Evolution of heterophil/lymphocyte ratios in response to ecological and life-history traits: A comparative analysis across the avian tree of life

Lymphocytes and heterophils are the two most abundant leucocyte types, which play a major role in adaptive and innate immune defence, respectively. The ratio of heterophils to lymphocytes (H/L ratio) may reflect a readiness to cope with infection through injury (via heterophils) rather than with a communicable disease (via lymphocytes). Since elevated H/L ratio constitutes a corticosterone-mediated response to external stressors, this trait is generally acknowledged as the robust measure of physiological stress in vertebrates. Here, I hypothesized that baseline H/L ratios of birds (as measured under normal physiological function) could be an important evolutionary trait shaped by species' ecology and life history. I predicted that H/L ratios should be determined by traits related to pathogen exposure (migratoriness, sociality, breeding latitude) and trade-offs between investment in reproduction (clutch size) and self-maintenance (longevity). I compiled published data on leucocyte profiles for nearly 250 bird species representing over half of all extant avian orders and nearly 30% of all extant avian families. Phylogenetically informed comparative methods were used to assess evolutionary associations of H/L ratios with ecological and life-history traits across the avian tree of life. Relatively strong phylogenetic signal and phylogenetic autocorrelation in avian H/L ratios indicated that most diversification in this trait occurred relatively early in bird radiation. Fluctuating selection and drift were identified as the major forces responsible for the evolution of H/L ratios in birds, while low H/L ratios were identified as an ancestral state in birds. Finally, phylogenetically informed Bayesian models showed that H/L ratios correlated negatively with longevity and positively with sociality and breeding latitude. This study was the first to describe the patterns of avian H/L ratio evolution in a broad phylogenetic framework. The results indicate that H/L ratios should not be merely recognized as a proxy for the intraspecific variation in physiological stress, but also as an important evolutionary trait, which probably have adaptive significance visible in a wider phylogenetic perspective.