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.

The innovation of the symbiosome has enhanced the evolutionary stability of nitrogen fixation in legumes.

Nitrogen-fixing symbiosis is globally important in ecosystem functioning and agriculture, yet the evolutionary history of nodulation remains the focus of considerable debate. Recent evidence suggesting a single origin of nodulation followed by massive parallel evolutionary losses raises questions about why a few lineages in the N2 -fixing clade retained nodulation and diversified as stable nodulators, while most did not. Within legumes, nodulation is restricted to the two most diverse subfamilies, Papilionoideae and Caesalpinioideae, which show stable retention of nodulation across their core clades. We characterize two nodule anatomy types across 128 species in 56 of the 152 genera of the legume subfamily Caesalpinioideae: fixation thread nodules (FTs), where nitrogen-fixing bacteroids are retained within the apoplast in modified infection threads, and symbiosomes, where rhizobia are symplastically internalized in the host cell cytoplasm within membrane-bound symbiosomes (SYMs). Using a robust phylogenomic tree based on 997 genes from 147 Caesalpinioideae genera, we show that losses of nodulation are more prevalent in lineages with FTs than those with SYMs. We propose that evolution of the symbiosome allows for a more intimate and enduring symbiosis through tighter compartmentalization of their rhizobial microsymbionts, resulting in greater evolutionary stability of nodulation across this species-rich pantropical legume clade.

Disintegration of the genus Prosopis L. (Leguminosae, Caesalpinioideae, mimosoid clade).

Robust evidence from phylogenomic analyses of 997 nuclear genes has recently shown, beyond doubt, that the genus Prosopis is polyphyletic with three separate lineages, each with affinities to other genera of mimosoids: (i) Prosopisafricana is an isolated lineage placed in the grade of Plathymenia, Newtonia and Fillaeopsis that subtends the core mimosoid clade; (ii) the remaining Old World species of Prosopis form a clade that is sister to the Indo-Nepalese monospecific genus Indopiptadenia and (iii) New World Prosopis has the Namibian / Namaqualand monospecific endemic genus Xerocladia nested within it. This means that it is now clear that maintaining the unity of the genus Prosopis sensu Burkart (1976) is no longer tenable. These three distinct lineages of Prosopis species correspond directly to Burkart's (1976) sectional classification of the genus, to previously recognised genera and to the differences in types of armature that underpin Burkart's sections. Here, we address this non-monophyly by resurrecting three segregate genera - Anonychium, Neltuma and Strombocarpa and provide 57 new name combinations where necessary, while maintaining the morphologically distinctive and geographically isolated genera Xerocladia and Indopiptadenia. The genus Prosopis itself is reduced to just three species and an emended description is presented. The impacts of these name changes for a genus of such high ecological and human use importance are discussed. These impacts are mitigated by clear differences in armature which facilitate identification and by potential benefits from the deeper biological understanding brought about by recognition of these divergent lineages at generic rank. We provide an identification key to genera and present a map showing the distributions of the segregate genera, as well as drawings and photos illustrating variation in armature and fruits.

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.

Re-establishment of the genus Pseudalbizzia (Leguminosae, Caesalpinioideae, mimosoid clade): the New World species formerly placed in Albizia.

Following recent mimosoid phylogenetic and phylogenomic studies demonstrating the non-monophyly of the genus Albizia, we present a new molecular phylogeny focused on the neotropical species in the genus, with much denser taxon sampling than previous studies. Our aims were to test the monophyly of the neotropical section Arthrosamanea, resolve species relationships, and gain insights into the evolution of fruit morphology. We perform a Bayesian phylogenetic analysis of sequences of nuclear internal and external transcribed spacer regions and trace the evolution of fruit dehiscence and lomentiform pods. Our results find further support for the non-monophyly of the genus Albizia, and confirm the previously proposed segregation of Hesperalbizia, Hydrochorea, Balizia and Pseudosamanea. All species that were sampled from section Arthrosamanea form a clade that is sister to a clade composed of Jupunba, Punjuba, Balizia and Hydrochorea. We find that lomentiform fruits are independently derived from indehiscent septate fruits in both Hydrochorea and section Arthrosamanea. Our results show that morphological adaptations to hydrochory, associated with shifts into seasonally flooded habitats, have occurred several times independently in different geographic areas and different lineages within the ingoid clade. This suggests that environmental conditions have likely played a key role in the evolution of fruit types in Albizia and related genera. We resurrect the name Pseudalbizzia to accommodate the species of section Arthrosamanea, except for two species that were not sampled here but have been shown in other studies to be more closely related to other ingoid genera and we restrict the name Albizia s.s. to the species from Africa, Madagascar, Asia, Australia, and the Pacific. Twenty-one new nomenclatural combinations in Pseudalbizzia are proposed, including 16 species and 5 infraspecific varietal names. In addition to the type species Pseudalbizziaberteroana, the genus has 17 species distributed across tropical regions of the Americas, including the Caribbean. Finally, a new infrageneric classification into five sections is proposed and a distribution map of the species of Pseudalbizzia is presented.

Re-circumscription of the mimosoid genus Entada including new combinations for all species of the phylogenetically nested Elephantorrhiza (Leguminosae, Caesalpinioideae, mimosoid clade).

Recent phylogenomic analyses of 997 nuclear genes support the long-held view that the genus Entada is congeneric with Elephantorrhiza. Entada is resolved as monophyletic only if the genus Elephantorrhiza is subsumed within it. The two genera were distinguished solely by relatively minor differences in the mode of dehiscence of the fruits (a craspedium separating into one-seeded endocarp segments in Entada versus a craspedium with the whole fruit valve breaking away from the persistent replum in Elephantorrhiza) and the craspedial fruit type itself provides a shared synapomorphy for the re-circumscribed Entada. Here, we provide a synopsis of Entada, including 11 new combinations in total, for the eight species, one subspecies and one variety previously placed in Elephantorrhiza, as well as a new combination for a subspecies of Entadarheedei Spreng. not previously dealt with when Entadapursaetha DC. was placed in synonymy. These new combinations are: Entadaburkei (Benth.) S.A. O'Donnell & G.P. Lewis, comb. nov.; Entadaelephantina (Burch.) S.A. O'Donnell & G.P. Lewis, comb. nov.; Entadagoetzei (Harms) S.A. O'Donnell & G.P. Lewis, comb. nov.; Entadagoetzeisubsp.lata (Brenan & Brummitt) S.A. O'Donnell & G.P. Lewis, comb. nov.; Entadaobliqua (Burtt Davy) S.A. O'Donnell & G.P. Lewis, comb. nov.; Entadapraetermissa (J.H. Ross) S.A. O'Donnell & G.P. Lewis, comb. nov.; Entadarangei (Harms) S.A. O'Donnell & G.P. Lewis, comb. nov.; Entadarheedeisubsp.sinohimalensis (Grierson & D.G. Long) S.A. O'Donnell & G.P. Lewis, comb. nov.; Entadaschinziana (Dinter) S.A. O'Donnell & G.P. Lewis, comb. nov.; Entadawoodii (E. Phillips) S.A. O'Donnell & G.P. Lewis, comb. nov.; and Entadawoodiivar.pubescens (E. Phillips) S.A. O'Donnell & G.P. Lewis, comb. nov. We provide a revised circumscription of the genus Entada which now comprises 40 species distributed pantropically, with the greatest diversity of species in tropical Africa. We present a complete taxonomic synopsis, including a map showing the global distribution of the genus and photographs showing variation amongst species in habit, foliage, flowers and fruits. A short discussion about extrafloral nectaries, mainly observed in the Madagascan species, is presented.

Phylogenomic assessment prompts recognition of the Serianthes clade and confirms the monophyly of Serianthes and its relationship with Falcataria and Wallaceodendron in the wider ingoid clade (Leguminosae, Caesalpinioideae).

The Indo-Pacific legume genus Serianthes was recently placed in the Archidendron clade (sensu Koenen et al. 2020), a subclade of the mimosoid clade in subfamily Caesalpinioideae, which also includes Acacia, Archidendron, Archidendropsis, Falcataria, Pararchidendron, Paraserianthes and Wallaceodendron. Serianthes comprises ca. 18 species, five subspecies and two varieties that are characterised by bipinnately compound leaves with alternate sessile leaflets, branched axillary corymbiform panicles and woody indehiscent pods. Generic relationships, as well as species relationships within genera in the Archidendron clade, remain uncertain. While the sister relationship between Serianthes and the genus Falcataria is strongly supported by molecular data, the distinction between Serianthes and the monotypic genus Wallaceodendron has been questioned, based on their similar flower and fruit morphologies. We combined three gene-enriched hybrid capture DNA sequence datasets (generated from the 964 mimobaits v1 probe set, the expanded 997 mimobaits v2 probe set and the GoFlag angiosperm 408 probe set) and used their overlapping markers (77 loci of the target exonic and flanking regions) to test the monophyly of Serianthes and to investigate generic relationships within the Archidendron clade using 55 ingoid plus two outgroup taxa. We show that Serianthes is monophyletic, confirm the Serianthes + Falcataria sister relationship to Wallaceodendron and recognise this combined clade as the Serianthes clade within the Archidendron clade. We also evaluated the use of overlapping loci across datasets in combination with concordance analyses to test generic relationships and further investigate previously unresolved relationships across the wider ingoid clade. Concordance analysis revealed limited gene tree conflicts near the tips of the Archidendron clade, but increased discordance at the base of the clade, which could be attributed to rapid lineage divergence (radiation) and/or incomplete lineage sorting.

Dilemmas in generic delimitation of Senegalia and allies (Caesalpinioideae, mimosoid clade): how to reconcile phylogenomic evidence with morphology and taxonomy?

Senegalia comprises 219 species distributed in tropical and subtropical regions of North and South America, Africa, Asia and Australia. Two sections are currently recognised within Senegalia and these are most readily distinguished by the differences in disposition of their cauline prickles, i.e. sect. Senegalia with prickles at or near leaf nodes and sect. Monacanthea with mostly internodal prickles. Previous phylogenetic studies, based primarily on small numbers of plastid DNA loci, found Senegalia to be monophyletic with two large subclades corresponding to the sections. Here, we present new phylogenomic evidence from 997 single-copy nuclear gene sequences for a small, but representative set of species. These new analyses show that Senegalia is non-monophyletic, but instead, forms a grade that is paraphyletic with respect to the remainder of the ingoid clade (i.e. Ingeae + Acacia s.s. + Acaciella), comprising two well-supported subclades most likely representing the same clades as found in previous phylogenetic studies of the genus and, interspersed between these, a third, moderately supported clade, comprising the genera Mariosousa, Pseudosenegalia and Parasenegalia. In marked contrast to the nuclear phylogeny, the two Senegalia clades are sister groups in the plastid phylogeny, based on analyses of 72 chloroplast genes, rendering the genus monophyletic, based on plastid data alone. We discuss this new evidence that Senegalia is non-monophyletic in relation to the marked cytonuclear discordance, high gene tree conflict and lack of resolution across this senegalioid grade and review the consistency of the key morphological characters distinguishing the two sections of Senegalia. We conclude that it is likely that Senegalia will need to be split into two (or possibly more) genera: a re-circumscribed Senegalia s.s. that corresponds to the existing Senegaliasect.Senegalia plus the S.ataxacantha group (Senegaliasect.Monacanthea s.s.; future studies may show that this group warrants generic status) and a new genus corresponding to the remainder of sect. Monacanthea (here designated as Senegaliasect.Monacanthea p.p.). However, re-delimiting Senegalia now would be premature given that the key morphological characters are not fully congruent with the two sections and pending denser phylogenetic sampling of taxa. A judiciously selected list of critical taxa is presented to facilitate future phylogenomic studies. Finally, we discuss the identity of Albizialeonardii, which is also placed in this senegalioid grade in these new phylogenomic analyses and place it in synonymy with Parasenegaliavogeliana.

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.

Global Succulent Biome phylogenetic conservatism across the pantropical Caesalpinia Group (Leguminosae).

The extent to which phylogenetic biome conservatism vs biome shifting determines global patterns of biodiversity remains poorly understood. To address this question, we investigated the biogeography and trajectories of biome and growth form evolution across the Caesalpinia Group (Leguminosae), a clade of 225 species of trees, shrubs and lianas distributed across the Rainforest, Succulent, Temperate and Savanna Biomes. We focused especially on the little-known Succulent Biome, an assemblage of succulent-rich, grass-poor, seasonally dry tropical vegetation distributed disjunctly across the Neotropics, Africa, Arabia and Madagascar. We reconstructed a time-calibrated phylogeny, assembled species occurrence data and assigned species to areas, biomes and growth forms. These data are used to estimate the frequency of transcontinental disjunctions, biome shifts and evolutionary transitions between growth forms and test for phylogenetic biome conservatism and correlated evolution of growth forms and biome shifts. We uncovered a pattern of strong phylogenetic Succulent Biome conservatism. We showed that transcontinental disjunctions confined within the Succulent Biome are frequent and that biome shifts to the Savanna, Rainforest and Temperate Biomes are infrequent and closely associated with shifts in plant growth forms. Our results suggest that the Succulent Biome comprises an ecologically constrained evolutionary arena spanning large geographical disjunctions across the tropics.