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

The taxonomic challenge posed by cryptic species (two or more distinct species classified as a single species) has been recognized for nearly 300 years, but the advent of relatively inexpensive and rapid DNA sequencing has given biologists a new tool for detecting and differentiating morphologically similar species. Here, we synthesize the literature on cryptic and sibling species and discuss trends in their discovery. However, a lack of systematic studies leaves many questions open, such as whether cryptic species are more common in particular habitats, latitudes or taxonomic groups. The discovery of cryptic species is likely to be non-random with regard to taxon and biome and, hence, could have profound implications for evolutionary theory, biogeography and conservation planning.

The evolutionary history of the phytopathogenic Gibberella fujikuroi complex of Fusarium and related species was investigated by cladistic analysis of DNA sequences obtained from multiple unlinked loci. Gene phylogenies inferred from the mitochondrial small subunit (mtSSU) rDNA, nuclear 28S rDNA, and beta-tubulin gene were generally concordant, providing strong support for a fully resolved phylogeny of all biological and most morphological species. Discordance of the nuclear rDNA internal transcribed spacer 2 (ITS2) gene tree is due to paralogous or xenologous ITS2 sequences. PCR and sequence analysis demonstrated that every strain of the ingroup species tested possesses two highly divergent nonorthologous ITS2 types designated type I and type II. Only the major ITS2 type, however, is discernable when PCR products are amplified and sequenced directly with conserved primers. The minor ITS2 type was recovered using ITS2 type-specific PCR primers. Distribution of the major ITS2 type within the species lineages exhibits a homoplastic pattern of evolution, thus obscuring true phylogenetic relationships. The results suggest that the ancestral ITS2 types may have arisen following an ancient interspecific hybridization or gene duplication which occurred prior to the evolutionary radiation of the Gibberella fujikuroi complex and related species of Fusarium. The results also indicate that current morphological-based taxonomic schemes for these fungi are unnatural and a new classification is required.

The operational species concept, i.e., the one used to recognize species, is contrasted to the theoretical species concept. A phylogenetic approach to recognize fungal species based on concordance of multiple gene genealogies is compared to those based on morphology and reproductive behavior. Examples where Phylogenetic Species Recognition has been applied to fungi are reviewed and concerns regarding Phylogenetic Species Recognition are discussed.