Low Effective Dispersal of Asexual Genotypes in Heterogeneous Landscapes by the Endemic Pathogen Penicillium marneffei

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Abstract
Long-distance dispersal in microbial eukaryotes has been shown to result in the establishment of populations on continental and global scales. Such “ubiquitous dispersal” has been claimed to be a general feature of microbial eukaryotes, homogenising populations over large scales. However, the unprecedented sampling of opportunistic infectious pathogens created by the global AIDS pandemic has revealed that a number of important species exhibit geographic endemicity despite long-distance migration via aerially dispersed spores. One mechanism that might tend to drive such endemicity in the face of aerial dispersal is the evolution of niche-adapted genotypes when sexual reproduction is rare. Dispersal of such asexual physiological “species” will be restricted when natural habitats are heterogeneous, as a consequence of reduced adaptive variation. Using the HIV-associated endemic fungus Penicillium marneffei as our model, we measured the distribution of genetic variation over a variety of spatial scales in two host species, humans and bamboo rats. Our results show that, despite widespread aerial dispersal, isolates of P. marneffei show extensive spatial genetic structure in both host species at local and country-wide scales. We show that the evolution of the P. marneffei genome is overwhelmingly clonal, and that this is perhaps the most asexual fungus yet found. We show that clusters of genotypes are specific to discrete ecological zones and argue that asexuality has led to the evolution of niche-adapted genotypes, and is driving endemicity, by reducing this pathogen's potential to diversify in nature. Scientists believe that micro-organisms are spread around the planet on currents of air, a hypothesis that is known as “ubiquitous dispersal”. While fungi release huge quantities of widely dispersed spores, it is not known why many species remain endemic to specific regions around the globe. Research by the authors suggests an answer to this conundrum, by investigating the genetic structure of a fungus, Penicillium marneffei, that causes disease in people with damaged immune systems. This research has shown that P. marneffei spores can be dispersed over a wide distance, but fail to penetrate the new environments that they find themselves in. This appears to be because the fungus has largely dispensed with sexual reproduction, which means that its ability to adapt to new challenges is limited. The authors use DNA typing to show that different “clones” of the fungus are associated with different environments, and suggest that adaptation to these environments is constraining the organism's ability to successfully disperse in nature. This may explain why P. marneffei is endemic to a relatively small area of southeast Asia, and the authors go on to suggest that the long-term consequence of this strategy may be the eventual extinction of the organism.