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Research Article
Boliviadendron, a new segregate genus of mimosoid legume (Leguminosae, Caesalpinioideae, mimosoid clade) narrowly endemic to the interior Andean valleys of Bolivia
expand article infoÉlvia Rodrigues de Souza, Priscilla Gomes C. de Almeida, Lamarck Rocha, Erik J.M. Koenen§|, Margoth Atahuachi Burgos, Gwilym P. Lewis#, Colin E. Hughes§
‡ Universidade Estadual de Feira de Santana, Feira de Santana, Brazil
§ University of Zurich, Zürich, Switzerland
| Université Libre de Bruxelles, Bruxelles, Belgium
¶ Universidad Mayor de San Simón, Cochabamba, Bolivia
# Royal Botanic Gardens, Kew, Richmond, United Kingdom
Open Access

Abstract

Phylogenetic analyses of DNA sequence data sampling all species of Leucochloron alongside representatives of genera of the Inga and Albizia clades of the larger ingoid clade of mimosoid legumes (sensu Koenen et al. 2020) confirm the non-monophyly of the genus Leucochloron. We show that Leucochloron bolivianum is placed in the Albizia clade, while the remaining four species of Leucochloron are placed in the Inga clade, in line with previous results. To rectify this non-monophyly, L. bolivianum is segregated as the new genus, Boliviadendron, with a single species, Boliviadendron bolivianum, narrowly endemic to the interior Andean valleys of Bolivia. We illustrate this new segregate genus, present a map of its distribution and discuss the striking lack of morphological distinctions between Boliviadendron and Leucochloron, as well as the phylogenetic and morphological affinities of Boliviadendron to the genera Enterolobium and Albizia.

Keywords

Fabaceae, generic delimitation, Leucochloron, monophyly, taxonomy

Introduction

The genus Leucochloron Barneby & J.W. Grimes was established by Barneby and Grimes (1996) as part of their generic system for the mimosoid legume tribe Ingeae in the New World, with four species, all of them native to Brazil: L. incuriale (Vell.) Barneby & J.W. Grimes, L. limae Barneby & J.W. Grimes, L. minarum (Glaz. ex Harms) Barneby & J.W. Grimes and L. foederale (Barneby & J.W. Grimes) Barneby & J.W. Grimes. Barneby and Grimes (1996) based their new genus on the combination of lack of armature, perulate resting buds, homomorphic flowers arranged in globose axillary capitula, broad plano-compressed stiffly papery or weakly coriaceous fruits and shiny discoid exareolate seeds, encircled by a marginal nerve or minute wing.

In May 2002, C.E. Hughes and collaborators collected material of an undescribed mimosoid legume tree from a single locality on the mid-elevation eastern flanks of the Bolivian Andes. A small number of additional collections from nearby localities have been made in subsequent years. This material shares the same combination of characters used by Barneby and Grimes (1996) to delimit Leucochloron and, hence, provided the basis for description of a fifth species, Leucochloron bolivianum C.E. Hughes & Atahuachi (Hughes and Atahuachi (2006, publ. 2007).

This apparently morphologically commodious generic home for Leucochloron bolivianum has been brought into question by phylogenetic evidence from Almeida (2014), LPWG (2017) and more recently generated DNA sequence data for 964 nuclear genes for two species of Leucochloron, L. bolivianum and L. limae, which showed that the genus Leucochloron is non-monophyletic (Koenen et al. 2020). Here, we further test this non-monophyly to ascertain where the remaining three species of Leucochloron are placed phylogenetically in relation to the two separate Leucochloron lineages identified by Koenen et al. (2020), with the aim of providing a solid basis for generic re-delimitation.

Materials and methods

Morpho-taxonomic analyses and sample selection for DNA extraction were based on field collections and herbarium specimens from BOLV, FHO, HUEFS, K, LPB, MBM, MEXU, NY, SP and VIC (acronyms follow Thiers 2022, [continuously updated]) collections and previous taxonomic literature (Hughes and Atahuachi 2006, publ. 2007; Almeida 2014).

We sampled 47 accessions (40 of them newly sequenced here and seven using sequences from GenBank) in 19 genera, including all genera of the Albizia and Inga clades sensu Koenen et al. (2020), except Abarema s.s., plus a representative set of other lineages spanning the ingoid clade (see Suppl. material 1: Table S1, for GenBank accession numbers and voucher information). All five recognised species of Leucochloron were sampled, including seven accessions of Leucochloron bolivianum. Acacia Mill. (i.e. Acacia sensu stricto), which is also a member of the wider ingoid clade, was selected as outgroup.

Total genomic DNA was extracted from silica-dried or herbarium leaf tissue using a modified 2 × CTAB protocol (Doyle and Doyle 1987). DNA samples with low amplification were purified using Sepharose CL-6B (Sigma, St. Louis, Missouri, USA), following the manufacturer’s protocol. We sequenced eight loci which have been used in previous phylogenetic studies of generic relationships in the ingoid clade (e.g., Souza et al. 2013): the nuclear ribosomal 5.8S subunit and flanking ITS1 and ITS2 spacers, the external transcribed spacer ETS and the plastid loci rps16, psbA-trnH, rpL32-trnL, trnL intron, trnL-F and trnD-T (see Suppl. material 1: Table S2 for primer sequences and amplification protocols). The ITS amplifications were performed with primers 17SE and 26SE or primers ITS92 and ITS4. The trnD-T region was amplified in two independent reactions combining primers: trnDguc + trnEuuc and trnYgua + trnTggu (Shaw et al. 2007).

Polymerase Chain Reactions (PCR) were performed using TopTaq Master Mix Kit (QIAGEN GmbH, Hilden, Germany) according to the manufacturer’s protocol, in 10–15 μl of final reaction volume. For the nrITS and ETS amplifications, 1.0 M betaine and 2% DMSO (dimethylsulphoxide; 2% of the preparation volume) were added. PCR products were purified by enzymatic treatments with Exonuclease I and Shrimp alkaline phosphatase (kit ExoSapIT, GE Healthcare Buckinghamshire, U.K.). Sequencing reactions were performed using the same primers used for PCR and Big Dye Terminator kit v.3.1 (Applied Biosystems, Foster City, California, U.S.A.), on the ABI3130XL Analyzer (Applied BioSystems), at the Laboratório de Sistemática Molecular de Plantas (LAMOL), of the Universidade Estadual de Feira de Santana (UEFS), Bahia, Brazil.

Electropherograms were assembled in Geneious 5.3.6 (Drummond et al. 2010) using default assembly settings. Consensus sequences were aligned in MUSCLE (Edgar 2004) using Geneious, with manual adjustments. We analysed three datasets: 1) the combined plastid loci, 2) combined nuclear loci and 3) combined plastid + nuclear loci. Incongruence between datasets was assessed via 1,000 replicates of the Homogeneity of Participation Test (Felsenstein 1985) using PAUP v. 4.0b10 for Windows (Swofford 2002).

Maximum Parsimony (MP) analyses were performed using PAUP v.4.0 (Swofford 2002), using Fitch parsimony (all characters unordered and equally weighted; Fitch 1971), 1,000 replications of taxon addition and resampling by tree bisection-reconnection (TBR) branch swapping, saving up to 15 trees per replication to prevent extensive searches in sub-optimal islands. Trees from the first search were used as a starting point for a second search using the same parameters retaining a maximum of 10,000 trees. Non-parametric bootstrapping (BS; Felsenstein 1985) was used to estimate clade support, assessed through 1,000 replications, simple taxon-addition and the TBR algorithm, saving up to 15 trees per replicate.

Maximum Likelihood (ML) analyses were performed using RAxML v.8 (Stamatakis 2014), on the CIPRES Science Gateway v.3.3 (Miller et al. 2010), using the GTR + CAT evolutionary model and estimating GAMMA distribution during the run. Branch support was evaluated using 1,000 rapid bootstrap replicates.

Best-fitting substitution models for each data partition were selected using the Akaike Information Criterion (AIC) using MrModeltest v.2.3 (Nylander 2004) (Suppl. material 1: Table S2). Bayesian Inference (BI) analysis was performed on MrBayes v.3.2.6 (Ronquist and Huelsenbeck 2003; Ronquist et al. 2012), on the CIPRES Science Gateway v.3.3 (Miller et al. 2010). Two separate runs of a Metropolis-coupled Markov Chain Monte Carlo (MCMC) were initiated with random starting trees and four simultaneous chains set at default temperatures (Ronquist and Huelsenbeck 2003) for 30 million generations, sampling once every 103 generations. Convergence was assessed using Tracer v.1.6 (Rambaut et al. 2014) to ensure effective sample sizes (ESS) ≥ 200. MrBayes was also used to summarise 75% post burn-in trees sampled from a 50% majority rule consensus tree that included posterior probabilities (PP) as branch support estimates. All trees from MP, BI and ML were visualised and edited in FigTree 1.4.4 (Rambaut 2018).

Results

While separate analyses of the nuclear ITS + ETS and plastid loci yielded gene trees that were, in many cases, poorly resolved (Suppl. material 1: Table S3, Suppl. material 2: Figs S1–S4), the combined nuclear + plastid analysis (Fig. 1) is sufficiently resolved to demonstrate that the genus Leucochloron is not monophyletic, with all seven accessions of L. bolivianum forming a robustly supported clade placed in a clade with Albizia Durazz., Enterolobium Mart. and Samanea (Benth.) Merr. and the other four species of Leucochloron forming a robustly supported clade that is placed in a clade with Inga Mill., Zygia P. Browne and Macrosamanea Britton & Rose ex Britton & Killip. (Fig. 1).

Figure 1. 

Majority-rule (50%) consensus tree from Bayesian analysis of the combined nuclear (ITS, ETS) and plastid (psbA-trnH, rpL32, rps16, trnD-T, trnL-F) data for Boliviadendron and related genera. Values above branches are Bayesian Posterior Probabilities (PP), below are Bootstrap Support (BS) percentages from the maximum parsimony (left) and Maximum Likelihood analyses (right). Branches supported by PP ≥ 95% are in bold. Only BS values ≥ 50% are shown; - indicates BS ≤ 50%; * indicates PP = 1.0 or BS = 100%.

Discussion

The non-monophyly of the genus Leucochloron is supported by two independent phylogenetic studies, one presented here sampling all five species currently assigned to the genus, based on a small set of widely-used nrDNA and plastid DNA sequence loci (Fig. 1) and the other sampling just two species, but based on phylogenomic analyses of 964 nuclear gene sequences and a broad sample of genera across the whole mimosoid clade (Koenen et al. 2020). This non-monophyly is further confirmed in a more recent phylogeny constructed using a slightly expanded set of 997 nuclear genes, derived from a modified version of the Mimobaits gene set of Koenen et al. (2020), which sampled all but five of the 151 genera of subfamily Caesalpinioideae (Ringelberg et al. 2022). This thorough sampling of both taxa and genes demonstrates beyond doubt that Leucochloron is indeed non-monophyletic, with L. bolivianum placed in the Albizia clade (sensu Koenen et al. 2020) and the remaining four species of Leucochloron forming a robustly-supported clade in the Inga clade (sensu Koenen et al. 2020; Fig. 1). These results provide strong evidence supporting segregation of L. bolivianum as a new genus, here named Boliviadendron.

This robustly-supported non-monophyly is unexpected, given the close morphological similarities between L. bolivianum and the other four species of Leucochloron. Indeed, there appear to be very few qualitative morphological differences separating Boliviadendron (i.e., L. bolivianum) from Leucochloron, suggesting that the original combination of character states used by Barneby and Grimes (1996) to delimit Leucochloron has essentially been recapitulated in Boliviadendron. These striking morphological similarities between Leucochloron and Boliviadendron must, thus, be viewed as further evidence of the extensive morphological homoplasy evident across mimosoids which has frequently misled generic delimitation (Ringelberg et al. 2022). For example, the presence of minute wing-like rims of seeds, which was one of the characters supporting placement of L. bolivianum in the genus Leucochloron (Hughes and Atahuachi 2006, publ. 2007), have been documented across phylogenetically scattered mimosoid legume lineages, including the genera Mimozyganthus Burkart (Luckow et al. 2005), Archidendropsis I.C. Nielsen and Leucochloron and now here in the phylogenetically distinct lineage Boliviadendron. This suggests that this character, just like seeds with true wings which also occur across a disparate set of unrelated mimosoid genera, is homoplasious and evolutionarily labile.

Morphological characters which weakly separate Boliviadendron from Leucochloron s.s. are: (i) the leaflet base is more evidently asymmetrical in Boliviadendron than in the species of Leucochloron and the under-surface of Boliviadendron leaflets has 1–2 (–3) prominent primary veins, but otherwise the venation is not evident vs. the evident reticulate secondary and tertiary venation on the lower leaflet surface in Leucochloron species; (ii) in Boliviadendron, the upper leaflet surfaces are consistently blotched purple-black, while leaflets of Leucochloron s.s. species are strongly discolorous, with the upper surface drying dark brown and often glossy; (iii) the indumentum in Boliviadendron tends to be shorter and white, especially on the corollas and calyces which have fine white, appressed, silky trichomes vs. the generally more ferruginous and longer indumentum, occasionally with golden and/or white hairs intermixed, of Leucochloron species; (iv) the number of pollen grains per polyad is constant in Boliviadendron at 16 (counted on the isotype Hughes 2423 and Wood 21618 at K), while in Leucochloron s.s., it is variable (even within species) with 16, 18, 24 or 32 grains.

In the Koenen et al. (2020) phylogeny, Boliviadendron appeared as sister to a clade comprising Enterolobium and Albizia s.s. (i.e., Old World Albizia). In the phylogeny presented here, Boliviadendron is also placed in a clade with Enterolobium and Albizia s.s. (Fig. 1) in line with the findings of Koenen et al. (2020). This close relationship of Boliviadendron to Enterolobium is reflected in the closely similar leaf and flower morphologies of these two genera, including the asymmetrically displaced primary vein of the leaflets (which also characterises many species of Albizia s.s.), the blotched purple-black upper leaflet surfaces and superficially very similar globose axillary capitula of homomorphic flowers immersed amongst coevally developing leaves. However, in fruit, these two genera are immediately distinguishable by the characteristically thickened indehiscent curved ‘ear-pod’ fruits of Enterolobium vs. the plano-compressed, inertly dehiscent fruits with chartaceous valves of Boliviadendron. This means that material of Boliviadendron lacking fruits can be difficult to distinguish from Enterolobium. Indeed, one of the collections, cited as L. bolivianum by Hughes and Atahuachi (2006, publ. 2007) (J.R.I. Wood 22134 at K, which has leaves and flowers only), has since been correctly identified as Enterolobium contortisiliquum (Vell.) Morong. Closer examination of the inflorescences of these two taxa, which can occur in close geographical proximity in Bolivia, shows that the flowers of Boliviadendron are essentially sessile, while those of Enterolobium contortisiliquum are pedicellate, on more robust inflorescences. The plano-compressed fruits with stiffly papery chartaceous or weakly coriaceous valves dehiscing inertly along both sutures in Boliviadendron are strongly reminiscent of the fruits of the other closely related genus, Albizia s.s., but the marked lack of a pleurogram on the seeds in Boliviadendron clearly distinguishes the genus from Albizia. It is notable that polyads, like those of Boliviadendron, are also 16-celled in Albizia s.s. (although only few species of the genus have been studied for their pollen characteristics), but can be 16 or 32-celled in Enterolobium.

Taxonomy

Boliviadendron E.R. Souza & C.E. Hughes, gen. nov.

Fig. 2

Type

Boliviadendron bolivianum (C.E. Hughes & Atahuachi) E.R. Souza & C.E. Hughes.

Diagnosis

Boliviadendron is similar in almost all respects to the genus Leucochloron and is segregated first and foremost because these two lineages are phylogenetically not closely related (Fig. 1; Koenen et al. 2020). Boliviadendron differs from Leucochloron in its more evidently asymmetrical leaflet bases, by having just 1–2 (–3) primary veins visible vs. the evident reticulate secondary and tertiary venation on the lower leaflet surface in Leucochloron, by the consistent purple-black blotches on the upper surface of the leaflets (sometimes the whole surface suffused purplish-black, but never glossy) vs. the strongly discolorous leaflets of Leucochloron where the upper surface dries dark brown and is often glossy and finally, by the shorter, white indumentum vs. the more generally ferruginous and longer indumentum of Leucochloron species.

Description

(modified from Hughes and Atahuachi 2006, publ. 2007). Small, unarmed multi-stemmed tree to 5–6 (–10) m tall and 20–35 cm dbh with an irregular spreading crown (Fig. 2A). Outer bark smooth, mid grey-brown, with horizontal lines of lenticels when young (Fig. 2B), becoming thick and corky and vertically fissured with age; inner bark reddish, then cream, gritty. Woody shoots glabrate, lenticellate, dull grey, lenticels round pustulate, the outer bark papery, slightly striate and sometimes slightly exfoliating. Young shoots, leaf stalks and peduncles minutely and sparsely to densely puberulent with whitish or dull golden 0.1– 0.2 mm hairs. Resting buds perulate, ovoid to 1.5 mm long and densely pilosulous (as for shoots), but these generally lacking. Stipules linear-triangular, 3 × 1.7–2 mm, caducous. Leaves bipinnate with 4–5 (–6) pairs of pinnae, leaf stalks canaliculate with two parallel longitudinal ridges, 7–11 cm long, ending in a 2 mm long mucro and including a 2.5–3.6 cm long petiole charged with a 1–1.3 mm diameter circular or weakly ellipsoid sessile or subsessile, thick-rimmed, cupular nectary at or slightly above mid-petiole position; similar smaller nectaries variably present between distal 1–2 pairs of pinnae or sometimes between all pinnae pairs. Longer interpinnal segments 1.3–1.7 cm long, the rachis of longer pinnae 6–8 cm with 15–20 pairs of leaflets per pinna. Leaflets slightly decrescent proximally and distally, larger leaflets 7–10 × 2.1–3.0 (–3.2) mm, not strongly discolorous, nearly glabrous or very sparsely puberulent above, sparsely puberulent below, on small, ridged, transversely elliptic, asymmetric 3 × 0.6 mm pulvinules, the first anterior or first pair of leaflets reduced to 1.2–1.5 mm long paraphyllidia. Leaflets linear-oblong, obliquely truncate at base, obtuse at apex, the tip sometimes acute, venation indistinct, palmate-pinnate brochidodromous, with 1–2 (–weakly 3) primary veins at base, the main primary vein distinctly asymmetric, dividing the blade 1:2–2.5, giving rise on each side to 3–4 sinuous secondary veins, albeit these often indistinct or obscured by the indumentum, venation very faintly immersed or invisible above, the 1–2 (–3) primary veins clearly visible and weakly prominulous below. Flowers sessile, homomorphic and arranged in lax globose capitula (Fig. 2C) on 2.5–3 cm-long slender peduncles, moriform in bud, 12–13 mm in diameter (excluding the filaments), the receptacle 1.3 mm in diameter, each capitulum with 20–25 flowers, whitish-green in bud due to dense silky puberulent indumentum on calyx and corolla. The capitula immersed in new foliage, solitary or in fascicles of 2–3 in axils of coeval leaves. Bracts sessile, short spatulate, 0.2–0.4 mm long, puberulent. Calyx narrowly campanulate, 2.5 mm long, the triangular lobes 0.3–0.4 mm long. Corolla tubular, slightly funnel-shaped, 5–6 mm long, the free lobes 1 mm, slightly reflexed. Androecium of ca. 40 stamens to 10 mm long, fused basally into a 3–4 mm long tube that is not or hardly exserted beyond the corolla. Ovary 0.8 mm long, sessile, the style 2.5 mm, held below anthers of the stamens. Pods (Fig. 2D) 1 per capitulum, sessile, (6–) 7–10 × 1.7–2 (–2.7) cm, (3–) 4–6 (–8)-seeded, flat plano-compressed, linear-oblong or oblong, obtuse at each end, sometimes with a short apiculum at apex, the valves straight or with slightly undulate margins, stiff papery, pale whitish- or yellow-green when unripe, turning dull orange-brown when ripe, obscurely venulose, sparsely and minutely puberulent overall, internally dull stramineous, framed by plain sutures < 1 mm wide, tardily dehiscent along both sutures, opening narrowly to release seeds, the valves remaining attached after dehiscence. Seeds horizontal at middle of pod, flat disciform, broadly suborbicular, 11–13 mm in diameter, < 1 mm thick, the testa thin, lustrous, translucent castaneous, slightly wrinkled when dry, pleurogram lacking, surrounded by a narrow 0.4–0.6 mm dark marginal nerve or minute wing.

Figure 2. 

Boliviadendron bolivianum A habit B bark and slash C flowers and leaves D fruits A, B from Hughes et al. 2608 C,D from Hughes et al. 2423. All photos Colin Hughes.

Geographic distribution

The monospecific genus Boliviadendron occupies a narrowly restricted distribution endemic to Bolivia and has been recorded from just a small number of localities on the eastern flanks of the Andes at mid-elevations in interior Andean valleys in the Departments of La Paz, Cochabamba and Santa Cruz (Fig. 3).

Figure 3. 

Distribution of Boliviadendron bolivianum endemic to the interior valleys on the eastern flanks of the Andes in Bolivia.

Habitat

Locally common in fence-lines and remnant patches of subhumid or seasonally dry Yungas forest and secondary thickets of Baccharis dracunculifolia DC., Dasyphyllum brasiliense (Spreng.) Cabrera (both Asteraceae), Dodonaea viscosa Jacq. (Sapindaceae) and Tecoma stans Juss. (Bignoniaceae). Other associated species include Apurimacia michelii Harms., Coursetia brachyrhachis Harms., Erythrina falcata Benth., Mimosa boliviana Benth., M. woodii Atahuachi & C.E. Hughes, Parapiptadenia excelsa (Griseb.) Burkart (all Leguminosae), Schinopsis haenkeana Engl. (Anacardiaceae), Cordyline dracaenoides Kunth (Asparagaceae), Kageneckia lanceolata Ruiz & Pav. (Rosaceae) and Cleistocactus laniceps (K. Schum.) Rol.-Goss (Cactaceae). Boliviadendron is known only from the slopes of interior valleys of Bolivia between 2150 and 2770 m alt., around the transition from seasonally-dry tropical inter-Andean valley forests to more moist mid-elevation montane Ceja de Monte Yungeña vegetation. Most collections (apart from two outlying localities in Dept. Santa Cruz) come from two nearby tributaries of the upper Río Cotacajes, in Prov. Ayopaya, Cochabamba and Prov. Inquisivi, La Paz, Bolivia, an area with several other narrowly-endemic plants, including Justicia pluriformis Wash. & J.R.I. Wood (Acanthaceae), Philibertia fontellae (Murillo) Goyder (Apocynaceae), Solanum stellativelutinum Bitter and S. tunariense Kuntze (Solanaceae) and Mimosa woodii (Leguminosae). Boliviadendron (as Leucochloron bolivianum) was assigned an IUCN threat category of Endangered (EN) B1ab(iii,iv) in 2011 (Atahuachi 2012) on account of its very limited extent of occurrence and threats from habitat destruction caused by agricultural expansion and fire which are continuing today.

Etymology

Boliviadendron is one of just two mimosoid legume genera known to be endemic to Bolivia (the other being Pseudosenegalia Seigler & Ebinger with two species) and that Bolivian endemism is highlighted here by the double-barrelled reference to that country in the name Boliviadendron bolivianum.

Boliviadendron bolivianum (C.E. Hughes & Atahuachi) E.R. Souza & C.E. Hughes, comb. nov.

Basionym

Leucochloron bolivianum C.E. Hughes & Atahuachi, Kew Bull. 61: 559. 2006, publ. 31 Jan 2007.

Type

Bolivia. La Paz, Prov. Inquisivi, 6 km N of Inquisivi, rd towards Cajuata, Circuata and Miguillas, 16°53'42"S, 67°08'23"W, 2385 m alt., 12 Dec 2003, C.E. Hughes, T. Ortuño & M. Mendoza 2423 (holotype: LPB; isotypes: BOLV, FHO, K [K000532854], USZ).

Additional material examined

Bolivia. Cochabamba, Prov. Ayopaya, 1 km S of Independencia on rd to Pongo, 17°05'03"S, 66°48'53"W, 2630 m alt., 15 May 2002 (unripe fr.), C.E. Hughes, J.R.I. Wood & R. Forrest 2287 (FHO!, K! [2 specimens], LPB!). Cochabamba, Ayopaya, 1 km above Independencia on road to Sailapata and La Mina, 17°04'S, 66°48'W, 2770 m, 18 Dec 2002 (fl.), J.R.I. Wood, M. Mercado & M. Mendoza 18731 (K!). La Paz, Prov. Inquisivi, ca. 10 km N of Inquisivi, rd to Licoma and Circuata, 16°53'71"S, 67°08'35"W, 2300 m alt., 27 March 2007 (unripe fr.), C.E. Hughes, T. Särkinen, A. Wortley & P. Duchen 2608 (FHO!, K! [2 specimens], LPB). La Paz, Prov. Inquisivi, 6 km N of Inquisivi, rd towards Cajuata, 16°53'43"S, 67°08'23"W, 2379 m alt., 12 Feb 2005 (ripe fr.), J.R.I. Wood, M. Atahuachi & T. Ortuño 21607 (BOLV, FHO!, K! [2 specimens], LPB). La Paz, Prov. Inquisivi, 0.5 km above Sica rd from Inquisivi to Cajuata, 16°52'32"S, 67°08'04"W, 2565 m alt., 12 Feb 2005 (fl.), J.R.I. Wood, M. Atahuachi & T. Ortuño 21618 (BOLV, FHO!, K! [2 specimens], LPB). La Paz, Prov. Inquisivi, 13 km from Inquisivi towards Licoma, crossing the Río Quime, 2150 m alt., 24 April 1992 (unripe fr.), St.G. Beck 21125 (K! [2 specimens]). La Paz, Prov. Inquisivi, along slopes E of Communidad Micayani to the Rio Khokhoni more or less to the junction with a fork flowing down from Communidad Yamora and following the Rio Khokhoni upstream 1 km from this point, ca. 4 km SE from Inquisivi, 16°55'S, 67°06'W, 2650 m alt., 14 Jan 1989 (fl.), M. Lewis 35094 (K!, LPB, MO). Santa Cruz, Prov. M. Caballero, ascending from Comarapa towards Cerro Bravo, 17°52'25"S, 64°31'32"W, 20 Nov 2005 (fl.), J.R.I. Wood & M. Mendoza 22081 (BOLV, FHO!, K! [2 specimens], LPB). Santa Cruz, Prov. Valle Grande, 14.2 km on the gravel road towards Moro Moro from the highway in the Trigal / Muyurina valley, 18°21'00"S, 64°14'27"W, 2335 m alt., 1 Jan 2011 (fl.), M. Nee & J.M. Mendoza F 57498 (NY!).

Acknowledgements

We thank the Laboratório de Sistemática Molecular de Plantas (LAMOL-UEFS) and the Jodrell Laboratory of the Royal Botanic Gardens, Kew staff for support with laboratory procedures and all the colleagues who kindly provided samples for DNA extraction. This work was supported by the FAPESB (grants: PTX0004/2016 and APP0096/2016), SISBIOTA (563084/2010-3) and the Swiss National Science Foundation through grants 310003A_156140 and 31003A_182453/1 to Colin Hughes and an Early.Postdoc.Mobility fellowship P2ZHP3_199693 to Erik Koenen. We are grateful to curators of all herbaria cited for providing access to their collections and to João Iganci and Luciano de Queiroz for comments and careful revision of the text.

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Supplementary materials

Supplementary material 1 

Table S1–S3

Lamarck Rocha

Data type: Tables

Explanation note: Includes voucher information, primers and protocols and summary of phylogenetic analyses.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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Supplementary material 2 

Figures S1–S9

Lamarck Rocha

Data type: Individual phylogenetic analyzes

Explanation note: Includes all trees derived from the BI, MP and ML with combined nuclear + plastidial loci, and individual analyses from nuclear, and plastidial loci.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (1.90 MB)
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