Seasonal variation in sex-specific immunity in wild birds

José O Valdebenito,Ádám Z Lendvai,Tamás Székely,Götz Eichhorn,Jordi Figuerola,Naerhulan Halimubieke

doi:10.1038/s41598-020-80030-9

Abstract

Whilst the immune system often varies seasonally and exhibits differences between males and females, the general patterns in seasonality and sex differences across taxa have remained controversial. Birds are excellent model organisms to assess these patterns, because the immune system of many species is well characterised. We conducted a meta-analysis using 41 wild bird species from 24 avian families to investigate sex differences and seasonal (breeding/non-breeding) variations in immune status, including white blood cell counts, phytohaemagglutinin (PHA) test, bacteria-killing ability (BKA), haemolysis and haemagglutination assays. We found male-biased macrophage concentration, BKA and haemolysis titers, but only during the breeding season. Sex-specific heterophil concentrations, heterophil/lymphocyte ratios and PHA responses differed between breeding and non-breeding, suggesting larger changes in males than in females. Importantly, sex differences in immune status are stronger during the breeding period than during the non-breeding period. Taken together, our study suggests that both seasonal variation and sex differences in immune system are common in birds, although their associations are more complex than previously thought.

Highlights

Whilst the immune system often varies seasonally and exhibits differences between males and females, the general patterns in seasonality and sex differences across taxa have remained controversial
Our results show that across all immune variables, while there was no overall difference between males and females (Fig. 1A), there was an important variation in sex differences between the non-breeding and the breeding period (Fig. 1B; Table 1)
During the non-breeding period, bacteria-killing ability (BKA) tended to be higher in males (p = 0.089) while heterophil concentration tended to be higher in females (p = 0.079)

Summary

Introduction

Whilst the immune system often varies seasonally and exhibits differences between males and females, the general patterns in seasonality and sex differences across taxa have remained controversial. Et al.[9] did not find overall sexual differences in birds immunity, but they concluded that future studies of sex differences in immunity should include variables known to affect immune functioning, such as a ge[10], nutritional state11, photoperiod[12] or s easonality[13] The latter variable is especially relevant, because seasonal changes, in particular the transition between the non-breeding and the breeding period, involve major physiological and behavioural changes. We included information from nine measurements characterising immune status: the relative frequency of four types of white blood cells (heterophils, lymphocytes, macrophages, eosinophils), the ratio of heterophils/lymphocytes (H/L ratio, a glucocorticoid-mediated immune index of stress), and four widely used immune response indexes (the phytohaemagglutinin test, bacteria-killing ability assay, haemolysis assay, and the haemagglutination assay) For each of these nine immune parameters we estimated their overall meta-analytic means (i.e. estimates of sex-specific immune biases). Because breeding often incurs increased workload and higher energy demands compared to non-breeding birds in w inter[16], we expected the two periods to differ from each other, and season to significantly affect immune variables[31,32]

Methods

Results

Conclusion