Phylogeography of Toxoplasma gondii points to a South American origin

Toxoplasma gondii, a protozoan found ubiquitously in mammals and birds, is the etiologic agent of toxoplasmosis, a disease causing substantial public health burden worldwide, including about 200,000 new cases of congenital toxoplasmosis each year. Clinical severity has been shown to vary across geographical regions, with South America exhibiting the highest burden. Unfortunately, the drivers of these heterogeneities are still poorly understood, and the geographical origin and historical spread of the pathogen worldwide are currently uncertain. A worldwide sample of 168 T. gondii isolates gathered in 13 populations was sequenced for five fragments of genes (140 single nucleotide polymorphisms from 3153bp per isolate). Phylogeny based on Maximum likelihood methods with estimation of the time to the most recent common ancestor (TMRCA) and geostatistical analyses were performed for inferring the putative origin of T. gondii. We show that extant strains of the pathogen likely evolved from a South American ancestor, around 1.5 million years ago, and reconstruct the subsequent spread of the pathogen worldwide. This emergence is much more recent than the appearance of ancestral T. gondii, believed to have taken place about 11 My ago, and follows the arrival of felids in this part of the world. We posit that an ancestral lineage of T. gondii likely arrived in South America with felids and that the evolution of oral infectivity through carnivorism and the radiation of felids in this region enabled a new strain to outcompete the ancestral lineage and undergo a pandemic radiation.