Incomplete genetic compensation and countergradient variation of blood-oxygen transport in deer mice

Abstract

Novel environments can induce fitness-reducing responses (i.e., maladaptive plasticity) that should be eliminated by selection via genetic compensation. Across an environmental gradient, genetic compensation may result in a cryptic form of trait variation known as countergradient variation, in which genetic changes oppose environmental effects on trait expression. We combined lab and field data to quantify maladaptive hematological responses to hypoxia and cold in deer mice (Peromyscus maniculatus) across their ∼4000 m elevational range. In laboratory-raised mice native to low elevations, individuals increased their hemoglobin concentration and hematocrit in response to simulated high-elevation, a response that is maladaptive if unmitigated. In contrast, deer mice from high elevation increased hematocrit and hemoglobin to a lesser degree, consistent with genetic compensation. Unlike the predictions under complete genetic compensation, we observed a positive slope between hematological traits and elevation in the field, although this slope was lower than that observed in lowlanders in the lab. Our results suggest that deer mice have attenuated maladaptive hematological responses to high-elevation via genetic compensation that is incomplete, which has led to weak countergradient variation. We suggest this phenomenon is the result of a balance between positive selection for increased oxygen carrying capacity and antagonistic selection against elevated blood viscosity.

Keywords: Peromyscus; altitude; elevation; hematocrit; hemoglobin; maladaptive plasticity; non-adaptive plasticity; phenotypic plasticity.