Longitudinal monitoring of gut immune and inflammatory responses in a population of semi feral equids using novel, non-invasive biomarkers

Equids have co-evolved with a community of mutualistic, commensal and parasitic microbes and parasites. Gastrointestinal nematodes are ubiquitous parasites that can cause deleterious effects on host fitness at high abundance. However, nematodes can play a beneficial role in modulating host immune reactivity and depressing inflammatory pathways. Here we evaluate the relationship between seasonal nematode egg shedding in semi-feral Carneddau ponies and host gut inflammatory and <br/>immune responses. We predicted that if host immune state regulates parasite burdens, we should see immunotolerance (e.g. IL-10) highest when host condition/energy balance is poor (i.e. late winter/ early spring) and active immune responses (e.g. elevated Th2 and inflammation) when ponies have the highest energy reserves (i.e. late summer). <br/>We applied a validated toolkit of pro- and anti-inflammatory cytokine and immunoglobulin markers to a longitudinal faecal dataset with egg shedding rates. Nematode egg shedding peaked between late Summer and early Autumn and was lowest in winter. Carneddau ponies had elevated anti-inflammatory/ Treg (IL-10) throughout late winter and early spring, which coincided with a temporal increase in shedding lates. In the summer, ponies switched to a more pro-inflammatory state (higher IL-6 and <br/>TNF- α) and an increase in Th2 immunoglobulin (IgG3/5) in the late autumn, which corresponded with the peak in shedding. <br/>These results suggest that immune state appears to respond to both extrinsic (i.e. resources and thermoregulation) challenges and intrinsic (i.e. nematode fecundity and egg shedding rates). Mixed Th1/Th2 and pro-inflammatory responses peak in late summer-early autumn when both egg shedding and pony condition are highest, suggesting that ponies may permit burdens to increase until they are in an energetic state that allows them to invest in parasite clearance. Conversely, Th2/Treg responses are strongest in winter when ponies are most nutritionally stressed. <br/>This study presents the first multi-faceted characterisation of seasonal immune state changes in a semi-feral equid population. The relationship between energy stress and Treg suggests a causal link between gastrointestinal nematode burden and host immunocompetence. Parasite shedding rates have long been assumed to be parasite driven. These results suggest that host condition and immunocompetence may play a key role in nematode population dynamics.