE UNITED STATES, MEXICO, THE WEST INDIES, AND SOUTH AMERICA.

Chromosome counts of Asteraceae are reported from Mexico, the United States, the West Indies, Peru, and Bolivia. First counts are reported for 27 species, eight infraspecific taxa, and three interspecific hybrids in Brickellia, Chrysanthellum, Cirsium, Egletes, Erigeron, Flaveria, Gnaphalium, Heterotheca, Hieracium, Hymenothrix, Koanophyllon, Layia, Lessingia, Pectis, Sclerocarpus, Stuessya, Tagetes and Wedelia. Counts are also reported for 196 taxa or hybrids for which chromosome numbers have been published previously. Of these, nine are new numbers. Taxonomic implications of certain counts are discussed.

AN EMPIRICAL COMPARISON OF NUMERICAL WAGNER COMPUTER PROGRAMS.

Abstract- The performance of four computer programs that calculate Wagner trees (WAGNER 78, WAGPROC, PHYLIP, and PHYSYS) was compared for twenty-five data sets. Eight combinations of algorithms and options were tried, including different methods of adding taxa, optimizing stem states, obtaining multiple trees, and branch swapping. Using the criterion of finding a minimum length tree, PHYSYS with the WAG.S option performed best, providing the shortest tree for twenty-four of the twenty-five data sets. WAGPROC with the GLOB option found sixteen minima for eighteen data sets, exceeding run time on the remaining seven. All other algorithm/options were less successful in providing minimum trees. In comparing the options we found that minimum homoplasy is not completely reliable in optimizing trees and that the brute force algorithm is helpful but not required for finding minimum trees. The advancement index criterion for adding taxa to a tree is more effective than adding taxa in their data file sequence. The success of the PHYSYS WAG.S option and the WAGPROC GLOB demonstrate that both multiple trees and branch swapping are necessary to produce a minimum length tree.