Recent acquisition of Helicobacter pylori by Baka pygmies

Both anatomically modern humans and the gastric pathogen Helicobacter pylori originated in Africa, and both species have been associated for at least 100,000 years. Seven geographically distinct H. pylori populations exist, three of which are indigenous to Africa: hpAfrica1, hpAfrica2, and hpNEAfrica. The oldest and most divergent population, hpAfrica2, evolved within San hunter-gatherers, who represent one of the deepest branches of the human population tree. Anticipating the presence of ancient H. pylori lineages within all hunter-gatherer populations, we investigated the prevalence and population structure of H. pylori within Baka Pygmies in Cameroon. Gastric biopsies were obtained by esophagogastroduodenoscopy from 77 Baka from two geographically separated populations, and from 101 non-Baka individuals from neighboring agriculturalist populations, and subsequently cultured for H. pylori. Unexpectedly, Baka Pygmies showed a significantly lower H. pylori infection rate (20.8%) than non-Baka (80.2%). We generated multilocus haplotypes for each H. pylori isolate by DNA sequencing, but were not able to identify Baka-specific lineages, and most isolates in our sample were assigned to hpNEAfrica or hpAfrica1. The population hpNEAfrica, a marker for the expansion of the Nilo-Saharan language family, was divided into East African and Central West African subpopulations. Similarly, a new hpAfrica1 subpopulation, identified mainly among Cameroonians, supports eastern and western expansions of Bantu languages. An age-structured transmission model shows that the low H. pylori prevalence among Baka Pygmies is achievable within the timeframe of a few hundred years and suggests that demographic factors such as small population size and unusually low life expectancy can lead to the eradication of H. pylori from individual human populations. The Baka were thus either H. pylori-free or lost their ancient lineages during past demographic fluctuations. Using coalescent simulations and phylogenetic inference, we show that Baka almost certainly acquired their extant H. pylori through secondary contact with their agriculturalist neighbors.
Author Summary Genetic analyses of Helicobacter pylori have illuminated human migrations and the history of human infection by these bacteria. Both humans and H. pylori originated in Africa, and have been intimately associated for at least 100,000 years. We hypothesized that communities who still live in relative isolation might provide further details about the evolutionary history of H. pylori in Africa. We therefore investigated H. pylori within Baka Pygmies of southeast Cameroon, who live as hunter-gatherers in the tropical rainforest, and compared those bacteria to H. pylori from neighboring farming populations of non-Baka ethnicities. Unexpectedly, Baka Pygmies were much less commonly infected (20.8%) than the non-Baka (80.2%). H. pylori from hunter-gatherers and agriculturalists were genetically very similar and ancient H. pylori lineages were not identified in Baka. We used an epidemiological model to show that demographic factors including small population size and low life expectancy can account for the low infection rate among Baka Pygmies, and that this low rate could have been attained within a few hundred years of secondary contact with their neighbors. We also suggest that the ancestors of the Baka Pygmies were initially H. pylori-free or that their ancestral bacteria have been lost through past demographic fluctuations.