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

Matthew C Fisher,Nicholas J White,Michael D Smith,Sybren De Hoog,Elizabeth Johnson,William P Hanage,Nongnuch Vanittanakom

doi:10.1371/journal.ppat.0010020

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.

Highlights

In eukaryotes, sexual recombination is an almost universal phenomenon [1,2]
Such complexes are identified by eBURST as groups of genotypes that are linked by differing at only one out of the 21 multilocus microsatellite typing (MLMT) loci
Analysis of our MLMT dataset by eBURST showed that while 83 microsatellite type (MT) were specific to P. marneffei that had been recovered from HIV-positive patients, five MTs were found to infect both humans and bamboo rats (Figure 2)

Summary

Introduction

Sexual recombination is an almost universal phenomenon [1,2]. in many microbial eukaryotes, such as fungi, sexual reproduction is facultative, so loss-ofmeiosis mutations are effectively neutral. Modern ecological opinion holds that populations of microbial eukaryotes are huge owing to continent-wide dispersal via airborne spores; this is known as the ‘‘ubiquitous dispersal hypothesis’’ [4,5]. If this hypothesis is correct, the large value of Ne for these organisms will negate drift as a significant force in their evolution, and mating competence will be preserved. To understand why these fungi vary so widely in their ability to undergo successful long-distance aerial dispersal, we need to critically evaluate the ubiquitous dispersal hypothesis

Methods

Results

Conclusion