Abstract
The apparent rarity of sex in many fungal species has raised questions about how much sex is needed to purge deleterious mutations and how differences in frequency of sex impact fungal evolution. We sought to determine how differences in the extent of recombination between populations of Aspergillus flavus impact the evolution of genes associated with the synthesis of aflatoxin, a notoriously potent carcinogen. We sequenced the genomes of, and quantified aflatoxin production in, 94 isolates of A. flavus sampled from seven states in eastern and central latitudinal transects of the United States. The overall population is subdivided into three genetically differentiated populations (A, B, and C) that differ greatly in their extent of recombination, diversity, and aflatoxin-producing ability. Estimates of the number of recombination events and linkage disequilibrium decay suggest relatively frequent sex only in population A. Population B is sympatric with population A but produces significantly less aflatoxin and is the only population where the inability of nonaflatoxigenic isolates to produce aflatoxin was explained by multiple gene deletions. Population expansion evident in population B suggests a recent introduction or range expansion. Population C is largely nonaflatoxigenic and restricted mainly to northern sampling locations through restricted migration and/or selection. Despite differences in the number and type of mutations in the aflatoxin gene cluster, codon optimization and site frequency differences in synonymous and nonsynonymous mutations suggest that low levels of recombination in some A. flavus populations are sufficient to purge deleterious mutations.IMPORTANCE Differences in the relative frequencies of sexual and asexual reproduction have profound implications for the accumulation of deleterious mutations (Muller's ratchet), but little is known about how these differences impact the evolution of ecologically important phenotypes. Aspergillus flavus is the main producer of aflatoxin, a notoriously potent carcinogen that often contaminates food. We investigated if differences in the levels of production of aflatoxin by A. flavus could be explained by the accumulation of deleterious mutations due to a lack of recombination. Despite differences in the extent of recombination, variation in aflatoxin production is better explained by the demography and history of specific populations and may suggest important differences in the ecological roles of aflatoxin among populations. Furthermore, the association of aflatoxin production and populations provides a means of predicting the risk of aflatoxin contamination by determining the frequencies of isolates from low- and high-production populations.
Highlights
The apparent rarity of sex in many fungal species has raised questions about how much sex is needed to purge deleterious mutations and how differences in frequency of sex impact fungal evolution
The remaining isolate was identified as Aspergillus texensis, a recently described S-type species closely related to A. flavus [34]
The Frequency of Sex in Aspergillus flavus evident in our neighbor-net network (Fig. S6 in reference 33) emphasize that genetic distances to this closely related species are of much larger magnitude than those we find between populations of A. flavus
Summary
The apparent rarity of sex in many fungal species has raised questions about how much sex is needed to purge deleterious mutations and how differences in frequency of sex impact fungal evolution. Understanding how much recombination is needed to purge deleterious mutations in these species is further complicated, as the relative frequencies of sexual and clonal reproduction may vary among different populations [9]. There is evidence that the heterothallic plant-pathogenic ascomycete Aspergillus flavus comprises several genetically isolated sympatric populations in the United States that appear to differ in their relative degrees of recombination and clonality [13, 14]. The idea that A. flavus may be predominantly sexual [21] is difficult to reconcile with a large body of evidence about the predominantly asexual nature of this fungus These field studies occurred on very short timelines and do not capture whether the fitness of recombinant progeny is reduced by the disassociation of coadapted traits (i.e., recombination load), and sexual reproduction makes little contribution to the overall population. While some subdivision in the A. flavus population of the United States is evident, the importance of recombina-
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