Multivariate immune defences and fitness in the wild: complex but ecologically important associations among plasma antibodies, health and survival.
Despite our rapidly advancing mechanistic understanding of vertebrate immunity under controlled laboratory conditions, the links between immunity, infection and fitness under natural conditions remain poorly understood. Antibodies are central to acquired immune responses, and antibody levels circulating in vivo reflect a composite of constitutive and induced functional variants of diverse specificities (e.g. binding antigens from prevalent parasites, self tissues or novel non-self sources). Here, we measured plasma concentrations of 11 different antibody types in adult females from an unmanaged population of Soay sheep on St Kilda. Correlations among antibody measures were generally positive but weak, and eight of the measures independently predicted body mass, strongyle parasite egg count or survival over the subsequent winter. These independent and, in some cases, antagonistic relationships point to important multivariate immunological heterogeneities affecting organismal health and fitness in natural systems. Notably, we identified a strong positive association between anti-nematode immunoglobulin (Ig) G antibodies in summer and subsequent over-winter survival, providing rare evidence for a fitness benefit of helminth-specific immunity under natural conditions. Our results highlight both the evolutionary and ecological importance and the complex nature of the immune phenotype in the wild.
Institute of Evolutionary Biology, University of Edinburgh, , Edinburgh, UK, Institute of Infection and Immunity Research, University of Edinburgh, , Edinburgh, UK, Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh, , Edinburgh, UK, Department of Ecology and Evolutionary Biology, Princeton University, , Princeton, NJ, USA, Moredun Research Institute, Pentlands Science Park, Bush Loan, Midlothian, UK.
Daniel H
DH
Nussey
Kathryn A
KA
Watt
Abigail
A
Clark
Jill G
JG
Pilkington
Josephine M
JM
Pemberton
Andrea L
AL
Graham
Tom N
TN
McNeilly
D056704:Adaptive Immunity / Q000502:physiology*; D000818:Animals; D000974:Antibodies, Antinuclear / Q000097:blood*; D000953:Antigens, Protozoan / Q000097:blood*; D005260:Female; D010270:Parasite Egg Count; D025341:Principal Component Analysis; D017168:Rhabditida / Q000276:immunology*; D017196:Rhabditida Infections / Q000276:immunology / Q000401:mortality / Q000662:veterinary*; D012621:Seasons; D012756:Sheep / Q000276:immunology*; D012757:Sheep Diseases / Q000276:immunology* / Q000401:mortality / Q000469:parasitology
D000974:Antibodies, Antinuclear; D000953:Antigens, Protozoan
Soay sheep; anti-nuclear antibodies; fitness; immunity; natural selection; strongyle nematodes