Transcriptomic analysis elucidates evolution of the major histocompatibility complex class I in neotropical bats

Abstract

Abstract The Order Chiroptera comprises more than 1,400 species, each with its evolutionary history and under unique selective pressures, among which are the host–pathogen interactions. Bats have coped with complex interactions with a broad spectrum of microbes throughout their evolutionary history, prompting the development of unique adaptations that allow them to co-exist with microbes with pathogenic potential more efficiently than other nonadapted species. In this sense, an extraordinary immune system with unique adaptations has been hypothesized in bats. To explore this, we focused on the major histocompatibility complex (MHC), which plays a crucial role in pathogen recognition and presentation to T cells to trigger the adaptive immune response. We analyzed MHC class I transcripts in five species, each from different families of New World bats. From RNA-seq data, we assembled a partial region of the MHC-I comprising the α1 and α2 domains, which are responsible for peptide binding and recognition. We described five putative functional variants, two of which have two independent insertions at the α2 domain. Our results suggest that this insertion appeared after the divergence of the order Chiroptera and may have an adaptive function in the defense against intracellular pathogens, providing evidence of positive selection and trans-specific polymorphism on the peptide-binding sites.