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Phylogeny, Taxonomy and Diversification Events in the Caliciaceae

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Phylogeny, Taxonomy and Diversification Events in the Caliciaceae Fungal Diversity (2017) 82:221–238 DOI 10.1007/s13225-016-0372-y Phylogeny, taxonomy and diversification events in the Caliciaceae Maria Prieto1,2 & Mats Wedin1 Received: 21 December 2015 /Accepted: 19 July 2016 /Published online: 1 August 2016 # The Author(s) 2016. This article is published with open access at Springerlink.com Abstract Although the high degree of non-monophyly and Calicium pinicola, Calicium trachyliodes, Pseudothelomma parallel evolution has long been acknowledged within the occidentale, Pseudothelomma ocellatum and Thelomma mazaediate Caliciaceae (Lecanoromycetes, Ascomycota), a brunneum. A key for the mazaedium-producing Caliciaceae is natural re-classification of the group has not yet been accom- included. plished. Here we constructed a multigene phylogeny of the Caliciaceae-Physciaceae clade in order to resolve the detailed Keywords Allocalicium gen. nov. Calicium fossil . relationships within the group, to propose a revised classification, Divergence time estimates . Lichens . Multigene . and to perform a dating study. The few characters present in the Pseudothelomma gen. nov available fossil and the complex character evolution of the group affects the interpretation of morphological traits and thus influ- ences the assignment of the fossil to specific nodes in the phy- Introduction logeny, when divergence time analyses are carried out. Alternative fossil assignments resulted in very different time es- Caliciaceae is one of several ascomycete groups characterized timates and the comparison with the analysis based on a second- by producing prototunicate (thin-walled and evanescent) asci ary calibration demonstrates that the most likely placement of the and a mazaedium (an accumulation of loose, maturing spores fossil is close to a terminal node rather than a basal placement in covering the ascoma surface). These are traits connected with the Calicium clade. Our dating analysis show two successive passive dispersal of the ascospores. For a long time, events giving rise to main clades of mazaediate taxa within the Caliciaceae was classified together with all other mazaediate Caliciaceae, in the Upper-Lower Cretaceous boundary and in the and otherwise similar fungi in the order Caliciales, a Paleocene. As a result of this study, Cyphelium is synonymized presumably monophyletic group among ascomycete fungi, with Calicium, Acolium is resurrected, and the new genera until Tibell (1984) suggested that most of the group was a Allocalicium and Pseudothelomma are described. Twelve new highly polyphyletic assemblage of taxa, which had developed combinations are proposed: Acolium karelicum, Acolium a mazaedium and passive spore dispersal independently. marcianum, Allocalicium adaequatum, Calicium carolinianum, Subsequent phylogenetic studies supported this view (Gargas Calicium lecideinum, Calicium lucidum, Calicium notarisii, and Taylor 1995; Gargas et al. 1995; Wedin and Tibell 1997; Lumbsch et al. 2004, 2009; Hibbett et al. 2007;Tehleretal. 2009; Prieto et al. 2013) showing that mazaediate fungi are * Maria Prieto clearly dispersed over the phylogenetic tree of Ascomycota. [email protected] The family Caliciaceae belongs to the Lecanoromycetes (Wedin and Tibell 1997), the largest class of lichenized 1 Department of Botany, Swedish Museum of Natural History, PO Box Fungi (Kirk et al. 2008). Despite the substantial recent ad- 50007, 10405 Stockholm, SE, Sweden vances in the understanding of Lecanoromycetes evolution 2 Departamento de Biología y Geología, Física y Química Inorgánica, at both supraordinal level (e.g. Lumbsch et al. 2004; Wedin Universidad Rey Juan Carlos, C/ Tulipan s/n; 28933 Mostoles, et al. 2005;Miadlikowskaetal.2006, 2014) and lower levels Madrid, Spain (i.e. family and genera, Baloch et al. 2010;Gayaetal.2012; 222 Fungal Diversity (2017) 82:221–238 Divakar et al. 2013; Singh et al. 2013; Otálora et al. 2014; including the Calicium viride group (Calicium s. str.), and Westberg et al. 2015;Resletal.2015)numerousgroupsare finally clade IV which includes the Acolium-clade, phylogenetically poorly understood and in great need of Tholurna-clade, and an odd Calicium species, C. nobile. further study, and the otherwise well-known Caliciaceae These four clades have unclear relationships to each other, is one of these. Caliciaceae forms a group with the non- and most lack obvious phenotypic characteristics to delimit mazaediate Physciaceae (Wedin et al. 2000, 2002). them. Although the Caliciaceae and Physciaceae have been sug- It is clear that the natural relationships within the gested to form the suborder Physciineae in the Teloschistales mazaediate Caliciaceae remain unresolved, and that several (Miadlikowska et al. 2006; Hibbett et al., 2007;Kirketal. of the mazaediate genera as currently understood are non- 2008; Lumbsch and Huhndorf 2010), recent classifications monophyletic and thus unnatural. It is still unclear whether tend to raise the Caliciaceae-Physciaceae group to ordinal lev- some of these mazaediate groups are more closely related to el (Gaya et al. 2012) using the name Caliciales. The opinion non-mazaediate groups within the Caliciaceae-Physciaceae on the family delimitation varies somewhat. If one prefers clade (Caliciales sensu Gaya et al. 2012). treating all Caliciaceae and Physciaceae as one family, the Adding a temporal dimension to the phylogeny may im- name Physciaceae was proposed for conservation (Wedin prove the phylogenetic reconstruction of phenotypic evolu- and Grube 2002) and should then be used. Recently, however, tion, by detecting causal events or processes in the underlying a two-family concept tends to be preferred (Gaya et al. 2012); phylogenetic diversity, and further by establishing a universal Caliciaceae, which includes the non-mazaediate genera with time-framework for biological classification that will facilitate Bacidia-type asci (the Buellia-group of Rambold et al. 1994; studies in comparative evolution (Avise 2009). Divergence e.g. the buellioid genera, Dirinaria and Pyxine; Wedin et al. time estimation has become increasingly prominent in evolu- 2002; Miadlikowska et al. 2006, 2014; Gaya et al. 2012), tionary biology, including in the study of several groups of together with all mazaediate genera in this group, and Ascomycota (Amo de Paz et al., 2011; Gueidan et al. 2011; Physciaceae, which includes taxa belonging to the BPhyscia- Prieto and Wedin 2013; Beimforde et al. 2014; Divakar et al. group^ of Rambold et al. (1994), characterized by Lecanora- 2015;Gayaetal.2015). Information used to calibrate a phy- type asci. Within the Caliciaceae the recognition of two sub- logenetic tree is obtained from three principal sources: (1) families has recently been proposed (Gaya et al. 2012): geological events; (2) estimates from independent molecular Calicioideae and Buellioideae, but this was very preliminary, dating studies; and (3) the fossil record, which normally is the based on a small taxon sampling, and it was rather unclear major source of calibration points (Forest 2009). There are, what other taxa should be included in the two groups in addi- however, several major complications in fungal dating analy- tion to the sampled ones. ses, among which the scarcity of fossils (Berbee and Taylor Tibell (2003) studied the generic delimitations in the 2010), the correct interpretation of the fossils available mazaediate Caliciaceae based on combined ITS and LSU (Kaasalainen et al. 2015), and in particular the unclear assign- rDNA data, where many details on the relationships within ment of fossils to specific nodes in the phylogeny (Forest this group were revealed. Five well-supported clades were 2009), are potential sources of errors. identified and informally called the Tholurna-clade, One fossil belonging to Calicium was described from Calicium glaucellum-clade, Calicium hyperelloides-clade, Baltic amber dating back 55–35 million years ago (Rikkinen Calicium viride-clade and the Cyphelium tigillare-clade (in 2003). The specimen is embedded in amber and is composed the ITS tree, the Acolium-clade was added, making a total of of a single detached ascoma with numerous spores. The six clades). Perhaps the most interesting results were that both ascoma consists of a smooth stalk with a broadly obconical Calicium and Cyphelium in the sense of Tibell (1984)were capitulum and a well-developed mazaedium without any vis- found to be non-monophyletic. In the ITS tree, Cyphelium ible pruina (something that could have been lost in the pres- inquinans and C. karelicum (the Acolium-clade) formed a ervation process), and with apparently roughly ornamented group with the monotypic Acroscyphus and Texosporium, spores. Although this fossil, in combination with other fossils, and a clade of Calicium adaequatum and Tholurna dissimilis was used in several dated phylogenies as a calibration point (the Tholurna-clade), but Cyphelium tigillare (type of (Prieto and Wedin 2013; Beimforde et al. 2014)andtheas- Cyphelium)andC. notarisii did not belong within that group. signment to Calicium is not disputed, the exact position within Calicium species were further distributed in four of the six Calicium is uncertain as there is no distinct morphological trait clades from the ITS tree. Tibell expanded these investigations suggesting a clear affinity to any group of extant species. in a larger paper on Himalayan Calicium species (Tibell 2006) In the present study, we produce a multilocus phylogeny of using ITS rDNA sequences, where he identified four well- the Caliciaceae-Physciaceae clade
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