Evolutionary history, longevity and terrestriality predict Toxoplasma gondii seroprevalence in free-ranging non-human primates

Evidence from captive populations indicates that lemurs are particularly vulnerable to toxoplasmosis, a parasitic disease caused by Toxoplasma gondii. In wild populations, however, seroprevalence in lemurs remains low. This may be partly due to their predominantly arboreal behavior, which limits exposure to environmentally transmitted oocysts. Alternatively, or additionally, low seroprevalence could reflect high mortality following infection due to limited evolutionary exposure to the parasite and, consequently, a lack of evolved resistance. In this study, we assess whether the evolutionary history of primates with felids influences susceptibility to T. gondii infection, independent of ecological exposure. Specifically, we predicted that (1) species with greater terrestriality would exhibit higher exposure risk, (2) species longevity would be positively associated with their seroprevalence to T. gondii and (3) primate superfamilies with longer histories of co-occurrence with felids would show higher seroprevalence than Lemuroidea at similar levels of terrestriality and longevity. Serum samples from 435 free-ranging lemurs were tested for T. gondii antibodies and a literature review of T. gondii seroprevalence in free-ranging primates was conducted. The overall seroprevalence in Lemuroidea was 5.4 %, significantly lower than that observed in Ceboidea (11.8 %) and Cercopithecoidea (27.6 %). Notably, seroprevalence in lemurs was lower than expected based on their terrestriality, suggesting that evolutionary isolation from felids may underlie heightened vulnerability. Longevity modifies the risk profile in a lineage-specific way where seroprevalence increases with lifespan in Cercopithecoidea but not for lemurs. Collectively, our findings support the hypothesis that lemurs are immunologically naïve to T. gondii, and in the face of expanding domestic cat populations and increasing habitat fragmentation, the parasite may pose an underrecognized conservation threat.