An Andean origin of Phytophthora infestans inferred from mitochondrial and nuclear gene genealogies

Abstract

Phytophthora infestans (Mont.) de Bary caused the 19th century Irish Potato Famine. We assessed the genealogical history of P. infestans using sequences from portions of two nuclear genes (beta-tubulin and Ras) and several mitochondrial loci P3, (rpl14, rpl5, tRNA) and P4 (Cox1) from 94 isolates from South, Central, and North America, as well as Ireland. Summary statistics, migration analyses and the genealogy of current populations of P. infestans for both nuclear and mitochondrial loci are consistent with an "out of South America" origin for P. infestans. Mexican populations of P. infestans from the putative center of origin in Toluca Mexico harbored less nucleotide and haplotype diversity than Andean populations. Coalescent-based genealogies of all loci were congruent and demonstrate the existence of two lineages leading to present day haplotypes of P. infestans on potatoes. The oldest lineage associated with isolates from the section Anarrhichomenun including Solanum tetrapetalum from Ecuador was identified as Phytophthora andina and evolved from a common ancestor of P. infestans. Nuclear and mitochondrial haplotypes found in Toluca Mexico were derived from only one of the two lineages, whereas haplotypes from Andean populations in Peru and Ecuador were derived from both lineages. Haplotypes found in populations from the U.S. and Ireland was derived from both ancestral lineages that occur in South America suggesting a common ancestry among these populations. The geographic distribution of mutations on the rooted gene genealogies demonstrate that the oldest mutations in P. infestans originated in South America and are consistent with a South American origin.

Fig. 1.

The rooted coalescent-based gene genealogy showing the distribution of mutations for South American (SA: Peru, Ecuador, Bolivia, Brazil) and non-South American (NSA: Costa Rica, Mexico, U.S., Ireland) populations for the mitochondrial (P3+P4) loci of Phytophthora infestans generated using GENETREE (32). Time scale is in coalescent units of effective population size. The direction of divergence is from the top (past–oldest) to the bottom (present–youngest). The numbers below the tree from top to bottom designate each distinct haplotype and its count (i.e., the number of occurrences of the haplotype in the sample), the count of each haplotype in each population, the mating type of the isolates, and the mtDNA haplotype (33). Maximum likelihood estimates of the tree with the highest root probability, standard deviation (SD) and Watterson's theta (55) were as follows: Likelihood = 3.5848 ×10⁻²², SD = 4.3213 ×10⁻¹⁹, theta = 5.0. Estimates were based on 10 million coalescent simulations and five independent runs to ensure convergence. Simulations were performed assuming constant population size.

Fig. 2.

The rooted coalescent-based gene genealogy showing the distribution of mutations for South American (SA: Peru, Ecuador, Bolivia, Brazil) and non-South American (NSA: Costa Rica, Mexico, U.S., Ireland) populations for the IRRAS locus of Phytophthora infestans generated using GENETREE (32). Time scale is in coalescent units of effective population size. The direction of divergence is from the top (past–oldest) to the bottom (present–youngest). The numbers below the tree from top to bottom designate each distinct haplotype and its count (i.e., the number of occurrences of the haplotype in the sample), the count of each haplotype in each population, the mating type of the isolates, and the mtDNA haplotype (33). Maximum likelihood estimates of the tree with the highest root probability, standard deviation (SD) and Watterson's theta (55) were as follows: Likelihood = 3.5320 × 10⁻²³, SD = 4.8689 × 10⁻²⁰, theta = 2.0. Estimates were based on 10 million coalescent simulations and five independent runs to ensure convergence. Simulations were performed assuming constant population size.