A unique Toxoplasma gondii haplotype under strong selection has accompanied domestic cats in their global expansion

Abstract

ABSTRACTToxoplasma gondii is a cyst-forming apicomplexan parasite of virtually all warm-blooded species, with all true cats (Felidae) as definitive hosts. It is the etiologic agent of toxoplasmosis, a disease causing substantial public health burden worldwide. Its wide range of host species and its global occurrence probably complicate the study of its evolutionary history, and conflicting scenarios have been proposed to explain its current global distribution. In this study, we analyse a global set of 156 genomes (including 105 new genomes) and we provide the first direct estimate of T. gondii mutation rate and the first estimate of its generation time. We elucidate how the evolution of T. gondii populations is intimately linked to the major events that have punctuated the recent history of cats. We show that a unique haplotype —whose length represents only 0.16% of the whole T. gondii genome— is common to all domestic T. gondii strains worldwide and has accompanied wild cats (Felis silvestris) during their emergence from the wild to domestic settlements, their dispersal in the Old World and their recent expansion to the Americas in the last six centuries. By combining environmental and functional data to selection inference tools, we show that selection of this domestic haplotype is most parsimoniously explained by its role in initiation of sexual reproduction of T. gondii in domestic cats.