No Compensatory Relationship between the Innate and Adaptive Immune System in Wild-Living European Badgers.

Yung Wa Sin,Maria-Elena Mannarelli,Christina Buesching,Hannah L. Dugdale,Chris Newman,Geetha Annavi,Terry Burke,David W. Macdonald

doi:10.1371/journal.pone.0163773

Abstract

The innate immune system provides the primary vertebrate defence system against pathogen invasion, but it is energetically costly and can have immune pathological effects. A previous study in sticklebacks found that intermediate major histocompatibility complex (MHC) diversity correlated with a lower leukocyte coping capacity (LCC), compared to individuals with fewer, or many, MHC alleles. The organization of the MHC genes in mammals, however, differs to the highly duplicated MHC genes in sticklebacks by having far fewer loci. Using European badgers (Meles meles), we therefore investigated whether innate immune activity, estimated functionally as the ability of an individual’s leukocytes to produce a respiratory burst, was influenced by MHC diversity. We also investigated whether LCC was influenced by factors such as age-class, sex, body condition, season, year, neutrophil and lymphocyte counts, and intensity of infection with five different pathogens. We found that LCC was not associated with specific MHC haplotypes, MHC alleles, or MHC diversity, indicating that the innate immune system did not compensate for the adaptive immune system even when there were susceptible MHC alleles/haplotypes, or when the MHC diversity was low. We also identified a seasonal and annual variation of LCC. This temporal variation of innate immunity was potentially due to physiological trade-offs or temporal variation in pathogen infections. The innate immunity, estimated as LCC, does not compensate for MHC diversity suggests that the immune system may function differently between vertebrates with different MHC organizations, with implications for the evolution of immune systems in different taxa.

Highlights

The innate and adaptive immune systems provide two lines of defence against pathogen invasion in vertebrates [1]
There was no significant association between leukocyte coping capacity (LCC) and the presence of specific major histocompatibility complex (MHC) alleles and haplotypes (Fig 1; Tables B and C in S1 Supplementary)
In contrast to the complementary way that the innate and adaptive immune systems interact in the stickleback, where the lowest respiratory bursts were produced by individuals with optimal intermediate allelic diversity [24], we found no association between LCC and MHC heterozygosity in these European badgers

Summary

Introduction

The innate and adaptive immune systems provide two lines of defence against pathogen invasion in vertebrates [1]. Phagocytic neutrophils, are recruited immediately by chemical signals, such as chemokines, to the vicinity of infection These leukocytes kill pathogens via oxidative mechanisms, termed the respiratory burst; a process in which neutrophils release reactive oxygen species (ROS), such as superoxides and hydrogen peroxides, to destroy invasive pathogens such as bacteria [2]. The adaptive immune system involves different leukocytes, known as lymphocytes, with antigen-specific functions and antigen-presenting cells, providing a highly specific immunological memory for pathogens, retained throughout the lifetime of an individual These antigen-presenting cells, such as macrophages, B-cells and dendritic cells, express major histocompatibility complex (MHC) class II molecules on their surfaces, which bind and present pathogenic antigens to Tcells [8], in turn activating antibody production and other immune cascades. All nucleated somatic cells express MHC class I molecules that present antigens to cytotoxic Tcells [9]

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Results

Conclusion