The Irish potato famine pathogen Phytophthora infestans originated in central Mexico rather than the Andes

Abstract

Phytophthora infestans is a destructive plant pathogen best known for causing the disease that triggered the Irish potato famine and remains the most costly potato pathogen to manage worldwide. Identification of P. infestan's elusive center of origin is critical to understanding the mechanisms of repeated global emergence of this pathogen. There are two competing theories, placing the origin in either South America or in central Mexico, both of which are centers of diversity of Solanum host plants. To test these competing hypotheses, we conducted detailed phylogeographic and approximate Bayesian computation analyses, which are suitable approaches to unraveling complex demographic histories. Our analyses used microsatellite markers and sequences of four nuclear genes sampled from populations in the Andes, Mexico, and elsewhere. To infer the ancestral state, we included the closest known relatives Phytophthora phaseoli, Phytophthora mirabilis, and Phytophthora ipomoeae, as well as the interspecific hybrid Phytophthora andina. We did not find support for an Andean origin of P. infestans; rather, the sequence data suggest a Mexican origin. Our findings support the hypothesis that populations found in the Andes are descendants of the Mexican populations and reconcile previous findings of ancestral variation in the Andes. Although centers of origin are well documented as centers of evolution and diversity for numerous crop plants, the number of plant pathogens with a known geographic origin are limited. This work has important implications for our understanding of the coevolution of hosts and pathogens, as well as the harnessing of plant disease resistance to manage late blight.

Keywords: biological invasion; coalescent analysis; oomycete; population genetics; stramenopile.

Fig. 1.

Population structure of Mexico and Andes samples of P. infestans inferred using structure (32). (A) The Mexico sample shows admixed individuals assigned to K = 4 clusters. Isolates collected from patches of S. demissum are in bold type. Based on the index of association, I_A, there is no evidence of linkage disequilibrium among loci (P = 0.25), consistent with a sexually recombining population. (B) The Andes sample clusters into K = 2 distinct clades with little or no admixture. The hypothesis of no linkage among markers is rejected (P < 0.001), indicating a clonal population.

Fig. 2.

Root state probabilities by country inferred using BEAST (33). (A) Summarized maximum clade credibility phylogeny of Phytophthora clade 1c species. Colors of branches indicate the most probable geographic origin of each lineage. Posterior probabilities of major branches supporting the tree topology are shown below each branch. Root state posterior probabilities indicate that Mexico is the most probable origin of clade 1c (B) and P. infestans (C).

Fig. 3.

Estimated marginal posterior probabilities of relative divergence times in pairwise comparisons among Andes clonal lineages (EC-1, PE-3, PE-7, and US-1) and the Mexico population estimated using IMa (64). Smaller means and modes of the scaled time since divergence indicate more recent divergence of lineages. Lineages EC-1, PE-3, and PE-7 show more recent divergence from one another than from US-1 and Mexico.

Fig. 4.

Scenarios for the evolution of P. infestans in the Andes tested using ABC in DIYABC (35). Shown are the scenarios with the highest posterior probabilities out of 15 scenarios testing the relationships of PE-3, PE-7, and EC-1 lineages, in turn, to the US-1 lineage and Toluca Valley population (SI Appendix, Fig. S10). Present-day populations are at the base of the tree schematic. Ancestral relationships among these populations are represented by lines intersecting in the past, with the vertex of the schematic representing the most recent common ancestor of all samples. Horizontal lines indicate admixture events between the ancestral populations connected by the horizontal line. Potential changes in population size over time are indicated by changes in line thickness, but line thickness is not proportional to population size. The dashed line represents an unsampled population that has contributed to the genetic variation observed in sampled populations. (A) For PE-3, the most probable scenario includes an admixture of US-1 and an unsampled population, leading to the PE-3 lineage. (B and C) For PE-7, support is split between two scenarios containing an admixture event with an unsampled population. (D and E) For EC-1, the scenarios with the greatest support showed a simple divergence from the Toluca population or an admixture between Toluca and an unsampled population. Posterior probabilities for all tested scenarios and their 95% confidence intervals are given in SI Appendix, Table S4.

Fig. 5.

Final three scenarios used to examine the relationships between the Toluca Valley population and EC-1, PE-3, and US-1 lineages in the Andes by ABC. Tree schematics are drawn as in Fig. 4. The three scenarios are simple divergence of populations such that PE-3 is an ancestral lineage (A); emergence of the PE-3 lineage after an admixture of US-1 and an unsampled population (B); and scenario B plus emergence of the EC-1 by an admixture between the Toluca population and an unsampled population (C). Scenario B was the most likely of the three, with a posterior probability of 0.74. The 95% confidence intervals for the posterior probabilities are in brackets.