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Guillemin-Et-Al.-2016.Pdf Molecular Phylogenetics and Evolution 94 (2016) 814–826 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev The bladed Bangiales (Rhodophyta) of the South Eastern Pacific: Molecular species delimitation reveals extensive diversity q Marie-Laure Guillemin a,b, Loretto Contreras-Porcia c,d, María Eliana Ramírez c,e, Erasmo C. Macaya f,g, ⇑ Cristian Bulboa Contador c, Helen Woods h,i, Christopher Wyatt j,k, Juliet Brodie h, a Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile, Casilla 567, Valdivia, Chile b UMI 3614 Evolutionary Biology and Ecology of Algae, CNRS, Sorbonne Universite´s UPMC Univ. Paris 06, Pontificia Universidad Cato´lica de Chile, Universidad Austral de Chile c Departamento de Ecología y Biodiversidad, Facultad de Ecología y Recursos Naturales, Universidad Andres Bello, República 440, Santiago, Chile d Center of Applied Ecology & Sustainability (CAPES), Pontificia Universidad Católica de Chile, Santiago, Chile e Museo Nacional de Historia Natural, Área Botánica, Casilla 787, Santiago, Chile f Departamento de Oceanografía, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Concepción, Chile g Millennium Nucleus Ecology and Sustainable Management of Oceanic Island (ESMOI), Coquimbo, Chile h Natural History Museum, Department of Life Sciences, Cromwell Road, London SW7 5BD, UK i Centre for Ecology and Hydrology, Edinburgh, Bush Estate, Penicuik, Midlothian, Scotland EH26 0QB, UK j EMBL/CRG Research Unit in Systems Biology, Centre for Genomic Regulation (CRG), Barcelona 08003, Spain k Universitat Pompeu Fabra (UPF), Barcelona 08003, Spain article info abstract Article history: A molecular taxonomic study of the bladed Bangiales of the South Eastern Pacific (coast of Chile) was Received 4 June 2015 undertaken based on sequence data of the mitochondrial COI and chloroplast rbcL for 193 specimens Revised 22 September 2015 collected from Arica (18°S) in the north to South Patagonia (53°S) in the south. The results revealed for Accepted 30 September 2015 the first time that four genera, Porphyra, Pyropia, Fuscifolium and Wildemania were present in the region. Available online 17 October 2015 Species delimitation was determined based on a combination of a General Mixed Yule Coalescence model (GMYC) and Automatic Barcode Gap Discovery (ABGD) coupled with detection of monophyly in tree Keywords: reconstruction. The overall incongruence between the species delimitation methods within each gene Automatic Barcode Gap Discovery (ABGD) was 29%. The GMYC method led to over-splitting groups, whereas the ABGD method had a tendency Chile Mitochondrial COI to lump groups. Taking a conservative approach to the number of putative species, at least 18 were rec- General Mixed Yule Coalescence (GMYC) ognized and, with the exception of the recently described Pyropia orbicularis, all were new to the Chilean Morphological plasticity flora. Porphyra and Pyropia were the most diverse genera with eight ‘species’ each, whereas only a ‘single’ Plastid rbcL species each was found for Fuscifolium and Wildemania. There was also evidence of recently diverging groups: Wildemania sp. was distinct but very closely related to W. amplissima from the Northern Hemisphere and raises questions in relation to such disjunct distributions. Pyropia orbicularis was very closely related to two other species, making species delimitation very difficult but provides evidence of an incipient speciation. The difference between the ‘species’ discovered and those previously reported for the region is discussed in relation to the difficulty of distinguishing species based on morphological identification. Ó 2015 Elsevier Inc. All rights reserved. 1. Introduction due to the simple and variable morphology of specimens, and all bladed species were assigned to the genus Porphyra until The bladed Bangiales are a diverse, cosmopolitan order of mor- Sutherland et al. (2011), on the basis of a two-gene phylogeny, split phologically simple red algae, and an economically important the genus into eight genera: Boreophyllum, Clymene, Fuscifolium, resource used in the production of ‘‘nori”. Identification and taxo- Lysithea, Miuraea, Porphyra, Pyropia and Wildemania. A ninth nomic placement within the order have been highly problematic bladed genus, Neothemis, has been added recently, based on a study of the bladed Bangiales in the western Mediterranean (Sánchez et al., 2014, 2015). As a consequence of the generic revi- q This paper was edited by the Associate Editor Adrian Reyes-Prieto. sion, we are now in a position to evaluate/re-evaluate local and ⇑ Corresponding author. regional Bangiales floras. Although the difficulty of distinguishing E-mail address: [email protected] (J. Brodie). http://dx.doi.org/10.1016/j.ympev.2015.09.027 1055-7903/Ó 2015 Elsevier Inc. All rights reserved. M.-L. Guillemin et al. / Molecular Phylogenetics and Evolution 94 (2016) 814–826 815 species remains, generic circumscriptions enable better placement characterized by a diffusive overlap of biota of the two major pro- at the generic level which in turn enables us to focus on species vinces (Camus, 2001). Depending on the region, the coastline is present at the regional and local level (e.g. Mols-Mortensen et al., affected by many different factors. For example, northern and 2012; Vergés et al., 2013). central Chile is subject to abnormally cold, but highly productive The number of species in the Bangiales has been reported to be waters due to up-welling subsurface waters. This highly heteroge- well over 150 (Brodie et al., 2008a). However, where in Sutherland neous coastline also varies in terms of its tidal range, temperature, et al. (2011) approximately 58 out of 126 bladed samples included salinity and circulation patterns (Fernández et al., 2000; in the analysis were undescribed or with uncertain identity, and López-Cristoffanini et al., 2013). On the other hand, the shoreline the ongoing discovery of species (e.g. Mols-Mortensen et al., south of 42°S, consists of a dense array of islands, channels and 2012; López-Vivas et al., 2014; Ramírez et al., 2014; Sánchez fjords, strongly influenced by glacial rivers and sub-Antarctic et al., 2014), the number is anticipated to be considerably higher. oceanographic and climatic conditions. Thus, those ecological As for some other algal groups, characterized by simple morpholo- particularities make the Chilean coast a particularly interesting gies and intraspecific variability of morphological features, e.g. the area to study the macroalgal biodiversity of the rocky intertidal. red algal genus Portieria (Payo et al., 2013), the green algal genus Until recently, only six species of bladed Bangiales were Boodlea (Leliaert et al., 2009) and the brown algal genus Lobophora reported from the coast of Chile (Ramírez and Santelices, 1991): (Vieira et al., 2014), species discrimination based on morphological P. capensis Kützing, P. columbina Montagne, P. miniata (C. Agardh) analysis alone in bladed Bangiales has proven to be mostly unreli- C. Agardh f. cuneiformis Setchell & Hus, P. thurettii Dawson, able (Brodie et al., 2008a; Broom et al., 2010; Kucera and Saunders, P. umbilicalis (Linnaeus) Kützing [qv Brodie et al., 2008b], 2012; Nelson, 2013; Sánchez et al., 2014). Recent studies using P. woolhousiae Harvey. A further four species were recorded by molecular markers and phylogenetic reconstruction and/or genetic González and Santelices (2003): P. linearis Greville, P. pseudolinearis distance for species identification have concluded that names have Ueda, P. lanceolata [now Pyropia lanceolata (Smith & Hollenberg) been misapplied in some regions and that bladed Bangiales species S.C. Lindstrom], Porphyra torta Krishnamurthy [now Pyropia torta could be much more diverse and regionally confined than recog- (Krishnamurthy) S.C. Lindstrom]. Another species, Porphyra kunthi- nized, especially in the Southern Hemisphere (Jones et al., 2004; ana Kützing, described from Valparaíso, Chile (Kützing, 1843), was Brodie et al., 2008a; Broom et al., 2010; Nelson and Broom, 2010). subsumed into Porphyra columbina (see Ramírez and Santelices, In hyper-diverse groups, where cryptic diversity is widespread, 1991); however, the identity of this species remains to be rapid molecular methods to delimit species have been used to cir- confirmed. A new species, Pyropia orbicularis M.E. Ramírez, cumvent the difficulties of morphology-based identification. The L. Contreras-Porcia & M.L. Guillemin, has been described recently use of DNA barcodes, while presenting problems in recently (Ramírez et al., 2014). However, with the exception of this new diverging groups or in cases of hybridization or introgression Pyropia record, there is currently no evidence to date that any of (e.g. Mols-Mortensen et al., 2012), have been demonstrated to be the other species occur in this region. For example, Porphyra a very effective tool with which to identify species (Kekkonen capensis, which was reported from Magallanes and Tierra del Fuego and Hebert, 2014). Recently, two new analytical methods have in Chile, was originally described from the Cape of Good Hope, been developed for species delineation: the General Mixed Yule- South Africa (Kützing, 1843). Sequence data for 18°S (the only coalescent (GMYC; Pons et al., 2006) and the Automatic Barcode molecular data available for this species) from South African mate- Gap Discovery (ABGD; Puillandre et al., 2012a).
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