Seasonal differences in baseline innate immune function are better explained by environment than annual cycle stage in a year-round breeding tropical songbird.

Abstract

Seasonal variation in innate immunity is often attributed to either temporal environmental variation or to life‐history trade‐offs that arise from specific annual cycle stages but decoupling them is difficult in natural populations.Here, we effectively decouple seasonal environmental variation from annual cycle stage effects by exploiting cross‐seasonal breeding and moult in the tropical Common Bulbul Pycnonotus barbatus. We test how annual cycle stage interacts with a key seasonal environmental variable, rainfall, to determine immunity at population and individual level. If immune challenge varies with precipitation, we might expect immune function to be higher in the wet season due to increased environmental productivity. If breeding or moult imposes resource constraints on birds, depending on or independent of precipitation, we might expect lower immune indices during breeding or moult.We sampled blood from 818 birds in four annual cycle stage categories: breeding, moult, simultaneous breeding and moulting, or neither. We quantified indices of innate immunity (haptoglobin, nitric oxide (NO x) and ovotransferrin concentrations, and haemagglutination and haemolysis titres) over two annual cycles of wet and dry seasons.Environment (but not annual cycle stage or interactions between both) explained variation in all immune indices, except NO x. NO x concentration differed between annual cycle stages but not between seasons. However, within the wet season, haptoglobin, NO x, ovotransferrin and haemolysis differed significantly between breeding and non‐breeding females. Aside from some recorded inconsistencies, population level results were largely similar to results within individuals that were measured repeatedly. Unexpectedly, most immune indices were higher in the dry season and during breeding.Higher immune indices may be explained if fewer or poorer quality resources force birds to increase social contact, thereby exposing individuals to novel antigens and increased infection risk, independently of environmental productivity. Breeding birds may also show higher immunity if less immune‐competent and/or infected females omit breeding. We conclude that seasonal environmental variation impacts immunity more directly in natural animal populations than via resource trade‐offs. In addition, immune indices were more often variable within than among individuals, but some indices are characteristic of individuals, and so may offer selective advantages if heritable.