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

Abstract

The claim that eukaryotic micro-organisms have global geographic ranges, constituting a significant departure from the situation with macro-organisms, has been supported by studies of morphological species from protistan kingdoms. Here, we examine this claim by reviewing examples from another kingdom of eukaryotic microbes, the Fungi. We show that inferred geographic range of a fungal species depends upon the method of species recognition. While some fungal species defined by morphology show global geographic ranges, when fungal species are defined by phylogenetic species recognition they are typically shown to harbour several to many endemic species. We advance two non-exclusive reasons to explain the perceived difference between the size of geographic ranges of microscopic and macroscopic eukaryotic species when morphological methods of species recognition are used. These reasons are that microbial organisms generally have fewer morphological characters, and that the rate of morphological change will be slower for organisms with less elaborate development and fewer cells. Both of these reasons result in fewer discriminatory morphological differences between recently diverged lineages. The rate of genetic change, moreover, is similar for both large and small organisms, which helps to explain why phylogenetic species of large and small organisms show a more similar distribution of geographic ranges. As a consequence of the different rates in fungi of genetic and morphological changes, genetic isolation precedes a recognizable morphological change. The final step in speciation, reproductive isolation, also follows genetic isolation and may precede morphological change.

Figure 1

(a) Phylogenetic species recognition applied to Neurospora and a graphic comparison to biological species recognition applied to the same individuals. Maximum-parsimony (MP) phylogram produced from the combined analysis of DNA sequences from four anonymous nuclear loci (TMI, DMG, TML and QMA loci, a total of 2141 aligned nucleotides). Tree length =916 steps; consistency index =0.651. Labels to the right of the phylogram indicate groups identified by phylogenetic species recognition and biological species recognition. Triangles at nodes indicate that all taxa united by (or distal to) a node belong to the same phylogenetic species. Taxon labels indicate strain number and geographic source. Branch support values for major branches with significant support are indicated by numbers above or below the branches (MP bootstrap proportions/Bayesian posterior probabilities). Figure and legend adapted from Dettman et al. (2003b) with permission of the authors and publisher. (b) Summary of results of phylogenetic species recognition in Neurospora. Neighbour-joining phylogram produced from three loci combined (DMG, TMI and TML) using exemplars of described species, and new phylogenetic species of Neurospora. Figure and legend adapted from Dettman et al. (in press) with permission of the authors and publisher.

Figure 1

(a) Phylogenetic species recognition applied to Neurospora and a graphic comparison to biological species recognition applied to the same individuals. Maximum-parsimony (MP) phylogram produced from the combined analysis of DNA sequences from four anonymous nuclear loci (TMI, DMG, TML and QMA loci, a total of 2141 aligned nucleotides). Tree length =916 steps; consistency index =0.651. Labels to the right of the phylogram indicate groups identified by phylogenetic species recognition and biological species recognition. Triangles at nodes indicate that all taxa united by (or distal to) a node belong to the same phylogenetic species. Taxon labels indicate strain number and geographic source. Branch support values for major branches with significant support are indicated by numbers above or below the branches (MP bootstrap proportions/Bayesian posterior probabilities). Figure and legend adapted from Dettman et al. (2003b) with permission of the authors and publisher. (b) Summary of results of phylogenetic species recognition in Neurospora. Neighbour-joining phylogram produced from three loci combined (DMG, TMI and TML) using exemplars of described species, and new phylogenetic species of Neurospora. Figure and legend adapted from Dettman et al. (in press) with permission of the authors and publisher.

Figure 2

Phylogenetic species recognition applied to Saccharomyces cerevisiae. Unrooted distance trees based on four loci combined (CDC 19, FZF1, SSU1 and PHD1). Support of internal branches given as bootstrap percentages from 10 000 resamplings of the data. Construction of trees from the same data using the parsimony optimality criterion yielded trees with essentially the same topology. Figure and legend adapted from Aa et al. (2006) with permission of the authors and publisher.

Figure 3

Phylogenetic species recognition applied to Schizophyllum commune based on IGS1 sequence data and heuristic parsimony analysis. Heuristic searches found 9700 equally parsimonious trees. Cartoon of one of 9700 equally parsimonious trees is shown (tree length =285 steps; CI =0.795). Clades are represented by triangles and large clades, NAM, SAM and EAS, represent phylogenetic species. Detailed trees with branch support are to be found in James et al. 2001. Figure and legend modified from those in James et al. (2001) with permission of the authors and publisher.

Figure 4

Phylogenetic species recognition applied to Lentinula based on ITS sequences. Strict consensus of 3000+ most parsimonious trees (tree length =234 steps; CI=0.861). Bootstrap values greater than 70% are shown above the branches. Numbered groups are phylogenetic species of Lentinula. Morphologically recognized species names are at right. PNG=Papua New Guinea. Figure and legend based on those in Hibbett (2001) with permission of the authors and publisher.

Figure 5

Neurospora mating success for sympatric and allopatric heterospecific pairings: the percentage of heterospecific matings between allopatric or sympatric individuals that reached the successive categories of reproductive success. At all geographic scales (regional, sub-regional and local), allopatric matings were significantly more likely than sympatric matings to proceed through the consecutive stages of the sexual cycle. The discrepancy between the allopatric and sympatric curves increases as the scale of sympatry decreases and is most pronounced for local sympatry, shown here. Categories of reproductive success: 0, no response; 1, aborted perithecia; 2, perithecia with no ascospores ejected; 3, perithecia with less than 1% of ejected ascospores having strongly melanized (i.e. black) walls; 4, perithecia with less than 15% black ascospores; 5, perithecia with less than 50% black ascospores; 6, perithecia with more than 50% black ascospores. Figure and legend modified from Dettman et al. (2003b) with permission of the authors and publisher.

Figure 6

Phylogenetic species recognition applied to Aspergillus fumigatus. Bayesian analysis of five loci combined with separate substitution models for each partition. Parsimony bootstrap support above 70% is given in bold. Bayesian posterior probability above 90 is italicized. The phylogeny is rooted using Neosartorya fischeri as an outgroup. Figure and legend modified from Pringle et al. (2005) with permission of the authors and publisher.

Figure 7

A graphical depiction of a plausible explanation for the differences observed between studies of microbial endemism using PSR, BSR and MSR: morphological characters evolve more slowly than those used for PSR or BSA, thereby recognizing taxonomic groups broader than species and masking endemism. (a) The observation of Finlay & Fenchel that the percent of morphospecies that are cosmopolitan is much higher in smaller organisms, with a sharp point of inflexion ca 1–10 mm. Data from fungi suggest that morphological characters evolve more slowly in small organisms, thereby recognizing coarser taxonomic groups and obscuring endemism. (b) Relationship between rate of character evolution and taxonomic resolution. Faster evolving characters yield greater resolution for more refined taxonomic distinctions. Slower evolving characters yield greater resolution for coarser taxonomic distinctions. PSR is usually performed on characters that are polymorphic among isolates, and thus it is appropriate for resolution of species. BSR is implicitly performed on reproductive isolating factors, which generally evolve rapidly and are naturally appropriate for the resolution of biological species. MSR, like PSR, is ideally performed on characters that are polymorphic among isolates. However, if no or few morphological characters are polymorphic among isolates, morphospecies will map to coarser taxonomic groups than the species observed by BSR and PSR.