Correlated evolution of oxidative physiology and MHC-based immunosurveillance in birds

Maintenance and activation of the immune system incurs costs, not only in
terms of substrates and energy, but also via collateral oxidative damage
to host cells or tissues during immune response. So far, associations
between immune function and oxidative damage have been primarily
investigated at intra-specific scales. Here, we hypothesized that
pathogen-driven selection should favour evolution of effective
immunosurveillance mechanisms (e.g. Major Histocompatibility Complex, MHC)
and antioxidant defences to mitigate oxidative damage resulting from
immune function. Using phylogenetically-informed comparative approaches,
we provided evidence for correlated evolution of host oxidative physiology
and MHC-based immunosurveillance in birds. Species selected for more
robust MHC-based immunosurveillance (higher gene copy numbers and allele
diversity) showed stronger antioxidant defences, although selection for
MHC diversity still showed a positive evolutionary association with
oxidative damage to lipids. Our results indicate that historical
pathogen-driven selection for highly duplicated and diverse MHC could have
promoted the evolution of efficient antioxidant mechanisms, but these
evolutionary solutions may be insufficient to keep oxidative stress at
bounds. Although the precise nature of mechanistic links between the MHC
and oxidative stress remains unclear, our study suggests that a general
evolutionary investment in immune function may require co-adaptations at
the level of host oxidative metabolism.