Evolutionary relationships, biogeography and morphological characters of Glinus (Molluginaceae), with special emphasis on the genus composition in Sub-Saharan Africa

Abstract

Glinus is a small genus of Molluginaceae with 8-10 species mostly distributed in the tropics of the World. Its composition and evolutionary relationships were poorly studied. A new molecular phylogeny constructed here using nuclear (ITS) and chloroplast (rbcL, trnK-matK) markers confirmed the monophyly of the genus. Based on ITS analysis, the following well-supported lineages are present within Glinus: the G. bainesii lineage is recovered as sister to the remainder of the genus followed by G. oppositifolius. Three other clades are: G. hirtus with G. orygioides; G. radiatus and G. lotoides; the latter is represented by a sample from North America, and G. zambesiacus as sister to G. setiflorus + G. lotoides + G. dictamnoides. On the plastid gene tree, G. bainesii + G. oppositifolius form a sister clade to all other Glinus species. The next clade is formed by G. hirtus and G. orygioides followed by G. radiatus plus an American sample of G. lotoides. The next branch comprises G. setiflorus as sister to G. zambesiacus + G. lotoides + G. dictamnoides. Glinus seems to have originated from Africa around the Late Eocene or Early Miocene, with further radiations to Australia and the Americas during the Late Miocene or Late Pliocene. Compared with the previous limited character set used for the diagnostics, we have found ten new morphological and carpological traits distinguishing Glinus members. In both trees based on nuclear and plastid datasets, the major phylogenetic clades cannot be characterized by the peculiar morphological characters. Many shared character states leading to their contrasting pattern in the multivariate analysis model are interpreted as a high homoplasy in the phylogenetically distant species. We paid special attention to the composition of the genus in Sub-Saharan Africa, a region with the greatest species diversity. Our results provide new insight into the taxonomy of Glinus in this region. Glinus lotoides var. virens accepted in many previous works is a synonym of G. dictamnoides that is closely related to G. lotoides based on molecular analysis and morphological characters. The status of the American populations of G. lotoides needs further investigation due to different characters of the specimens from the Old and the New World. Many specimens previously identified as G. lotoides var. virens and as the intermediates G. lotoides × G. oppositifolius belong to G. zambesiacus sp. nov. and G. hirtus comb. nov. (≡ Mollugo hirta); the latter species is resurrected from synonymy after 200 years of unacceptance. In some African treatments, G. hirtus was known under the invalidly published name G. dahomensis. Glinus zambesiacus is distributed in the southern and eastern parts of tropical Africa, and G. hirtus previously assumed to be endemic to West Africa is indeed a species with a wide distribution across the tropical part of the continent. Glinus microphyllus previously accepted as endemic to West Tropical Africa together with other new synonyms (G. oppositifolius var. lanatus, G. herniarioides, Wycliffea rotundifolia) is considered here as G. oppositifolius var. keenaniicomb. nov. (≡ Mollugo hirta var. keenanii), a variety found across the entire distribution of G. oppositifolius (Australia, Asia, and Africa). The presence of the American G. radiatus in Africa is not confirmed, and all records of this species belong to G. hirtus. The lectotypes of some names (G. dictamnoides, G. herniarioides, Mollugo hirta, M. setiflora, Pharnaceum pentagynum, Wycliffea) as well as a neotype of G. trianthemoides are designated. A new key to the identification of all Glinus species in Sub-Saharan Africa is provided. A checklist is given of all accepted species in this region (G. bainesii, G. hirtus, G. lotoides, G. oppositifolius s.l., G. setiflorus, and G. zambesiacus) with their nomenclature, morphological description and geographical distribution.

Keywords: Glinus; Molluginaceae; Biogeography; Sub-Saharan Africa; molecular phylogeny; taxonomic revision.

Figure 1.

Maximum likelihood phylogenetic cladogram of Glinus derived from the nrITS. Values above branches refer to bootstrap values resulting from the ML analysis (only values ≥50). Values below branches refer to posterior probabilities resulting from Bayesian inference (only values ≥0.95) and bootstrap values resulting from the parsimony analysis (only values ≥50). An asterisk (*) denotes a branch unsupported by either bootstrap values or posterior probability.

Figure 2.

Maximum likelihood phylogenetic cladogram of Glinus derived from the combined plastid matrix (rbcL, trnK-matK). Values above branches refer to bootstrap values resulting from the ML analysis (only values ≥50). Values below branches refer to posterior probabilities resulting from Bayesian inference (only values ≥0.95) and bootstrap values resulting from the parsimony analysis (only values ≥50). An asterisk (*) denotes a branch unsupported by either bootstrap values or posterior probability.

Figure 3.

Maximum clade credibility (MCC) tree of Glinus obtained from the BEAST analysis calibrated using secondary calibrations (see Methods). Mean divergence times (values at some nodes) are shown with their 95% highest posterior density (HPD: grey bars). To the left is the plastid gene tree and to the right the nuclear gene tree, respectively.

Figure 4.

Ancestral range estimation (ARE) based on the reduced MCC tree (“BioGeoBEARS” DEC+J on Glinus unconstrained ancstates: global optim, three areas max. anagenetic dispersal rate, d = 0.0063; extinction rate, e = 0; cladogenetic dispersal rate, j = 0.023; likelihood ratio test, LnL = -48.91). Coding of biogeographical areas as shown in the legend. Coding of species areas is given in coloured squares left of each species. Pie charts represent the ancestral area probability inferred for each node.

Figure 5.

Closed anthocarp of Glinus species AG. setiflorusBG. zambesiacus. Scale bar: 1 mm.

Figure 6.

Seeds of Glinus species A, BG. bainesii (Botswana, B. Farrington et al. 486, K) C, DG. hirtus, a form with smooth seeds (Senegal, Perrottet 373, G) E, FG. hirtus, colliculate seeds (DR Congo, Nsimundele 2060, BR) G, HG. ononoides (India, D. Freyn s.n., G). Magnification: 120× (A, C, E, G); 500× (B, D, F, H).

Figure 7.

Seeds of Glinus species A, BG. lotoides (Israel, T. Kushnir s.n., HUJ) C, DG. dictamnoides (Kenya, P.R.O. Bally 2679, G). Magnification: 120× (A, C); 500× (B, D).

Figure 8.

Seeds of Glinus species A, BG. oppositifolius (Zambia, R.B. Drummond & A.J.Cookson 6335, E) C, DG. oppositifolius var. glomeratus (Angola, E.J. Mendes 3155, M) E, FG. oppositifolius var. keenanii (DR Congo, R. Verschueren 203, BR) G, HG. orygioides (Australia, M.J. Thorpe et al. 119, K). Magnification: 120× (A, C, E, G); 500× (B, D, F, H).

Figure 9.

Seeds of Glinus species A, BG. radiatus (Venezuela, A. Fernández et al. 27692, G) C, DG. sessiliflorus (Australia, B.J. Lepschi & J.R. Connors 4854, W) E, FG. setiflorus (Ethiopia, G. Popov 1143, K) G, HG. zambesiacus (Zambia, Robinson 6780, M). Magnification: 120× (A, C, E, G); 500× (B, D, F, H).

Figure 10.

Seed coat cross-sections AG. bainesiiBG. hirtusCG. lotoidesDG. oppositifoliusEG. orygioidesFG. radiatusGG. sessiliflorusHG. setiflorusIG. zambesiacus. Scale bar: 10 µm. Glinus dictamnoides has the same seed coat structure as G. lotoides and is not illustrated here. Origin of the material is provided in the Table 4 and is designated with an asterisk (*).

Figure 11.

Classification of Glinus species by group average linkage algorithm of cluster analysis based on 17 characters. Black branches connect significantly (P < 0.05) different groups, red branches – insignificantly different groups.

Figure 12.

The number of Glinus species around the world. Areas coloured in mauve – one species, blue – two species, green – three species, yellow – four species, red – five species. Area boundaries are approximated. G. ononoides is a poorly known Indian taxon that needs to be studied further.

Figure 13.

Glinus bainesiiA, B an overview of the plant C flowers D leaves E–G close-up of individual flowers. Photographers – Roger and Alison Heath (A, C, E Okavango Delta, Ngamiland, Botswana, 28 Nov 2004 B, D, F, G Moremi Game Reserve, Ngamiland, Botswana, 21 Nov 2007).

Figure 14.

A herbarium specimen of Glinus bainesii (Botswana, Northern distr., 17 km SE of Maun at Samadupe drift over Botletle river, 23 Jan 1972, H. Biegel & G. Russell 3733, K001394831). Copyright of the Board of Trustees of the Royal Botanic Gardens, Kew.

Figure 15.

Distribution map of Glinus bainesii in Sub-Saharan Africa (coloured in yellow).

Figure 16.

Glinus hirtusA an overview of the plant B close-up of the leaf C, D flowers. Photographers – Roger and Alison Heath (A, D Moremi Game Reserve, Ngamiland, Botswana, Nov 2010 B, C Selinda, Ngamiland, Botswana, 04 Nov 2004 (B), 23 Jan 2004 (C).

Figure 17.

A herbarium specimen of Glinus hirtus (Central African Republic, 300 m NW of Gounda, 9°18'N, 21°12'E, alt. 450 m, 28 Jul 1982, J.M. Fay 2763, K001394828 as G. dahomensis). Copyright of the Board of Trustees of the Royal Botanic Gardens, Kew.

Figure 18.

Distribution map of Glinus hirtus in Sub-Saharan Africa (coloured in yellow).

Figure 19.

Glinus lotoidesA an overview of the plant B close-up of the leaves and buds C close-up of the flower D closed anthocarp. Photographer – Ridha El Mokni (Sidi Mechrig – Sejnane, Bizerta Governorate, Tunisia, 23 Oct 2015).

Figure 20.

A herbarium specimen of Glinus lotoides (Kayes region, Comitradougou, 100 km from Diéma, 14°25'N, 8°18'W, alt. 317 m, 25 Feb 2006, R. Dembele et al. ML-283, K001394833). Copyright of the Board of Trustees of the Royal Botanic Gardens, Kew.

Figure 21.

Distribution map of Glinus lotoides in Sub-Saharan Africa (colored in yellow).

Figure 22.

Glinus oppositifolius var. oppositifoliusA, B general view of the plant C close-up of the flowers D close-up of the leaves. Photographers – Roger and Alison Heath (Moremi Game Reserve, Ngamiland, Botswana, 07 Feb 2011).

Figure 23.

A herbarium specimen of Glinus oppositifolius var. oppositifolius (Kenya, [Lamu county], Kiunga, 55 m NE Lamu, 6 Aug 1961, J.B. Gillespie 167, K001394829). Copyright of the Board of Trustees of the Royal Botanic Gardens, Kew.

Figure 24.

Distribution map of Glinus oppositifolius var. oppositifolius in Sub-Saharan Africa (colored in yellow).

Figure 25.

A herbarium specimen of Glinus oppositifolius var. keenanii labeled as G. microphyllus (Tanzania, Rufiji distr., 2 Dec 1955, E. Milne-Redhead & P. Taylor 7528, K001394830). Copyright of the Board of Trustees of the Royal Botanic Gardens, Kew.

Figure 26.

Distribution map of Glinus oppositifolius var. keenanii (green circles) and G. oppositifolius var. glomeratus (blue circles) in Sub-Saharan Africa (colored in yellow).

Figure 27.

A herbarium specimen of Glinus oppositifolius var. glomeratus (Angola, Cuando-Cubango prov., Longa, Longa river, 1360 m, 17 Mar 1960, E.J. Mendes 3155, BM013839321).

Figure 28.

A herbarium specimen of Glinus setiflorus (Tanzania, Dodoma region, Ikowa Dam, 60 km E of Dodoma, 900 m, 29 Jul 1970, M. Thulin & B. Mhoro 515, K001394832). Copyright of the Board of Trustees of the Royal Botanic Gardens, Kew.

Figure 29.

Distribution map of Glinus setiflorus in Sub-Saharan Africa (colored in yellow).

Figure 30.

Holotype of Glinus zambesiacus Sukhor., sp. nov. (Zambia, Barotseland, [Western province] Mongu, mud at edge of river, 6 January 1966, Robinson 6780, K000865904). Copyright of the Board of Trustees of the Royal Botanic Gardens, Kew.

Figure 31.

Distribution map of Glinus zambesiacus in Sub-Saharan Africa (colored in yellow).