Pathogen-mediated selection and phylogeny shape MHC architecture in 33 bat genomes

Adaptive immunity is an ancestral hallmark of jawed vertebrates, yet its genomic organisation is far from static-continually reconfigured through extensive gene family duplication and evolutionary turnover. The major histocompatibility complex (MHC) plays a central role in presenting antigens derived from intra- and extracellular pathogens, eliciting pathogen-specific immune responses. Its polymorphic nature makes the MHC particularly difficult to study with genomic architecture deciphered only in a handful of species.

We manually annotated 2,095 MHC-I, -II and flanking genes across 33 high quality bat genomes, covering all 21 Chiropteran families, mapping the pan-bat genomic organisation of the MHC for the first time.

Selection and phylogenetic conservatism drive the organization of class I and II loci, while copy number variation appears largely independent of host, ecological, or environmental factors. However, we observe suggestive trends indicating that roosting behaviour, body size, and geographic distribution may predict copy number variation at certain loci. Moreover, core gut bacterial similarity increased with structural similarity in class II loci, suggesting that bacterial communities may exert selective pressures that shapes the class II repertoires. In contrast, neither viral diversity nor similarity - estimated from a public virus database - appeared to influence class I organisation. Ancestral reconstructions indicate that similarities were present in the ancestor of both Yinpterochiroptera and Yangochiroptera species, and family-level differences emerged later, particularly in speciose families such as Rhinolophidae, Hipposideridae and Vespertilionidae.

Overall, the genomic organization of the complete MHC region provides insight into how bat ecology may have shaped its evolution.