Understanding range-wide immune gene variation in an endangered big cat (Panthera tigris)

Abstract

Assessing genetic diversity at loci putatively involved in fitness, such as immune genes, could provide important insights into the survival and vulnerability of endangered species. Research on immune genes in wild species has traditionally focussed on the Major Histocompatibility Complex (MHC) genes, which represent a small proportion of the immune gene repertoire and limits our understanding of immunity in non-model species. Here, we investigate five families of non-MHC immune genes - Tumor Necrosis Factors, interleukins, Toll-like Receptors, Leukocyte Immunoglobulin-Like Receptors, and chemokines - involved in adaptive and innate immunity in tiger Panthera tigris, an endangered carnivore known to have experienced historical bottlenecks and inbreeding. By leveraging 107 publicly available whole genomes, this study provides a comparative, multi-subspecific assessment of non-MHC immunogenetic diversity in tigers and identifies populations of conservation concern. We found higher genetic variation at immune receptor genes compared to neutral regions and immune signaling genes. Site frequency spectra suggest balancing selection on Toll-like receptor genes. Further, tiger populations with histories of bottlenecks and inbreeding, such as South China tigers and North western Indian tigers exhibit reduced genetic diversity and higher mutation load at immune genes, compared to large and connected tiger populations. Overall, we find that genetic drift is likely the predominant evolutionary force shaping genetic variation in tigers at both neutral and immune loci. However, some immune polymorphisms persist despite drift, thereby maintaining elevated variation, indicating that tigers have not been entirely stripped of their immunogenetic resilience. Such immunogenetic resilience may prove vital as spillover threats intensify. Significance statementUnderstanding immune gene diversity beyond the MHC genes is essential for accurately assessing the adaptive potential of endangered species. Here, we leverage whole-genome sequencing across multiple tiger subspecies to show that non-MHC immune receptor genes harbour greater variation than neutral loci, and that balancing selection might maintain diversity at Toll-like receptor genes. Even in bottlenecked populations, some immune polymorphisms are retained, indicating that tigers possess broader immunogenetic resilience than previously thought.