Human impact on the diversity and virulence of the ubiquitous zoonotic parasiteToxoplasma gondii

Abstract

A majority of emerging infectious diseases in humans are zoonoses. Understanding factors that influence the emergence and transmission of zoonoses is pivotal for their prevention and control.Toxoplasma gondiiis one of the most widespread zoonotic pathogens known today. Whereas only a few genotypes ofT. gondiidominate in the Northern Hemisphere, many genotypes coexist in South America. Furthermore,T. gondiistrains from South America are more likely to be virulent than those from the Northern Hemisphere. However, it is not clear what factor(s) shaped modern-day genetic diversity and virulence ofT. gondii. Here, our analysis suggests that the rise and expansion of farming in the past 11,000 years established the domestic cat/mouse transmission cycle forT. gondii, which has undoubtedly played a significant role in the selection of certain linages ofT. gondii. Our mathematical simulations showed that within the domestic transmission cycle, intermediately mouse-virulentT. gondiigenotypes have an adaptive advantage and eventually become dominant due to a balance between lower host mortality and the ability to superinfect mice previously infected with a less virulentT. gondiistrain. Our analysis of the global type II lineage ofT. gondiisuggests its Old World origin but recent expansion in North America, which is likely the consequence of global human migration and trading. These results have significant implications concerning transmission and evolution of zoonotic pathogens in the rapidly expanding anthropized environment demanded by rapid growth of the human population and intensive international trading at present and in the future.