Abstract
While it is now broadly accepted that inter-individual variation in the outcomes of host–pathogen interactions is at least partially genetically controlled, host immunogenetic characteristics are rarely investigated in wildlife epidemiological studies. Furthermore, most immunogenetic studies in the wild focused solely on the major histocompatibility complex (MHC) diversity despite it accounts for only a fraction of the genetic variation in pathogen resistance. Here, we investigated immunogenetic diversity of the Alpine ibex (Capra ibex) population of the Bargy massif, reservoir of a virulent outbreak of brucellosis. We analysed the polymorphism and associations with disease resistance of the MHC Class II Drb gene and several non-MHC genes (Toll-like receptor genes, Slc11A1) involved in the innate immune response to Brucella in domestic ungulates. We found a very low neutral genetic diversity and a unique MHC Drb haplotype in this population founded few decades ago from a small number of individuals. By contrast, other immunity-related genes have maintained polymorphism and some showed significant associations with the brucellosis infection status hence suggesting a predominant role of pathogen-mediated selection in their recent evolutionary trajectory. Our results highlight the need to monitor immunogenetic variation in wildlife epidemiological studies and to look beyond the MHC.
Highlights
While it is broadly accepted that inter-individual variation in the outcomes of host–pathogen interactions is at least partially genetically controlled, host immunogenetic characteristics are rarely investigated in wildlife epidemiological studies
Genetic factors of susceptibility to brucellosis in Alpine ibex have never been investigated while several associations with innate gene polymorphism have been discovered in domestic ungulates[31,32]
We revealed a significant association with toll-like receptors (Tlrs)[1] genotype (Fig. 2, Table S5): homozygous individuals carrying two copies of the frequent haplotype (Tlr1a) had a lower probability to be seropositive than heterozygous individuals (AES = −1.90 [−3.52, −0.29])
Summary
While it is broadly accepted that inter-individual variation in the outcomes of host–pathogen interactions is at least partially genetically controlled, host immunogenetic characteristics are rarely investigated in wildlife epidemiological studies. Host genetic and immunogenetic characteristics are rarely investigated in wildlife epidemiological studies despite evidence that inter-individual variation in the outcomes of host–pathogen interactions is at least partially genetically controlled[4]. Pathogen-mediated selective pressures shape the genetic components of host immunity and give rise to inter-individual variation in resistance to infectious diseases[5]. This immunogenetic variation is well documented in humans and domestic animals but much less in wild animals. Beyond the conservation and ethical issues, this outbreak has raised public health and economic concerns since, for the first time, cattle and humans were infected by the wildlife reservoir[30] In this context, it was critical to identify the drivers of pathogen persistence in this population and individual characteristics favoring its spread. Genetic factors of susceptibility to brucellosis in Alpine ibex have never been investigated while several associations with innate gene polymorphism have been discovered in domestic ungulates[31,32]
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