Providing Scale to a Known Taxonomic Unknown—At Least a 70-Fold Increase in Species Diversity in a Cosmopolitan Nominal Taxon of Lichen-Forming Fungi

Abstract

Robust species delimitations provide a foundation for investigating speciation, phylogeography, and conservation. Here we attempted to elucidate species boundaries in the cosmopolitan lichen-forming fungal taxon Lecanora polytropa. This nominal taxon is morphologically variable, with distinct populations occurring on all seven continents. To delimit candidate species, we compiled ITS sequence data from populations worldwide. For a subset of the samples, we also generated alignments for 1209 single-copy nuclear genes and an alignment spanning most of the mitochondrial genome to assess concordance among the ITS, nuclear, and mitochondrial inferences. Species partitions were empirically delimited from the ITS alignment using ASAP and bPTP. We also inferred a phylogeny for the L. polytropa clade using a four-marker dataset. ASAP species delimitations revealed up to 103 species in the L. polytropa clade, with 75 corresponding to the nominal taxon L. polytropa. Inferences from phylogenomic alignments generally supported that these represent evolutionarily independent lineages or species. Less than 10% of the candidate species were comprised of specimens from multiple continents. High levels of candidate species were recovered at local scales but generally with limited overlap across regions. Lecanora polytropa likely ranks as one of the largest species complexes of lichen-forming fungi known to date.

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“…This is very different to what we encountered in previous macrolichen surveys (112)(113)(114)(115)(116)(117) where species tend to comprise: a) few closely related haplotypes, identifiable as discrete lineages in phylogenetic trees and network reconstructions and b) few overrepresented haplotypes common across large geographic regions (115,118,119). The observed phylogenetic continuum is similar to that of Lecanora polytropa, a species complex proposed to comprise 70 putative species worldwide (62). Interpreting diverging genotypes as separate species artificially inflates the estimates of species diversity.…”

“…The morphological study resulted in identifying 42 operational units (species and pseudospecies) of which twelve were collected outside of the main study area, nine are clearly identifiable, three have been described based on molecular characters and are doubtful (Figure 1a) and the remaining eighteen show intermediate character combinations and are difficult to place, being potentially undescribed species. The consensus in lichenology is that molecular taxonomic methods are necessary to overcome the bias introduced by overly simple and subjective morphological species concepts (52,62). To address diversity, most surveys follow a similar recipe (63): assembling a phylogenetic dataset, proposing a set of operational taxonomic units (OTUs), which are finally validated using a multilocus framework, often based on multispecies coalescent (107)(108)(109)(110) or an analogous strategy (111).…”

“…The consensus in lichenology is that molecular taxonomic methods are necessary to overcome the bias introduced by overly simple and subjective morphological species concepts ( 52 , 62 ). To address diversity, most surveys follow a similar recipe ( 63 ): assembling a phylogenetic dataset, proposing a set of operational taxonomic units (OTUs), which are finally validated using a multilocus framework, often based on multispecies coalescent ( 107 – 110 ) or an analogous strategy ( 111 ).…”

“…The limitations of phylogenetic methods of species delimitation are well known ( 31 ) and have been thoroughly discussed in the fungal literature ( 52 ), despite which they remain useful for species discovery ( 62 , 63 ). Most models used in species delimitation rely on strong assumptions about the contribution that reproductive isolation, genetic drift, and mutation have to the genetic variability at macro and microevolutionary levels.…”

“…To open the treasure chest of fungal diversity, molecular taxonomists progressively incorporated growingly complex methods of unsupervised species discovery and validation (53)(54)(55)(56)(57)(58)(59)(60)(61). However, recent surveys tone down notably the former claims made on the extent of fungal diversity (62) former claims on hidden fungal diversity. In addition to the known limitations of DNA barcoding when used for species delimitation, validation, and recognition (63), phylogenetic methods of species delimitation (31), despite their progressive refinement (64)(65)(66)(67)(68)(69)(70)(71), are quite limited in their application and share the same caveats.…”