Oxygen availability drives blood traits and the cell number-size tradeoff across Andean hummingbirds

Abstract

Predictable trait variation across environmental gradients suggests that adaptive evolution repeatedly finds the same solution to a challenge. Trait-environment associations can reflect long-term, genetic evolution across phylogenies, or short-term, plastic responses of individuals. When phylogenetic and population-level patterns match, it implies consistency between the long timescale of adaptation and the short timescale of acclimatization. Alternatively, genetic adaptation can find solutions that break the rules of trait-environment covariation. For example, blood-hemoglobin concentration ([Hb]) increases at high elevations in animals, but genetic adaptations in some populations have been shown to augment tissue oxygenation while curtailing hemoglobin production, altering this predictable [Hb]-elevation association. Here, we tested whether species adaptation to elevation generally alters trait-environment relationships for blood. To do this, we measured blood traits of 1,217 individuals representing 77 species of Andean hummingbirds, across a 4,600 m elevational gradient. We used hierarchical Bayesian modeling to estimate blood trait responses to elevation, environmental temperature, precipitation, individual and species characteristics, and phylogeny. Strikingly, the effects of elevation on [Hb] and hematocrit (Hct) were nearly identical for individuals and species, implying that rules of elevational blood variation are set by physics of gas exchange in the hummingbird respiratory system and are unchanged by species adaptation. However, when we looked at mechanisms of [Hb] adjustment--by changes in red blood cell size or number--we did find a signal of species adaptation: To adjust [Hb], species at low and high elevations, respectively, tended to adjust cell size, whereas species at mid-elevations tended to adjust cell number. Despite scale-independent elevational variation in [Hb] and Hct, the species-specific balance of red blood cell size versus number appears to have been affected by adaptations that distinguish hummingbird species living at moderate versus high elevations.