Microbiota drives local MHC class II adaptation in a wild aquatic bird species

Claudio Verdugo, Pedro Rodrigues, Luis Castañeda

Genes of the Major Histocompatibility Complex (MHC) represent one of the most polymorphic genes in the vertebrate genome and are a critical component of the adaptive immune response. Synanthropic and cosmopolitan birds are exposed to local array of pathogens that may lead to specific immune adaptations. In order to analyze population-specific patterns of association of genetic variability and pathogen community, 105 Neotropic cormorants (Phalacrocorax brasilianus) from two populations were sampled. We compared MHC variation, at both class I (against intracellular parasites) and II (against extracellular parasites) by amplicon NGS sequencing, and levels of pathogen (i.e. RNA/DNA viruses, gut microbiota by 16S metabarcoding, and hemosporidian) between birds from a synanthropic and human subsidized population and a non-subsidized population in Southern Chile. Variation at four selectively neutral markers (i.e. two mitochondrial and two nuclear genes) were also sequenced. We detected a high diversity of gamma-coronaviruses infecting birds from the subsidized site (20.2%), but also adenovirus (8.7%) and herpesvirus (3.8%). Hemoparasites were found at a very low rate in both sites (3.3%-Plasmodium sp., 1.6%- Leucocytozoon). The community structure of the gut microbiota show very low intra-population variability but highly structured among sites. The birds from the subsidized sites have a less diverse microbiota mostly dominated gen. Campylobacter from the Proteobacteria. Accordingly, we found that birds from subsidized sites had lower MHC class II diversity than non-subsidized sites. These patterns were not likely to be caused by differences in population demography as neutral markers were very low, contrary to our expectations, and showed no evidence of population structure among sites. Our results emphasizes that human-altered habitats may have unpredictable effects not only on the agents that may infect wildlife but also may affect the genetic variability at critical immune genes.

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