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.

Geographic variation in baseline innate immune function does not follow variation in aridity along a tropical environmental gradient

“…Instead they suggest flexibility within individuals to respond to local conditions. This result is consistent with findings from our earlier year-round study on Common Bulbuls in Jos where we found higher immune indices in the dry season compared to the wet season, and a further increase in some immune indices as the dry season progressed 43 . The high variability within locations (Table S1) confirms that innate immunity is highly flexible 26 .…”

“…This period coincides with the small breeding peak just before the onset of moult in the species 38 . In the same study, breeding Common Bulbuls had higher nitric oxide concentration, while moulting birds had lower concentrations, and this pattern was consistent within individuals 43 . Common Eiders Somateria mollissima also show higher nitric oxide concentration during breeding 80 .…”

“…www.nature.com/scientificreports www.nature.com/scientificreports/ We did not consider differences in immune indices between sexes because Common Bulbuls are sexually monomorphic. Moreover, in previous studies with Common Bulbuls where we determined sex molecularly, there were no sex related differences for the same immune indices 43,50 . Common Bulbuls are socially monogamous, so we expect a one-to-one sex ratio.…”

“…Studies in poultry have shown increase in nitric oxide production during coccidian infection 24,78,79 , and this is often associated with increased humidity aiding coccidian oocysts sporulation: but we did not assess infection status in this study. In a previous study with Common Bulbuls, nitric oxide concentration was highest around the interface between the wet and dry season 43 . This period coincides with the small breeding peak just before the onset of moult in the species 38 .…”

A fruit diet rather than invertebrate diet maintains a robust innate immunity in an omnivorous tropical songbird

“…Note however, that diet composition affected haemagglutination titre during the first 12 weeks of the experiment (combined with ovotransferrin as PC1), thus the absence of a treatment effect in the full range of the experiment may be associated with increased variability in immune indices (Figure S3) observed after the onset of the rains (Figure S1). In the wild, innate immune function differs between the wet and dry season in common bulbuls (Nwaogu, Cresswell, Versteegh, & Tieleman, ; Nwaogu, ). The negative correlation between haptoglobin concentration and body mass may be due to a breakdown of muscle proteins to supply amino acids for hepatic acute phase protein synthesis (Jain et al, ; Londhe & Guttridge, ).…”