Double trouble: trypanosomatids with two hosts have lower infection prevalence than single host trypanosomatids

Trypanosomatids are a diverse family of protozoan parasites, some of which cause devastating human and livestock diseases. There are two distinct infection life cycles in trypanosomatids; some species complete their entire life cycle in a single host (monoxenous) while others infect two hosts (dixenous). Dixenous trypanosomatids are mostly vectored by insects, and the human trypanosomatid diseases are caused mainly by vectored parasites. While infection prevalence has been described for subsets of hosts and trypanosomatids, little is known about whether monoxenous and dixenous trypanosomatids differ in infection prevalence. Here, we use meta-analyses to synthesise all published evidence of trypanosomatid infection prevalence for the last two decades, encompassing 931 unique host-trypansomatid systems. In examining 584 studies that describe infection prevalence, we find, strikingly, that monoxenous species are two-fold more prevalent than dixenous species across all hosts. We also find that dixenous trypanosomatids have significantly lower infection prevalence in insects than their non-insect hosts. To our knowledge, these results reveal for the first time, a fundamental difference in infection prevalence according to host specificity where vectored species might have lower infection prevalence as a result of a potential 'jack of all trades, master of none' style trade-off between the vector and subsequent hosts. Lay Summary Trypanosomatids are a group of parasitic protists that infect a wide range of hosts, from plants to people. These parasites are transmitted in two distinct ways, either directly from one host to another within the same species, or are vectored through the bite of an infected insect. These different lifestyles must have dramatic effects on parasite traits, but these traits have never been systematically compared. Here, for the first time, we ask whether the complex life-cycle of vectored trypanosomatids alter infection prevalence? To examine this, we used natural language processing and machine learning to process and interrogate all published infection prevalence data from the last 20 years in both vectored (multiple hosts) and non-vectored (single host) trypanosomatid parasites. We found that trypanosomatids with only one host infect a much higher proportion of hosts than the vectored parasites. Our work is the first to identify a fundamental difference in the biology of vectored vs non-vectored parasites, but also creates a key insight: the extant burden of trypanosomatid diseases might be maintained by a remarkably small proportion of infected vectors; thus, small reductions in the proportion of infectious vectors could have oversized effects on vertebrate infection.

Automated summary

In this study, all published data on trypanosomatid infection prevalence from the last 20 years were synthesized and analyzed. The results showed that monoxenous trypanosomatids have a two-fold higher infection prevalence compared to dixenous trypanosomatids across all hosts. It was also found that dixenous trypanosomatids have a significantly lower infection prevalence in insects than in non-insect hosts. These findings reveal a fundamental difference in infection prevalence according to host specificity and provide insights into the trade-off between the vector and subsequent hosts.