Species delimitation and evolution of metal bioaccumulation in the lichenized Acarospora smaragdula (Ascomycota, Fungi) complex

Abstract

The crustose lichenized fungi in the Acarosporaceae are splendid examples of organisms managing to survive in extremely harsh environments, such as highly mineralized rocks and low-pH habitats. Some representatives of the Acarospora smaragdula complex are known to accumulate substantial amounts of potentially toxic metals including iron and copper, resulting in populations with highly divergent coloration and morphology. These populations have often been treated as distinct species by lichen taxonomists. Parsimony and parsimony jackknifing analyses of b-tubulin, nuclear ITS rDNA, and mtSSU rDNA sequence data sets was used to investigate the evolution of iron and copper accumulation and the production of the secondary compound norstictic acid in populations within the A. smaragdula species complex in Sweden, with additional samples mainly from Norway and the UK. Phylogenetic species recognition (concordance of single-gene phylogenies) was used to investigate species delimitations. Seven species are recognized in the complex. Atypically green, copper-accumulating samples, often given species rank, do not form a distinct group but are nested within A. smaragdula s. str., indicating that this ability is widespread in this species. Rust-coloured, iron-accumulating samples form two well supported separate groups, indicating that two morphologically distinct, obligate, ironaccumulating species are present, but facultatively iron-accumulating populations occur in at least one additional species. Norstictic acid, sometimes claimed to characterize the whole A. smaragdula complex, is only present in A. smaragdula s. str. The evolutionary significance of metal accumulation in Acarospora is discussed, as is the significance of our results for the application of phylogenetic species recognition ⁄ gene tree concordance-based species recognition, and DNA barcoding.

Goodbye morphology? A paradigm shift in the delimitation of species in lichenized fungi

“…It may be expected to find cryptic species among the morphologically simple crustose lichens. These include for example, fungi in Acarosporaceae (Wedin et al 2009), Graphidaceae , and Lecanoraceae (Leavitt et al 2011c), Lecideaceae (Ruprecht et al 2010), and Teloschistaceae (Muggia et al 2008;Vondrak et al 2009); cryptic species with subtle morphological or chemical differences have also frequently found in foliose and fruticose lichens. These include, for example, species complexes in Lobariaceae (McDonald et al 2003), several genera in Parmeliaceae (Kroken and Taylor 2001;Molina et al 2004;Divakar et al 2005b;Seymour et al 2007;Wirtz et al 2008;McCune and Schoch 2009), Peltigeraceae (Goffinet et al 2003;O'Brien et al 2009), some genera in Physciaceae (Cubero et al 2004;Divakar et al 2007;Lücking et al 2008;Elix et al 2009), and Sphaerophoraceae (Högnabba and Wedin 2003).…”

Lichen Systematics: The Role of Morphological and Molecular Data to Reconstruct Phylogenetic Relationships

“…Because the morphological variability within the large genus Acarospora is still poorly understood, species delimitations are uncertain. Wedin et al (2009) found seven phylogenetic species within the A. smaragdula complex, of which most were morphologically well characterized.…”

Hidden diversity in the morphologically variable script lichen (Graphis scripta) complex (Ascomycota, Ostropales, Graphidaceae)

“…Traditional taxonomic treatments within the family largely rely on chemistry, apothecium shape, and ascospore morphology (Staiger 2002). Molecular data on other lichenized fungal lineages have shown that the classification based on these characters usually underestimates the number of distinct lineages under a single taxonomic name (Crespo and Lumbsch 2010;Crespo and Ortega 2009;Hodkinson and Lendemer 2011;McCune and Schoch 2009;Ruprecht et al 2010;Spribille et al 2011;Vondrák 2012;Wedin et al 2009). Within Graphidaceae, traits traditionally used for classification were shown to have evolved independently several times (Lumbsch et al 2014;Rivas Plata and Lumbsch 2011).…”