Noninvasive measurement of mucosal immunity in a free‐ranging baboon population

Abstract

Ecoimmunological patterns and processes remain understudied in wild primates, in part because of the lack of noninvasive methods to measure immunity. Secretory immunoglobulin A (sIgA) is the most abundant antibody present at mammalian mucosal surfaces and provides an important first line of defense against pathogens. Recent studies show that sIgA can be measured noninvasively in feces and is a good marker of mucosal immunity. Here we validated a commercial ELISA kit to measure fecal IgA in baboons, tested the robustness of its results to variation in collection and storage conditions, and developed a cost‐effective in‐house ELISA for baboon fecal IgA. Using data from the custom ELISA, we assessed the relationship between fecal IgA concentrations and gastrointestinal parasite burden, and tested how sex, age, and reproductive effort predict fecal IgA in wild baboons. We find that IgA concentrations can be measured in baboon feces using an in‐house ELISA and are highly correlated to the values obtained with a commercial kit. Fecal IgA concentrations are stable when extracts are stored for up to 22 months at −20°C. Fecal IgA concentrations were negatively correlated with parasite egg counts (Trichuris trichiura), but not parasite richness. Fecal IgA did not vary between the sexes, but for males, concentrations were higher in adults versus adolescents. Lactating females had significantly lower fecal IgA than pregnant females, but neither pregnant nor lactating female concentrations differed significantly from cycling females. Males who engaged in more mate‐guarding exhibited similar IgA concentrations to those who engaged in little mate‐guarding. These patterns may reflect the low energetic costs of mucosal immunity, or the complex dependence of IgA excretion on individual condition. Adding a noninvasive measure of mucosal immunity will promote a better understanding of how ecology modulates possible tradeoffs between the immune system and other energetically costly processes in the wild.

Responsiveness of fecal immunoglobulin A to HPA‐axis activation limits its use for mucosal immunity assessment

“…The combined extract was finally centrifuged for 5 min at 2000 g , the supernatant was transferred into a polypropylene tube, and samples were stored at −20°C until IgA analysis. Different from Gesquiere et al (2020), we added a second extraction step after we found in an initial experiment on a subset of 18 samples that re‐extraction increased IgA concentrations on average by 42% (range 32%–54%). In addition to improving overall extraction efficiency (c.f.…”

“…In 340 fecal extracts, IgA was measured using the commercial monkey IgA ELISA kit (Life Diagnostics, Inc., Cat# IGA‐3) previously used for IgA assessment in fecal samples of baboons (Gesquiere et al, 2020). For measurement, all extracts were diluted 1:20 with assay diluent provided by the kit, and samples were measured in duplicate according to the manufacturer's instructions.…”

“…IgA levels can be measured in minimally or noninvasively collected samples, including saliva, urine, and feces of many species, such as rodents (Bundgaard et al, 2012; Eriksson et al, 2004; Pihl & Hau, 2003; Taira et al, 2015), domestic animals (Carlsson et al, 2007; Heinrichs et al, 2013; Tress et al, 2006), equids (Krueger et al, 2019; Tombak et al, 2020), Asian elephants ( Elephas maximus : Edwards et al, 2019; Kosaruk et al, 2020), roe deer ( Capreolus capreolus : Escribano‐Avila et al, 2013), Nonhuman primates ( Papio spp . : Gesquiere et al, 2020; P. troglodytes : Lantz et al, 2018; M. fascicularis : Paramastri et al, 2007) and humans (Kang et al, 2018; Scholtens et al, 2008). However, previous studies using fIgA measurements as a measure of parasitic infections produced inconsistent results.…”

“…In sheep, increased IgA levels were related to resistance to gastrointestinal nematode infection (Pernthaner et al, 2006). In baboons, fIgA concentrations were negatively correlated with egg counts of Trichuris trichiura , but not with parasite richness (Gesquiere et al, 2020). The inconsistencies in the reported association patterns of parasite infection and IgA level changes are likely related to species specificities, but may also be caused by differences in encountered stressors including food scarcity which differs between provisioned and wild populations.…”

Immunity to Soil-Transmitted Helminths: Evidence From the Field and Laboratory Models

“…However, epidemiological evaluation of STH burden in human populations shows that in endemic areas, infected individuals suffer chronic parasitism throughout their lives (79)(80)(81)(82). This holds true for non-human primates (83)(84)(85), livestock (86,87), and wild rodent populations (88,89). In humans, infection burden correlates strongly with age following one of two patterns: (i) parasite burden builds rapidly during early childhood but peaks shortly before adolescence, burden then declines and plateaus at a low level throughout adulthood e.g., Trichuris trichiura, and Ascaris lumbricoides (79,90,91); or (ii) STH burden builds consistently throughout childhood and early adolescence but plateaus at a moderate level prior to adulthood e.g., Necator americanus and Ancylostoma duodenale (82).…”