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

Abstract

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

“…Additionally, Brenan (1966Brenan ( , 1986 noted that the epicarp of Adenopodia pods remains attached to the endocarp, whereas these structures separate in the mature pods of Entada. In their review of the genera of tribe Mimoseae, Lewis and Elias (1981) used this suite of characters to argue for a more parsimonious placement of Adenopodia within the informal Piptadenia group of genera. This placement of Adenopodia, separate from Entada in the Piptadenia-containing Mimosa clade (sensu Koenen et al 2020), is supported by recent large-scale phylogenomic analyses (Koenen et al 2020;Ringelberg et al 2022). In that same review of Mimoseae genera, Lewis and Elias (1981) highlighted the close affinity between Entada and Elephantorrhiza Benth., an essentially southern African genus of eight species of geoxylic suffrutices, shrubs or small trees and placed them in their informal Entada group.…”

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 Stryphnodendron and Mimosa clades, taxa from which were used to root trees in this study, are highlighted in orange and purple, respectively and indicated with an asterisk. phylogenetic and phylogenomic analyses until recently (Brown et al 2022;Ringelberg et al 2022). Recent efforts to resolve phylogenetic relationships within the species-rich Archidendron clade have been hampered by a paucity of molecular data or incomplete taxon sampling in previous studies (Brown et al 2008;Brown et al 2011;Koenen et al 2020).…”

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

“…We show that sect. Arthrosamanea, with expanded taxon sampling relative to Koenen et al (2020), and as also shown by the study of Ringelberg et al (2022), is monophyletic with only two exceptions: Albizia leonardii Barneby & J.W. Grimes which is placed among taxa of the 'senegalioid grade' (Ringelberg et al 2022;Terra et al 2022) and Albizia carbonaria Britton that is more closely related to Pseudosamanea (Koenen 2022b;Ringelberg et al 2022).…”

“…Finally, neither Zygia P. Browne nor Marmaroxylon Killip are monophyletic, although a new generic classification for those genera has yet to be proposed (Ferm et al 2019). The non-monophyly of Albizia documented here and elsewhere (Koenen et al 2020;Ringelberg et al 2022) is thus not a surprise and reflects the state of flux surrounding generic delimitation in mimosoids, especially within the ingoid clade. Some of the taxonomic proposals of Barneby and Grimes (1996) relative to the American segregates of Albizia s.l.…”