Maternally derived anti-helminth antibodies predict offspring survival in a wild mammal

Abstract

The transfer of antibodies from mother to offspring provides crucial protection against infection to offspring during early life in humans and domestic and laboratory animals. However, few studies have tested the consequences of variation in maternal antibody transfer for offspring fitness in the wild. Further, separating the immunoprotective effects of antibodies from their association with nutritional resources provided by mothers is difficult. Here, we measured plasma levels of total and parasite-specific antibodies in neonatal (less than 10 days old) wild Soay sheep over 25 years to quantify variation in maternal antibody transfer and test its association with offspring survival. Maternal antibody transfer was predicted by maternal age and previous antibody responses, and was consistent within mothers across years. Neonatal total IgG antibody levels were positively related to early growth, suggesting they reflected nutritional transfer. Neonatal parasite-specific IgG levels positively predicted first-year survival, independent of lamb weight, total IgG levels and subsequent lamb parasite-specific antibody levels. This relationship was partly mediated via an indirect negative association with parasite burden. We show that among-female variation in maternal antibody transfer can have long-term effects on offspring growth, parasite burden and fitness in the wild, and is likely to impact naturally occurring host-parasite dynamics.

Keywords: IgG; Soay sheep; Teladorsagia circumcincta; immunoglobulin; maternal antibodies; maternal effects.

Figure 1.

(a) A priori SEM linking neonatal anti-T. circumcincta and total IgG antibodies to first-winter survival based on associations in this study and from previous work on this system (see electronic supplementary material, table S2 for details). (b) Final SEM with values on arrows indicating standardized path coefficients with standard errors in brackets, except for the bidirectional links between neonatal measures which show correlation coefficients. Missing paths in the a priori model were added where indicated using Shipley's test of d-separation and unsupported paths were removed based on p-values ≥0.05. Effects are separated into positive (grey full lines) and negative (black dashed lines) effects with p-values indicated by asterisks (***p < 0.001, **p < 0.01 and *p < 0.05).

Figure 2.

Associations between neonatal anti-T. circumcincta IgG levels (corrected for capture age and standardized, see Methods for full details) and neonatal survival (a) and neonatal anti-T. circumcincta IgG levels and first-winter survival (b) in Soay sheep. Plots show raw data with GLMM predictions and standard errors estimated for singleton female lambs with average values for all continuous fixed effects in the model specified in electronic supplementary material, table S7 with just neonatal anti-T. circumcincta IgG levels included.