Molecular Data, Based on an Exhaustive Species Sampling of The

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Molecular Data, Based on an Exhaustive Species Sampling of The Botanical Journal of the Linnean Society, 2017, XX, 1–19. With 5 figures. Molecular data, based on an exhaustive species sampling of the fern genus Rumohra (Dryopteridaceae), reveal a biogeographical history mostly shaped by dispersal and several cryptic species in the widely distributed Rumohra adiantiformis LUCIE BAURET1,2*, GERMINAL ROUHAN1, REGINA Y. HIRAI3, LEON PERRIE4, JEFFERSON PRADO3, ALEXANDRE SALINO5, BRUNO SENTERRE6,7, LARA SHEPHERD4,8, MICHAEL SUNDUE9, MARC-ANDRÉ SELOSSE1,10 and MYRIAM GAUDEUL1 1Muséum national d’Histoire naturelle, Sorbonne Universités, Institut de Systématique, Evolution, Biodiversité (UMR 7205 CNRS, MNHN, UPMC, EPHE), Herbier national, 16 rue Buffon CP39, F-75005 Paris, France 2Université Pierre et Marie Curie, Sorbonne Universités, Institut de Systématique, Evolution, Biodiversité (UMR 7205 CNRS, MNHN, UPMC, EPHE), 57 rue Cuvier CP48, F-75005 Paris, France 3Instituto de Botânica, Caixa Postal 68041, CEP 04045-972 São Paulo, SP, Brazil 4Museum of New Zealand Te Papa Tongarewa, PO Box 467, Wellington, New Zealand 5Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, Pampulha, 31270-901 Belo Horizonte, Brazil 6Evolutionary Biology & Ecology, CP 160/12, Université Libre de Bruxelles, 50 Av. F. Roosevelt, 1050, Bruxelles, Belgium 7Natural History Museum, PO Box 720, Victoria, Mahé, Seychelles 8School of Biological Sciences, Victoria University of Wellington, PO Box 600, Wellington, New Zealand 9The Pringle Herbarium, Department of Plant Biology, The University of Vermont, 27 Colchester Ave., Burlington, VT 05405, USA 10Department of Plant Taxonomy and Nature Conservation, University of Gdańsk, ul. Wita Stwosza 59, 80-308 Gdańsk, Poland Received 6 June 2017; revised 11 August 2017; accepted for publication 15 September 2017 Rumohra is a fern genus comprising seven species, three in South America, three in Madagascar and one (R. adian- tiformis) which is widely distributed across the Southern Hemisphere. Our goals were to assess species delimitation based on molecular data and to infer the biogeographical history that led to such contrasting distributions among species. We sampled all Rumohra spp., with 46 samples including 28 R. adiantiformis accessions from 14 regions, and sequenced eight plastid DNA regions: atpA, atpB, atpB-rbcL, rbcL, rps4-trnS, trnG-trnR, trnH-psbA and trnL/trnL- trnF. The resulting phylogenetic trees showed R. adiantiformis to be polyphyletic, with at least six lineages found in distinct geographical regions. Given the apparent absence of distinctive morphological characters among lineages, they are best understood as cryptic species. Such genetically distinct but morphologically similar populations may result from a recurrent history of hybridization, morphological convergence or (most probably) morphological stasis. Molecular dating and ancestral area estimations showed that Rumohra diverged from the genus Megalastrum c. 46.4 Mya in the Neotropics, and started to diversify 11.2 Mya. Its biogeographical history was probably shaped by seven long-distance dispersal (LDD) events including three initial events from the Neotropics to southern Africa, the *Corresponding author. E-mail: [email protected] © 2017 The Linnean Society of London, Botanical Journal of the Linnean Society, 2017, XX, 1–19 1 Downloaded from https://academic.oup.com/botlinnean/article-abstract/doi/10.1093/botlinnean/box072/4627929 by guest on 14 November 2017 2 L. BAURET ET AL. Malagasy region and southern South America. The Australasian lineage resulted from a LDD from southern South America, and the three species endemic to Madagascar diversified in situ. ADDITIONAL KEYWORDS: Madagascar – molecular phylogeny – pteridophytes – Southern Hemisphere – species concept – systematics – western Indian Ocean. INTRODUCTION one species name because of their similar morphology, but are genetically distinct; Bickford et al., 2007) is Delimiting species is an essential prerequisite for probably still limited by the low variability of molecu- studies of ecology and evolution and the implemen- lar markers, especially in plants, and by the sampling tation of appropriate conservation measures. Beyond schemes adopted, which often consist of a single or few morphological investigations, molecular markers have individual/accession(s) per morphologically recognized greatly improved our ability to circumscribe taxonomic species. However, a growing number of studies provide units in recent decades, leading to a so-called integra- evidence for cryptic species in various plant groups tive taxonomy (Rouhan & Gaudeul, 2014). Molecular (Bickford et al., 2007; see also, e.g. Hedenäs & Eldenäs, markers are especially valuable in groups with few 2007; Pillon et al., 2009; Bauret et al., 2017; Crowl, morphological attributes and in groups comprising Myers & Cellinese, 2017). Genetic data can also pro- morphologically similar populations that sometimes vide insight into the evolutionary (phylogenetic) rela- occur across large geographical areas. In the latter tionships among taxa and their diversification history, case, a widely distributed morphologically defined spe- providing hypotheses to explain the observed species cies might consist of a single interconnected gene-pool distributions and morphological disparity or, by con- (e.g. if dispersal is frequent), or may be composed of trast, morphological uniformity. several evolutionarily independent lineages. Indeed, Rumohra Raddi is a small fern genus of seven, mostly large geographical distances can lead to reduced gene tropical species. It contains one species with popula- exchange among populations, resulting in neutral tions spread across the whole Southern Hemisphere genetic divergence under the action of genetic drift. [R. adiantiformis (G.Forst) Ching], whereas the Nevertheless, such genetic divergence is not necessar- remaining six species are restricted to two centres of ily accompanied by morphological changes (morpho- endemism (Table 1): South America (three endemics; logical stasis). Alternatively, morphological similarity Sundue, Hirai & Prado, 2013) and Madagascar (three in widely distributed taxa can result from convergence endemics; Rakotondrainibe, 2010). Species are terres- towards traits that confer a selective advantage and trial, epilithic or epiphytic, and the genus is morpho- that are therefore independently selected in lineages logically characterized by a combination of several that are not closely related (Patterson & Givnish, features (Fig. 1): creeping rhizomes with a dorsal leaf 2002). The discovery of cryptic species (distinct species arrangement; elongate ventral meristele; lanceolate that are, or have been, erroneously classified under Table 1. Distribution of the seven Rumohra spp. Western Indian America Australasia Other Ocean – Africa R. adiantiformis Madagascar, Mascarenes, Neotropics, Galapagos*, Australia, Papua Tristan da Cunha, Comoros, Seychelles, southern South America, New Guinea, New South Indian Ocean Southern Africa Falkland Islands, West Zealand (type Islands, Bermuda* Indies locality) R. berteroana – Juan Fernández Islands – – R. glandulosissima – Neotropics (Brazilian – – Atlantic Rainforest) R. linearisquamata Madagascar – – – R. lokohensis Madagascar – – – R. madagascarica Madagascar – – – R. quadrangularis – Neotropics (Brazilian – – Atlantic Rainforest) *Unsampled localities for the widely distributed R. adiantiformis. © 2017 The Linnean Society of London, Botanical Journal of the Linnean Society, 2017, XX, 1–19 Downloaded from https://academic.oup.com/botlinnean/article-abstract/doi/10.1093/botlinnean/box072/4627929 by guest on 14 November 2017 RUMOHRA: PHYLOGENETICS AND BIOGEOGRAPHY 3 © 2017 The Linnean Society of London, Botanical Journal of the Linnean Society, 2017, XX, 1–19 Downloaded from https://academic.oup.com/botlinnean/article-abstract/doi/10.1093/botlinnean/box072/4627929 by guest on 14 November 2017 4 L. BAURET ET AL. to deltate, two- to three- (to four-) pinnate laminae; Schneider & Ranker, 2001). Nevertheless, this scen- decurrent leaf margins forming erect wings along the ario remained tentative for Rumohra, due to limited axes; and peltate indusia. Because the architecture of sampling. the lamina is fairly uniform across the genus, species In this study, we focused on Rumohra and, based on are mostly distinguished based on their rhizome habit, an exhaustive species sampling and extensive within- rhizome scales and lamina indument (e.g. sessile and/ species sampling for the widely distributed R. adian- or stipitate glands). tiformis, we inferred the molecular phylogeny of the Rumohra belongs to Dryopteridaceae subfamily genus in a spatiotemporal framework. Our goals were: Elaphoglossoideae (PPGI, 2016) or Polypodiaceae sub- (1) to assess the monophyly of the genus and its spe- family Dryopteridoideae (Christenhusz & Chase, 2014). cies; (2) more specifically, to identify whether R. adian- With the genera Megalastrum Holttum (91 species; tiformis represents a single taxonomic unit or several Moran, Prado & Sundue, 2014a, b), Lastreopsis Ching distinct but morphologically similar evolutionary units (16 species; Labiak et al., 2015) and Parapolystichum (cryptic species); and (3) to infer the biogeographical (Keyserl.) Ching (28 species; Labiak et al., 2015; history of the group. Sundue & Testo, 2016), Rumohra forms a monophy- letic group of 142 species referred to as lastreopsid ferns (Labiak et al., 2014). To date, no phylogenetic MATERIAL AND
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