Research Article |
Corresponding author: Rafael F. de Almeida ( dealmeida.rafaelfelipe@gmail.com ) Academic editor: André Simões
© 2023 Rafael F. de Almeida, Isa L. de Morais, Marco O.O. Pellegrini, Cassio van den Berg.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
de Almeida RF, de Morais IL, Pellegrini MO, van den Berg C (2023) Molecular phylogeny and character-mapping support the synonymy of Cordobia and Gallardoa in Mionandra (Malpighiaceae). Plant Ecology and Evolution 156(3): 352-364. https://doi.org/10.5091/plecevo.101657
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Background and aims – Cordobia, Gallardoa, Mionandra, and Peixotoa (Stigmaphylloid clade, Malpighiaceae) are four small, closely related genera comprising shrubs or lianas endemic to South American savannas, dry forests, and temperate steppes. Their generic limits have significantly changed in the last century, and past molecular phylogenetic studies of Malpighiaceae have not tested the morphological characters of this group to identify synapomorphies supporting these clades/genera.
Material and methods – We sampled the monospecific Cordobia and Gallardoa, one species of Mionandra (out of 2 spp.), nine species of Peixotoa (out of 29 spp.), and a single species of Camarea and Janusia as outgroups. Bayesian and Maximum Likelihood analyses were carried out for this clade based on five molecular markers (i.e. ETS, ITS, PHYC, matK, and ndhF). A set of 16 macromorphological characters was scored and coded for identifying synapomorphies under the Maximum Likelihood criteria.
Key results – Our molecular phylogeny recovered Peixotoa as monophyletic and sister to the clade comprising Cordobia + Gallardoa + Mionandra, strongly corroborating previous phylogenetic studies of Malpighiaceae. The character-mapping analyses recovered two synapomorphies supporting the Cordobia + Gallardoa + Mionandra + Peixotoa clade, six supporting Mionandra s.l. (i.e. Cordobia + Gallardoa + Mionandra), and five supporting Peixotoa. Cordobia and Gallardoa are proposed as synonyms of Mionandra, alongside the necessary combinations, typifications, and identification keys.
Conclusions – Morphological characters related to the degree of connation of the stipules, leaf indumentum type, petiole length, inflorescence architecture, number of flowers per inflorescence, presence of a peduncle in the 1-flowered cincinni, sepal connation, posture and texture, petal width and margin integrity, staminode presence, shape and size, and the shape of the apex of styles were key in circumscribing these lineages. Mionandra s.l. is proposed and characterised, including a new combination, an identification key to distinguish its species, a distribution map, and taxonomy notes.
Cono Sur, Malpighiales, Peixotoa, taxonomy, Stigmaphylloid clade, systematics
Malpighiaceae has undergone unparalleled changes in its traditional classification in the last two decades due to the publication of several molecular phylogenetic studies (
The Stigmaphylloid clade is one of the new lineages recently resolved for Malpighiaceae, comprising several subclades (i.e. Bronwenia W.R.Anderson & C.Davis, Diplopterys A.Juss., Stigmaphyllon, Banisteriopsis, Sphedamnocarpus s.l., the Cordobioids, and the Aspicarpoids;
Their taxonomic history is quite convoluted, with most species of Cordobia, Gallardoa, and Mionandra having been treated under the latter. Mionandra was first described by
In this study, we reconstructed a molecular phylogeny of the Peixotoid clade based on three nuclear (ETS, ITS, and PHYC) and two plastid (matK and ndhF) genes to answer the questions: 1. Are Cordobia, Gallardoa, and Mionandra supported by morphological synapomorphies? 2. If not, would Mionandra s.l. (including Cordobia and Gallardoa) be supported by any morphological synapomorphies?
We sampled 14 species in this study representing 12 species from the Peixotoid clade (out of 31 spp.), including the type species of all four genera and a single species of Camarea and Janusia, respectively, as outgroups, representing tribe Gaudichaudieae as their sister group (Supplementary material
All trees were rooted in tribe Gaudichaudieae (Camarea + Janusia), the sister group of the Peixotoid clade, according to
Macro-morphological characters were scored from protologues and specimens consulted in herbaria (ALCB, ASE, BHCB, CEN, CEPEC, CESJ, CGMS, COL, CVRD, CTES, EAC, ESA, F, FLOR, FUEL, FURB, G, HAS, HB, HCF, HEPH, HRB, HRCB, HUCP,
The nuclear dataset represented 2,366 characters of the dataset, the plastid dataset represented 1,729 characters, and the combined plastid + nuclear dataset included 4,095 analysed characters. Topologies produced by BI and ML analyses, based on the individual nuclear and plastid datasets, did not exhibit incongruences among the topologies produced, so we performed a combined analysis of plastid + nuclear datasets (Fig.
Phylogeny and character-mapping of the Peixotoid clade. A. Phylogram recovered from the Maximum Likelihood analysis showing bootstrap values above the branches and posterior probability values below the branches. B. Consensus tree showing the character-mapping summarisation resulting from the Mesquite Maximum Likelihood analysis and WinClada visualisation. Red circles represent synapomorphies, and white circles represent homologies. The numbers above the circles represent the character numbers, and those below the circles represent the character states provided in Supplementary materials
We recovered three synapomorphies (stipules connate at the base or up to the middle, 1-flowered cincinni lacking peduncles [i.e. sessile], and sepals revolute at apex) for the Peixotoid clade alongside the outgroups representing tribe Gaudichaudieae (Fig.
The first clade recovered within the Peixotoid clade included the genera Cordobia + Gallardoa + Mionandra supported by six synapomorphies (sepals free at base, chartaceous, and entirely revolute, antherodes filiform and minute, apex of styles truncate to expanded) and a single homoplasy (1-flowered cincinni) (Fig.
The Peixotoid clade was recovered as highly supported (PP 1.0 / BS 100) in our tree (Fig.
Morphologically, Mionandra s.l. (including Cordobia and Gallardoa) is well-circumscribed with six synapomorphies and a single homoplasy (Fig.
Even though
Distinguished from the remaining genera of the Stigmaphylloid clade by its stipules connate, cincinni sessile and 1-flowered, and sepals completely distally revolute or involute along margins.
The Peixotoid clade currently comprises two monophyletic and morphologically well-circumscribed genera divided into a total of 32 species. Peixotoa is the largest genus of the two, currently with 29 species (
Diagnostic morphological characters differentiating both genera of the Peixotoid clade.
Character | Mionandra | Peixotoa |
Habit | Erect or scandent to prostrate subshrubs | Erect to scandent shrubs or lianas |
Stipules | Connate at base or up to the middle (i.e. bifid) | Completely connate (i.e. entire) |
Leaves | Never reduced in the inflorescences | Reduced in the inflorescences |
Petiole | Short | Long |
Leaf blades | Hirsute-sericeous | Various but never hirsute-sericeous |
Inflorescences | Solitary umbels | Umbels arranged in dichasia or thyrsi |
Umbels | Sessile, 1-flowered | Pedunculate, 4-flowered |
Bracts | Absent | Present |
Bracteoles | Absent | Present |
Sepals | Free, chartaceous, completely revolute or involute along margins | Connate at base, coriaceous, revolute only at apex |
Petal limb | Narrowly elliptic to oblanceolate or obovate to widely obovate | Orbicular |
Stamens | 5 | 5 |
Staminodes | 3–5 | 5 |
Antherodes | Filiform, minute | Globose, conspicuous |
Style | Truncate to slightly expanded | Capitate |
Fruits | Wings reduced, rarely dorsal wing well-developed, lateral wings free or fused at base | Wings well-developed, dorsal wing dominant, lateral and dorsal wings fused at base forming a basal crest |
1. | Stipules connate at base or up to the middle (i.e. bifid); umbels 1-flowered, bract and bracteoles absent; sepals free, completely revolute or involute along margins; antherodes filiform, minute; styles apex truncate to slightly expanded | Mionandra |
– | Stipules connate (i.e. entire); umbels 4-flowered, bract and bracteoles present; sepals connate at base, revolute only at apex; antherodes globose, conspicuous; styles apex capitate | Peixotoa |
Brittonella
Rusby (
Cordobia
Nied. (
Gallardoa
Hicken (
Mionandra camareoides Griseb.
Distinguished from Peixotoa by its stipules connate at the base or up to the middle (i.e. bifid), leaves short-petiolate, hirsute-sericeous; umbels 1-flowered, peduncles absent; sepals free, chartaceous, completely revolute or involute along margins; petals narrowly elliptic, margin glandular-fimbriate; fertile stamens 5, staminodes 3–5, antherodes filiform, minute; style apex truncate to slightly expanded; mericarps with wings reduced, rarely dorsal wing well-developed (Table
Erect or scandent to prostrate subshrubs; xylopodium present; indumentum throughout the plant ranging from sericeous to glabrescent; stipules expanded, connate at base or up to the middle (i.e. bifid), triangular, interpetiolar, persistent or deciduous. Leaves opposite, never reduced in the inflorescences; petioles cylindric, short-petiolate (up to 2 mm long), eglandular; blade narrowly elliptic, elliptic, lanceolate to ovate, base cuneate to obtuse, margin entire, apex acute to acuminate, abaxially 0–2-glandular near the base. Umbels solitary, terminal; cincinni 1-flowered; bracts absent; peduncles absent; bracteoles absent. Flowers bisexual, zygomorphic, chasmogamous; pedicels short to elongate; sepals concealing petals during enlargement of bud, completely revolute or involute along margins at anthesis, lateral sepals abaxially 2-glandular, the anterior usually eglandular; petals clawed, yellow, sometimes turning orange at age, both sides glabrous, limb narrowly elliptic to oblanceolate or obovate to widely obovate, base cuneate, margin glandular-fimbriate, apex round, claw plane, posterior petal erect, glandular along margins, lateral petals patent to erect. Androecium 8–10, fertile stamens 5, staminodes 3–5; filaments connate at base, straight, rarely curved, stamen filaments longer than staminode filaments, glabrous or pubescent; connective minute, inconspicuous; fertile anthers monomorphic or dimorphic, erect at apex, glabrous; antherodes absent to present, filiform, reduced to a glandular tissue, glabrous. Gynoecium with carpels connate their whole length in flower, separating during fruit development, styles thick, cylindric, erect, equal, divergent, apex of styles truncate to slightly expanded, stigma terminal to lateral, crateriform or discoid. Schizocarp breaking apart into 3 winged mericarps, separating from a short torus; mericarps with dorsal wing reduced, sometimes well-developed; lateral wings always reduced, free or fused; wings coriaceous, margin sinuate; nut ridged near areole; areole ovate to elliptic. Seeds smooth or rugose; embryos ovoid, cotyledons bent, equal or unequal.
Mionandra s.l. comprises four species confined to dry forests (Chaco), savannas, and temperate steppes (Patagonian steppes) from Argentina, southern Bolivia, and western Paraguay in South America (Fig.
A comprehensive treatment for the genera comprising Mionandra s.l. (including Cordobia and Gallardoa) and three of their four species are presented by Aliscioni and Torretta (2017) within the Flora of Argentina project, with M. paraguariensis (which does not occur in Argentina) not included in the treatment. Thus, we provide an updated key to all species of Mionandra s.l., plus comments on the recognition of M. paraguariensis.
1. | Leaves 2-glandular near base; sepals involute along margins; stamens dimorphic (the latero-posterior ones with shorter, stout and curved filaments, the posterior ones and the anterior filaments thin and straight but the anterior shorter in length); mericarps rugose, dorsal wing well-developed | M. argentea |
– | Leaves eglandular; sepals revolute at apex; stamen monomorphic; mericarps smooth, dorsal wing reduced to a crest | 2 |
2. | Erect subshrubs; leaves adpressed-sericeous, margin revolute; petals turning orange at age; style apex slightly expanded; mericarps with lateral wings fused in an orbicular structure; cotyledons equal | M. fischeri |
– | Scandent to prostrate subshrubs; leaves hirsute-sericeous at least abaxially, margin plane; petals remaining yellow at age; apex truncate; mericarps with lateral wings free; cotyledons unequal | 3 |
3. | Leaves adaxially hirsute-sericeous at maturity; flowers 1–1.2 cm diam.; petals narrowly elliptic to oblanceolate, apex obtuse; stamen filaments pubescent; staminodes 3, ½ the length of the stamen filaments | M. camareoides |
– | Leaves adaxially glabrous at maturity; flowers 2.5–3 cm diam.; petals obovate to widely obovate, apex truncate to emarginate; stamen filaments glabrous; staminodes 5, the same length as the stamen filaments | M. paraguariensis |
Cryptolappa argentea
(Griseb.) Kuntze (
Aspicarpa argentea
(Griseb.) Nied. (
Cordobia argentea
(Griseb.) Nied. (
Gaudichaudia argentea
(Griseb.) Chodat (
Janusia argentea Griseb., nom. not validly publ.
Peixotoa cordobensis
Kuntze (
ARGENTINA – Córdoba • in fruticetis Sierra de Córdoba, prope La Higuera; 1872; fl.; Lorentz s.n.; holotype: GOET; isotypes: CORD [CORD00005912], K [K000427020].
Mionandra argentea. A. Shrubby habit. B. Detail of a floral shoot showing the partially connate stipules in the node and the sessile 1-flowered cincinnus with a long-pedicellate floral bud. C. Flower in frontal view. D. Flower in lateral view showing the sepals involute along margins. Photographs A–B by Étienne Lacroix-Carignan; C–D by Andrea Cocucci.
Mionandra camareoides
Griseb. (
Brittonella pilosa
Rusby (
Mionandra camareoides f. prostrata
Nied. (
Mionandra prostrata
Stuck. ex Nied. (
ARGENTINA – Córdoba • en el campo acerca de Córdoba; Dec. 1870; fl.; Lorentz 407b; lectotype (designated here): GOET [GOET007649]; isolectotype: CORD [CORD00005913].
Mionandra camareoides var. paraguariensis
(Chodat) Nied. (
PARAGUAY – Cordillera • between the municipalities of Caacupé and Tobati; s.d.; Chodat & Vischer 238; holotype: G [G 208718].
After revisiting the original description of
Gallardoa fischeri
Hicken, Physis: Revista de la Sociedad Argentina de Ciencias Naturales, Buenos Aires 2: 101. 1916. (
Cordobia fischeri
(Hicken) Nied. (
ARGENTINA – Rio Negro • vicinity of General Roca; Dec. 1913; fl. fr.; Fischer 10; lectotype (designated here): SI [SI002629]; isolectotypes: BKL [BKL00000970], CM [CM1185], GH [GH00872231, GH00872232], K [K000427018, K000427019], SI [SI002630, SI002631, SI002632, SI002633, SI002634], US [US00108538, US00108539].
Peixotoa glabra A.Juss.
Distinguished from Mionandra s.l. by its stipules completely connate, leaves long-petiolate, never hirsute-sericeous; umbels 4-flowered; sepals connate at base, coriaceous, revolute only at apex; petals orbicular, margin dentate; fertile stamens 5, staminodes 5, antherodes globose, conspicuous; style apex capitate; mericarps with wings well-developed, dorsal wing dominant.
Peixotoa catarinensis. A. Detail of a sterile branch showing the connate stipules. B. Detail of the base of a leaf in abaxial view. C. Detail of a flowering branch. D. Floral bud in lateral view. E. Flower in frontal view. F. Winged mericarps in lateral view. Photographs by Marco Pellegrini.
Peixotoa comprises 29 species occurring in dry forests, rainforests, and savannas in Brazil, eastern Bolivia, and eastern Paraguay in South America (Fig.
Peixotoa has a contemporary taxonomic revision available for 28 of its species (
Studies mapping the evolution of macro-morphological characters in molecular phylogenies are the steppingstone to challenge traditional classifications and propose new predictive systems in Malpighiaceae, reflecting the evolutionary history of their taxa (
We would like to thank the staff of the
GenBank accession numbers for all markers and species sampled in this study.
Morphological matrix with all 16 characters scored and coded for all species sampled.
Character descriptions for all 16 characters scored in the morphological matrix.