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The metapopulation structure of Phytophthora infestans sensu lato is genetically diverse in the highlands of Ecuador. Previous reports documented the diversity associated with four putative clonal lineages of the pathogen collected from various hosts in the genus Solanum. This paper simultaneously analyzes diversity of the complete collection of isolates, including a large number that had not yet been reported. This analysis confirmed the existence of three pathogen populations, which all appear to be clonal lineages, and that correspond to those previously reported as US-l, EC-1, and EC-3. No evidence was found from the analyses of recently collected isolates that would contradict earlier reports about these three lineages. In contrast, new data from a group of isolates from several similar hosts caused us to modify the previous description of clonal lineage EC-2 and its previously proposed hosts, S. brevifolium and S. tetrapetalum. Given the uncertainty associated with the identification of these hosts, which all belong to the section Anarrhichomenum, we refer to them as the Anarrhichomenum complex, pending further taxonomic clarification. New pathogen genotypes associated with the Anarrhichomenum complex were isolated recently that are A1 mating type and Ia mitochondrial DNA (mtDNA) haplotype, and therefore differ from the previously described EC-2 lineage, which is A2 and Ic, respectively. Because of uncertainty on host identification, we do not know if the new genotypes are limited to one host species and therefore represent yet another host-adapted clonal lineage. For now, we refer to the new genotypes and previously described EC-2 genotypes, together, as the pathogen group attacking the Anarrhichomenum complex. Two A2 isolates identical to the previously described EC-2 archetype were collected from severely infected plants of pear melon (S. muricatum). Pear melon is generally attacked by US-1, and this is the first clear case we have documented in which two distinct pathogen genotypes have caused severe epidemics on the same host. Based on presence of unique marker alleles (restriction fragment length polymorphism [RFLP] and mtDNA) and genetic similarity analysis using RFLP and amplified fragment length polymorphism data, EC-3 and isolates from the Anarrhichomenum complex are genetically distinct from all genotypes of P. infestans that have been reported previously. No current theory of historical migrations for this pathogen can adequately support a Mexican origin for EC-3 and genotypes of the Anarrhichomenum complex and they may, therefore, be palaeoendemic to the Andean highlands. To date, we have identified 15 hosts in the genus Solanum, in addition to the Anarrhichomenum complex, and some unidentified species of P. infestans sensu lato in Ecuador. Five of the Solanum hosts are cultivated. One isolate was collected from Brugmansia sanguinea, which represents the first report from Ecuador of a host of this pathogen that is not in the genus Solanum. However, P. infestans sensu lato was only found on flower petals of B. sanguinea. This study provides new insights into the population structure of highly specialized genotypes of P. infestans sensu lato in the Andean highlands. The results are discussed in light of previous hypotheses regarding the geographic origin of the pathogen. [ABSTRACT FROM AUTHOR]