Pathogen-mediated selection favours the maintenance of innate immunity gene polymorphism in a widespread wild ungulate

Toll-like Receptors (TLR) play a central role in recognition and host
frontline defence against a wide range of pathogens. A number of recent
studies have shown that TLR genes (Tlrs) often exhibit large polymorphism
in natural populations. Yet, there is little knowledge on how this
polymorphism is maintained and how it influences disease susceptibility in
the wild. In previous work, we showed that some Tlrs exhibit similarly
high levels of genetic diversity as genes of the Major Histocompatibility
Complex (MHC), and signatures of contemporary balancing selection in roe
deer (Capreolus capreolus), the most abundant cervid species in Europe.
Here, we investigated the evolutionary mechanisms by which
pathogen-mediated selection could shape this innate immunity genetic
diversity by examining the relationships between Tlr (Tlr2, Tlr4 and Tlr5)
genotypes (heterozygosity status and presence of specific alleles) and
infections with Toxoplasma and Chlamydia, two widespread intracellular
pathogens known to cause reproductive failure in ungulates. We showed that
Toxoplasma and Chlamydia exposures vary significantly across year and
landscape structure with few co-infection events detected, and that the
two pathogens exert antagonistic selection on Tlr2 polymorphism. By
contrast, we found limited support for Tlr heterozygote advantage. Our
study confirmed the importance of looking beyond Mhc genes in wildlife
immunogenetic studies. It also emphasized the necessity to consider
multiple pathogen challenges and their spatiotemporal variation to improve
our understanding of vertebrate defence evolution against pathogens.