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High Levels of Endemism Among Galapagos Basidiolichens

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High Levels of Endemism Among Galapagos Basidiolichens Fungal Diversity (2017) 85:45–73 DOI 10.1007/s13225-017-0380-6 High levels of endemism among Galapagos basidiolichens 1,2 3,4 5 Manuela Dal Forno • Frank Bungartz • Alba Ya´nez-Ayabaca • 6,7 2 Robert Lu¨cking • James D. Lawrey Received: 29 December 2016 / Accepted: 7 April 2017 / Published online: 20 April 2017 Ó School of Science 2017 Abstract This study is a re-assessment of basidiolichen namely Cora galapagoensis, Cyphellostereum uno- diversity in the Galapagos Islands. We present a molecular quinoum, Dictyonema barbatum, D. darwinianum, D. phylogenetic analysis, based on 92 specimens from Gala- ramificans, and D. subobscuratum; and four species have pagos, using two nuclear ribosomal DNA markers (ITS and already been described previously, namely Acantholichen nuLSU). We also re-examined the morphology and anat- galapagoensis, Cora santacruzensis, Dictyonema pectina- omy of all sequenced material. The molecular results tum, and D. galapagoense, here recombined as Cyphel- confirm our previous assessment that all Galapagos lostereum galapagoense. Our analysis is set on a very basidiolichens belong to the Dictyonema clade, which in broad phylogenetic framework, which includes a large Galapagos is represented by four genera: Acantholichen, number of specimens (N = 826) mainly from Central and Cora, Cyphellostereum, and Dictyonema. Most species South America, and therefore strongly suggests an unusu- previously reported from Galapagos in these genera were at ally high level of endemism previously not recognized. the time believed to represent widely distributed taxa. This This analysis also shows that the closest relatives of half of conclusion, however, has changed with the inclusion of the basidiolichens now found in Galapagos are from molecular data. Although almost the same number of mainland Ecuador, implying that they reached the islands species is distinguished, the phylogenetic data now suggest through the shortest route, with all species arriving on the that all are restricted to the Galapagos Islands. Among islands through independent colonization events. them, six species are proposed here as new to science, Keywords Lichens Á Systematics Á Biodiversity Á Evolution Á Lichenized basidiomycetes Á Galapagos Electronic supplementary material The online version of this article (doi:10.1007/s13225-017-0380-6) contains supplementary material, which is available to authorized users. & Manuela Dal Forno 2 Department of Environmental Science and Policy, George [email protected] Mason University, Fairfax, VA 22030-4444, USA Frank Bungartz 3 Charles Darwin Foundation for the Galapagos Islands, [email protected] Puerto Ayora, Galapagos, Ecuador Alba Ya´nez-Ayabaca 4 School of Life Sciences, Arizona State University, [email protected] PO Box 874501, Tempe, AZ 85287-4501, USA Robert Lu¨cking 5 Facultad de Ciencias Agrı´colas, Universidad Central del [email protected] Ecuador, Ciudadela Universitaria, Quito, Ecuador James D. Lawrey 6 Botanical Garden and Botanical Museum Berlin, Ko¨nigin- [email protected] Luise-Straße 6–8, 14195 Berlin, Germany 7 1 Department of Botany, Smithsonian Institution, National Science & Education, The Field Museum, 1400 South Lake Museum of Natural History, 10th St & Constitution Ave NW, Shore, Chicago, IL 60605, USA Washington, DC 20560, USA 123 46 Fungal Diversity (2017) 85:45–73 Introduction 3. Dictyonema sp. (Weber 1993) (an unidentified, appressed filamentous, crustose species). The Galapagos Islands represent an isolated ecosystem 4. Acantholichen pannarioides P. M. Jørg. (Jørgensen long considered a living laboratory of evolution (Darwin 1998; Lawrey et al. 2009;Lu¨cking et al. 2009). 1859; Carlquist 1974; Williamson 1981; Bensted-Smith These four species include one foliose growth form 2002). Assuming that species only rarely managed to col- (Dictyonema glabratum), one filamentous, shelf-forming onize the islands, presumably from South and Central morphotype (Dictyonema sericeum), an appressed-fila- America, when they did arrive they filled unoccupied mentous, crustose form (Dictyonema sp.), and a ecological niches and evolved independently from their microsquamulose taxon (Acantholichen pannarioides). All mainland relatives. Many groups of organisms therefore specimens subsequently collected were generally assigned exhibit high levels of endemism in the archipelago: to one of these taxa based on their morphology. In addition, 32–43% for vascular plants, *50% for invertebrates (ex- Dictyonema moorei (Nyl.) A. Henssen and D. mem- cluding insects), 47% for insects, and 59% for land verte- branaceum C. Agardh. were used as working names for brates (Tye et al. 2002). However, endemism in lichens has specimens collected in the islands, but in the first revision typically been considered to be much lower, around 3–10% of the group published by Ya´nez et al. (2012), these names (Weber 1986;Ya´nez et al. 2013). were added to the list of rejected taxa for the archipelago Until 2005, when the Charles Darwin Foundation (CDF) (Bungartz et al. 2013c). initiated a new, comprehensive species inventory, William Ya´nez et al. (2012) were the first to document the diversity Weber was responsible for gathering most of the modern of basidiolichens in the Galapagos using a revised genus lichen collections from the Galapagos, resulting in a concept based on Lawrey et al. (2009), who recognized four checklist including 196 species (Weber 1986). Since then, genera within the Dictyonema clade: Acantholichen P.M. there have been three updated checklists: two by Elix and Jørg., Cora Fr., Cyphellostereum D.A. Reid, and Dicty- McCarthy (1998, 2008), who included 229 and 253 spe- onema C. Agardh ex Kunth sensu stricto (s.str.). Ya´nez et al. cies, respectively, and the third by Bungartz et al. (2013c), (2012) used a conservative approach when identifying which included 579 accepted species, along with several Galapagos material based on this revised concept, recog- reports of names still under revision. nizing new species only where no available name could be As part of the general species inventory of lichens in the applied. This led to the distinction of eight taxa in the Dic- Galapagos, several revisionary treatments dedicated to tyonema clade for the islands: Acantholichen pannarioides, particular groups have been published recently (Aptroot Cora glabrata (Spreng.) Fr., Cyphellostereum imperfectum and Bungartz 2007; Aptroot and Sparrius 2008; Aptroot Lu¨cking, Barillas & Dal-Forno, Cyphellostereum sp., Dic- et al. 2008; Bungartz 2008; Bungartz et al. tyonema galapagoense Ya´nez, Dal Forno & Bungartz, Dic- 2010, 2013a, b, 2015, 2016a, b; Tehler et al. 2009;Ya´nez tyonema pectinatum Dal Forno, Ya´nez-Ayabaca & Lu¨cking, et al. 2013). These also include a first treatment of Gala- Dictyonema sericeum, and Dictyonema schenkianum (Mu¨ll. pagos basidiolichens (Ya´nez et al. 2012), which was based Arg.) Zahlbr. Of these, D. galapagoense and D. pectinatum only on morphological and anatomical studies. were proposed as new to science based on Galapagos spec- Prior to the treatment of Ya´nez et al. (2012), four imens and C. imperfectum was described as new, based on basidiolichen taxa had been reported from the Galapagos material from Guatemala, citing also material from the Islands, partially under different names, all members of the Galapagos. As a result, of the seven species formally rec- Dictyonema sensu lato clade: ognized (excluding Cyphellostereum sp.), two (29%) were 1. Cora pavonia (Sw.) Fr. in Dodge (1935), also cited in considered endemic, whereas prior to that treatment, none of Weber (1966), later moved to Dictyonema montanum the four recognized taxa had been considered endemic. (Sw.) Parm. by Weber (1986), which was followed by Based on molecular, anatomical and morphological Elix and McCarthy (1998), although the correct name evidence, Dal-Forno et al. (2016a) recently discovered that at that time was either D. pavonium (Sw.) Parm. specimens traditionally identified as the widespread (Parmasto 1978) or subsequently D. glabratum neotropical Acantholichen pannarioides include at least six (Spreng.) D. Hawksw. (Hawksworth 1988). distinct species. Specimens collected in the Galapagos 2. Dictyonema sericeum (Fr.) Mont. by Linder (1934), Islands are all genetically and morphologically distinct changed to Dictyonema guadalupense (Rabenh.) from A. pannarioides, and are now considered to belong to Zahlbr. by Weber (1986), which was followed by Elix a species considered endemic to the archipelago, accord- and McCarthy (1998), although the accepted name at ingly named A. galapagoensis Dal-Forno, Bungartz & the time was D. sericeum (Parmasto 1978). Lu¨cking. 123 Fungal Diversity (2017) 85:45–73 47 Given the extensive collections representing the Dicty- Information for all taxa not from the Galapagos is provided onema clade gathered by us in the Galapagos Islands and in Suppl. Tables 1 (concatenated dataset), 2 (Cora), 3 throughout the Neotropics and other regions of the world, (Cyphellostereum), and 4 (Dictyonema). For Acantholichen and reports of high levels of regional and local endemism this information has already been published by Dal-Forno in this clade from other Neotropical areas (Dal-Forno et al. et al. (2016a) and therefore it is not repeated here. 2013, 2016a;Lu¨cking et al. 2013a, b, 2014a, 2016; Vargas et al. 2014), we set out to test the following hypotheses: Morphological and anatomical studies (1) Are all species of the Dictyonema clade now Re-examination of the Galapagos specimens was performed reported
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