Biogeographic range expansion into South America by Coccidioides immitis mirrors New World patterns of human migration

Abstract

Long-distance population dispersal leaves its characteristic signature in genomes, namely, reduced diversity and increased linkage between genetic markers. This signature enables historical patterns of range expansion to be traced. Herein, we use microsatellite loci from the human pathogen Coccidioides immitis to show that genetic diversity in this fungus is geographically partitioned throughout North America. In contrast, analyses of South American C. immitis show that this population is genetically depauperate and was founded from a single North American population centered in Texas. Variances of allele distributions show that South American C. immitis have undergone rapid population growth, consistent with an epidemic increase in postcolonization population size. Herein, we estimate the introduction into South America to have occurred within the last 9,000-140,000 years. This range increase parallels that of Homo sapiens. Because of known associations between Amerindians and this fungus, we suggest that the colonization of South America by C. immitis represents a relatively recent and rapid codispersal of a host and its pathogen.

Figure 1

Neighbor-joining tree of pairwise allele-sharing genetic distances calculated with the program MICROSAT. Tree construction was performed with programs in the PHYLIP package (36). The isolate marked with an asterisk signifies a patient who was diagnosed in Texas but was subsequently found to have acquired the infection in California (42). The tree is mid-point rooted, and the scale bar signifies 0.1 changes. CA, Californian; non-CA, non-Californian.

Figure 2

Unrooted phylogenetic tree of the 21 isolates sequenced at the following three loci: deoxygenase, serine proteinase, and chitinase. Distance trees were calculated with PAUP* 4.0 (35). The scale bar signifies 0.05% nucleotide divergence.

Figure 3

Scatterplots of genetic and geographical distances separating each pairwise combination of populations. CA populations are signified by circles; North American non-CA populations by filled diamonds; and South American non-CA populations by open diamonds. The regression line is dotted for CA (P = 0.16, not significant), solid for non-CA excluding the South American isolates (P = 0.017, significant), and dashed for non-CA including the South American isolates (P = 0.362, not significant).