Cryptic Speciation in the Cosmopolitan and Clonal Human Pathogenic Fungus Aspergillus Fumigatus

Abstract

Microbes and other organisms smaller than one to a few millimeters in size are hypothesized to have global populations, in contrast to the geographically restricted ranges of larger organisms. However, fungi, which routinely have reproductive propagules no larger than 10 micrometers, challenge the generality of this hypothesis because recent studies have shown that globally distributed morphological species embrace two or more geographically restricted phylogenetic species. We used the concordance of gene genealogies to recognize phylogenetic species in the globally distributed opportunistic human pathogenic fungus, Aspergillus fumigatus. Based on DNA sequence data of five loci for each of 63 individuals collected from five continents, we have delineated two phylogenetic species in this single morphological species. Unlike all other fungi examined to date, both genetically isolated groups showed a global distribution with no evidence of a correlation between genotype and geographic location. Sexual reproduction has never been observed in A. fumigatus, but when the same data were used to explore the association of alleles at the five loci for one of the phylogenetic species, evidence was found to support recombination. The discovery of a cryptic species is medically relevant because different species are likely to differ in virulence or drug resistance. The discovery of a globally distributed A. fumigatus species clade highlights the need for ecological studies of the fungus to either document global dispersal or propose alternative mechanisms by which it persists as single, global phylogenetic population.

Insights into the genus Diaporthe: phylogenetic species delimitation in the D. eres species complex

“…Fungi are excellent models for studying eukaryotic evolution with many examples of highly diverse species complexes with multiple recently diverged sibling species (Dettman et al 2003bKohn 2005;Pringle et al 2005;Giraud et al 2008). The genus Diaporthe is composed of species varying from relatively host-specific to species with broad host ranges.…”

Eukaryotic microbes, species recognition and the geographic limits of species: examples from the kingdom Fungi

“…PSR and population structure were then investigated by two different research groups, each working with different worldwide collections of individuals and each employing different polymorphic DNA regions as population genetic markers (Pringle et al 2005;Rydholm et al 2006). Pringle et al (2005) assembled a collection of 63 A. fumigatus individuals from every continent except Antarctica and sequenced five polymorphic loci for each individual. They found two phylogenetic species, one comprising just five of the individuals.…”

“…These two research groups also investigated reproductive mode in A. fumigatus by population genetic means and neither of them were able to reject the null hypothesis of recombination (Pringle et al 2005;Rydholm et al 2006). In addition, Pö ggeler (2002), Dyer et al (2003) and Paoletti et al (2005) found that the genes known to be required for mating in fungi that can reproduce sexually in cultivation are also found in A. fumigatus.…”

“…However, as noted at the outset, far larger fungal spores can move from South Africa to Australia (Watson & De Sousa 1983), weakening the argument that the unique distribution of A. fumigatus is a consequence of its very small spores. The other hypothesis is that the environment favoured by A. fumigatus, composting vegetation, has been greatly expanded by human activity (Pringle et al 2005). If this hypothesis is correct, then A. fumigatus should show evidence of a recent population expansion.…”

Multigene phylogenetic and population differentiation data confirm the existence of a cryptic species within Chrysoporthe cubensis

“…Well-known examples of taxa harbouring cryptic species include Coccidioides immitis (Burt et al 1996;Koufopanou et al 2001), Aspergillus flavus (Geiser et al 1998), Aspergillus fumigatus (Pringle et al 2005), Fusarium subglutinans (Steenkamp et al 2002), Amanita muscaria (Geml et al 2006), Neofusicoccum parvum and Neofusicoccum ribis ( [Pavlic et al 2008;. These species are mainly separated based on DNA sequence comparisons, and in some cases diagnostic morphological characters have later been found to support their separation (Geiser et al 2000;Taylor et al 2000;O'Donnell et al 2004;Pavlic et al 2008).…”