Population Structure and Genetic Diversity among Isolates of Coccidioides posadasii in Venezuela and Surrounding Regions

Abstract

Coccidioides posadasii is a pathogenic fungus that causes coccidioidomycosis in many arid regions of the Americas. One of these regions is bordered by the Caribbean Sea, and the surrounding landscape may play an important role in the dispersion of C. posadasii across South America through southeastern Mexico, Honduras, Guatemala, and Venezuela. Comparative phylogenomic analyses of C. posadasii reveal that clinical strains from Venezuela are genetically distinct from the North American populations found in (i) Arizona and (ii) Texas, Mexico, and the rest of South America (TX/MX/SA). We find evidence for admixture between the Venezuela and the North American populations of C. posadasii in Central America. Additionally, the proportion of Venezuelan alleles in the admixed population decreases as latitude (and distance from Venezuela) increases. Our results indicate that the population in Venezuela may have been subjected to a recent bottleneck and shows a strong population structure. This analysis provides insight into potential for Coccidioides spp. to invade new regions.IMPORTANCE Valley Fever is a fungal disease caused by two species of fungi: Coccidioides immitis and C. posadasii These fungi are found throughout the arid regions of North and South America; however, our understanding of genetic diversity and disease in South America is limited. In this report, we analyze 10 new genomes of Coccidioides posadasii from regions bordering the Caribbean Sea. We show that these populations are distinct and that isolates from Venezuela are likely a result of a recent bottleneck. These data point to patterns that might be observed when investigating recently established populations.

Keywords: Caribbean; Coccidioides posadasii; Valley Fever; Venezuela; coccidioidomycosis.

FIG 1

Maximum likelihood (ML) phylogenomic analyses among members of the C. posadasii complex. The ML tree was rooted with the C. immitis strain 202, and clades are displayed proportionally to the branch length of the clades since the majority of SNPs are derived from the overall C. posadasii/C. immitis divergence. Dual branch support was evaluated using 1,000 ultrafast bootstraps coupled with a Shimodaira-Hasegawa-like approximate likelihood ratio test and are displayed next to the clades. The approximate location of collection of each strain was added next to the taxon that represents the country (full names) or the American states as follows: Arizona (AZ); Nevada (NV), Texas (TX), Colorado (CO), Washington (WA), and Florida (FL).

FIG 2

Principal-component analysis (PCA) reveals population structure of C. posadasii. (A) PCA, including C. immitis and C. posadasii. PC1 (75.34%) separates species of Coccidioides, while PC2 (3.03%) suggests the existence of cryptic populations within C. posadasii. (B) PCA, including only isolates from C. posadasii. PC1 (14.26%) coordinates separates isolates from Venezuela and isolates from the rest of the geographic range. PC2 (8.52%) discriminates the TX/MX/SA and Arizona populations. The insets on each panel show the eigenvalues that were used to plot the two principal coordinates. (Asterisks represent the first 2 PCs.)

FIG 3

Strong population structure within C. posadasii. Population structure plots based on Bayesian posterior probabilities implemented in fastSTRUCTURE. We did the analysis in two ways, first using C. immitis as an outgroup for C. posadasii or using only C. posadasii strains. Each row represents an individual. The heights and colors of percentage of each population represent the probability of belonging to a given cluster.

FIG 4

Within-species admixture in C. posadasii. (A) Cross-validation error learning curve of the log likelihood values collected by ADMIXTURE from K = 1 to K = 8 population scenarios. (B) Individual admixture proportions of C. posadasii isolates as inferred with ADMIXTURE. The height and colors of percentage of each population represent the probability of a given strain belonging to a given population. (C) The proportion of the Venezuela admixture decreases as the distance from Caracas increases.