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.
Highlights
Maternal effects can explain a considerable proportion of observed phenotypic variation in early-life traits and have important short- and long-term consequences for offspring fitness [1]
Having found that neonatal anti-strongyle IgG antibody levels positively predicted offspring survival, we addressed whether this relationship was a direct association, or whether and how it was mediated through indirect associations with neonatal total IgG levels, offspring weight and parasite burden
Variation in maternal antibody transfer is related to maternal age and previous parasite-specific antibody levels in the mother’s plasma, suggesting that maternal antibody transfer is related to maternal condition and the mother’s ability to produce effective immune responses
Summary
Maternal effects can explain a considerable proportion of observed phenotypic variation in early-life traits and have important short- and long-term consequences for offspring fitness [1]. We measured maternally transferred antibody levels in blood samples taken from lambs within 10 days of birth ( ‘neonatal antibodies’) in a wild population of Soay sheep (Ovis aris) over a 25-year study period In this population, infection with strongyle nematodes has well-documented negative effects on health and survival, for lambs [18,19,20,21]. We aimed to determine the fitness benefits of maternal antibodies and dissect whether any effects were driven by parasite-specific antibodies (enhanced immunity to worms) or total IgG levels (enhanced maternal resource provisioning in colostrum) We achieved this by testing whether neonatal antibody levels predicted offspring body weight, parasite burden and antibody levels at weaning (four months old), as well as survival to weaning and first-winter survival. Our results demonstrate how variation among females in maternal antibody transfer can have important long-term consequences for offspring parasite resistance, growth and survival in the wild
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