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Out of Asia: Biogeography of Fungal Populations Reveals Asian Origin of Diversification of the Laccaria Amethystina Complex, and Two New Species of Violet Laccaria

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Out of Asia: Biogeography of Fungal Populations Reveals Asian Origin of Diversification of the Laccaria Amethystina Complex, and Two New Species of Violet Laccaria fungal biology 121 (2017) 939e955 journal homepage: www.elsevier.com/locate/funbio Out of Asia: Biogeography of fungal populations reveals Asian origin of diversification of the Laccaria amethystina complex, and two new species of violet Laccaria Lucie VINCENOTa,*,1, Flavius POPAb,c,1, Francisco LASOd, Kathrin DONGESb, Karl-Heinz REXERb, Gerhard KOSTb, Zhu L. YANGe, Kazuhide NARAf, Marc-Andre SELOSSEd,g aNormandie Univ, UNIROUEN, IRSTEA, ECODIV, Batiment^ Blondel, F-76821 Mont Saint Aignan Cedex, France bPhilipps-Universitat€ Marburg, Department of Systematic Botany and Mycology, Karl-von-Frisch Straße 8, 35039 Marburg, Germany cBlack Forest National Park, Department of Ecosystem Monitoring, Research & Conservation, Kniebisstraße 67, 77740 Bad Peterstal-Griesbach, Germany dMuseum National D’Histoire Naturelle, Institut de Systematique, Evolution, Biodiversite (UMR 7205 ISYEB), CP 50, 45 Rue Buffon, 75005 Paris, France eKey Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China fDepartment of Natural Environmental Studies, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8563, Japan gDepartment of Plant Taxonomy and Nature Conservation, University of Gdansk, Poland article info abstract Article history: Purple Laccaria are ectomycorrhizal basidiomycetes associated with temperate forests all over Received 1 March 2017 the Northern Hemisphere in at least two taxa: Laccaria amethysteo-occidentalis in North Amer- Received in revised form ica, and L. amethystina complex in Eurasia, as shown by Vincenot et al. (2012). Here, we 28 July 2017 combine a further study of the genetic structure of L. amethystina populations from Europe Accepted 9 August 2017 to southwestern China and Japan, using neutral Single Sequence Repeat (SSR; microsatellite) Available online 24 August 2017 markers; and a systematic description of two novel Asian species, namely Laccaria moshuijun Corresponding Editor: and Laccaria japonica, based on ecological, morphological, and molecular criteria (rDNA se- Kentaro Hosaka quences). Population genetics provides evidence of the ancient isolation of three regional groups, with strong signal for speciation, and suggests a centre of origin of modern popula- Keywords: tions closest to present-day Chinese populations. Phylogenetic analyses confirm speciation Cryptic geographic species at the molecular level, reflected in morphological features: L. moshuijun samples (from Fungal species complex Yunnan, China) display strongly variable cheilocystidia, while L. japonica samples (from Japan) Hydnangiaceae present distinctive globose to subglobose spores and clavate cheilocystidia. This study of Phylogeography a species complex primarily described with an extremely wide ecological and geographical Purple Laccaria range sheds new light on the biodiversity and biogeography of ectomycorrhizal fungi. Taxonomy ª 2017 British Mycological Society. Published by Elsevier Ltd. All rights reserved. * Corresponding author. Tel.: þ33 232769434. E-mail address: [email protected] (L. Vincenot). 1 Authors equally contributed to the experiments, data analyses and preparation of the manuscript. http://dx.doi.org/10.1016/j.funbio.2017.08.001 1878-6146/ª 2017 British Mycological Society. Published by Elsevier Ltd. All rights reserved. 940 L. Vincenot et al. Introduction in association with coniferous (Pinaceae) and deciduous (Betulaceae, Fagaceae, Salicaceae) hosts (Mueller 1984; Roy Ectomycorrhizal fungi (EMF) play a major role in ecosystems, et al. 2008). Therefore, a northern hemisphere distribution especially in temperate and boreal forests (Smith & Read of L. amethystina was assumed, although several different 2008), through their symbiotic association with the roots of violet species may exist worldwide (Wilson et al. 2013; numerous tree species. Most studies of EMF were done in ear- Wilson et al. 2017a; Fig 1).Onepossiblereasonforthissim- lier decades in Europe and North America, and this has plistic picture of global distribution could be difficulty in resulted in a geographic bias in the history of fungal systemat- delineating species within a global L. amethystina species ics (Dickie & Moyersoen 2008). complex, as suggested by Vincenot et al. (2012).Fewmor- Mycologists began to explore biogeographical patterns phological and systematically informative characters have and speciation processes of fungi in recent decades (Kohn been described, whereas more conspicuous characters 2005; Giraud et al. 2008), with case studies mostly focussing such as the colour of the different fruitbody parts show on pathogenic and saprotrophic species (Brown & broad phenotypic variation (Mueller 1992; Wang et al. Hovmøller 2002; Giraud et al. 2010; Stukenbrock 2013). Speci- 2004; Popa et al. 2014). Nevertheless, Mueller (1984) distin- ation and historical distribution of EMF species have been ex- guished the North American violet Laccaria amethysteo-occi- plored mainly at the local scale, and data remain scarce at the dentalis from the Eurasian L. amethystina. With a first continental level (Douhan et al. 2011; Vincenot & Selosse continental-scale characterization of spatial genetic struc- 2017). Yet today, many EMF species are still named world- ture of populations, Vincenot et al. (2012) showed that L. wide and across a variety of ecosystems using European or amethystina from Western Europe and Scandinavia belongs North American names, due to the above-mentioned geo- to a single, panmictic metapopulation, whose dispersal and graphic bias, and based on superficially similar morphology genetic homogenization were possibly favoured by host (Hawksworth 2001; Schmit & Mueller 2007; Feng et al. 2012). generalism (Roy et al. 2008)andtheabsenceofmajorgeo- The common assumption that some EMF species show graphic barriers. But we also demonstrated reproductive a worldwide distribution (Taylor et al. 2006)isreminiscent isolation between European and Japanese populations of of the Beijerinckian view that in the microbial world ‘every- L. amethystina, which is strongly supported by phylogenetic thing is everywhere’ (O’Malley 2007). Assumptions of world- analysis (Vincenot et al. 2012). This raised the hypothesis of wide distributions imply not-too-ancient, long-distance a cryptic species complex over Eurasia, and the need for in- gene flow, a long history of repeated diffuse gene flow over vestigation of more populations between the two investi- small to medium distances that prevent parapatric specia- gated Eurasian range limits. tion, or a combination of both processes (de Queiroz 2005; In the present study, we sought a finer understanding of Lomolino et al. 2010). The continental scale continuity of ecto- the biogeography of Eurasian L. amethystina and of the taxo- mycorrhizal host forests without major mountain barriers, nomic relationships within the L. amethystina species com- for example over Europe, may allow such gene flow plex. We used a larger set of neutral markers for population (Douhan et al. 2011). Nevertheless, phylogeographic analyses genetics, combined with phylogenetics, and completed mo- based on molecular data often distinguish cryptic biological lecular data with ecological, macro and micromorphological species, which have remained hidden so far because of the observations. Most importantly, we examined genotypic and limited availability (or investigation) of morphological char- phenotypic variation among populations from 12 sites over acters. In fact, recent studies of various fungal species, EMF three regions: Europe, China (Yunnan province, one of the or not, have highlighted a disjunctive population structure most important biodiversity hotspots in Asia; Myers et al. suggestive of distinct biological or phylogenetic species (e.g. 2000) and Japan. Based on these populations, we offer an Geml et al. 2006, 2010; O’Donnell et al. 2011; Grubisha et al. updated view of the L. amethystina complex over Eurasia, de- 2012; Zhao et al. 2013; Merenyi et al. 2014; Jargeat et al. 2016). lineate two new species, and propose biogeographic scenarios In particular, range disjunction can be related to global, an- relating their histories to that of the amended European cient geographic patterns, as observed between Old and L. amethystina sensu stricto. New World taxa (Geml et al. 2006, 2010; Garnica et al. 2011; O’Donnell et al. 2011). One of the most documented model species in ectomy- Material and methods corrhizal population genetics is Laccaria amethystina Cooke (Cooke 1884), because of its unique appearance, seemingly Collection and field sites wide geographic distribution and large host range (Gherbi et al. 1999; Wadud et al. 2006b; Roy et al. 2008; Vincenot Fruitbodies of Laccaria amethystina were collected at forest et al. 2012), and because of the early availability of molecu- sites in three regions: five sites in Europe, two in Japan (from lar resources for sister species L. bicolor (Martin et al. 2008). Vincenot et al. 2012) and five new sites in China (Table 1; It belongs to an ECM genus distributed worldwide (Wilson Fig 1). This sampling scheme covered regional Euclidian dis- et al. 2017a,b). The typical violet fruitbodies of L. amethys- tances of 2340 km (Europe), 370 km (China) and 960 km (Japan). tina are described as widely distributed from temperate As in Vincenot et al. (2012), all fruitbodies were collected at and boreal regions of the northern hemisphere to moun- least 1.5 m away from each other to avoid collecting the tain areas (above
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