The architecture of phenotypic flexibility within a complex trait: an empirical case study using avian thermogenic performance

Reversible modifications to trait values can allow individuals to match their phenotypes to changing environmental conditions, a phenomenon known as phenotypic flexibility. A systems capacity for flexibility may be determined by its underlying architecture, and these relationships can have important implications for both organismal adaptation and the evolvability of acclimatization responses. Theory provides two possible alternatives to explain the ways in which lower-level traits respond to environmental challenges and contribute to phenotypic flexibility in complex, whole-organism traits: symmorphosis predicts correspondence between structure and demand across all levels of a physiological system, while the alternative predicts that influence is concentrated in select elements of a physiological network. Here we provide a rich dataset -- composed of 20 sub-organismal, physiological traits paired with whole-organism metabolic rates for 106 adult Dark-eyed Juncos (Junco hyemalis) -- to explore the mechanistic basis of phenotypic flexibility in complex traits. When exposed to synthetic temperature cues, these individuals have previously been shown to increase their thermogenic capacity (Msum) and enhance their ability to maintain their body temperature in the cold. We show that the relationships among a number of the traits that contribute to Msum varied as the environmental context changed. Moreover, variation in Msum in response to temperature acclimation was correlated with only a handful of subordinate phenotypes. As a result, avian thermogenic flexibility does not appear to be a symmorphotic response. If this is generally true of complex traits, it suggests that simple and reversible modifications can significantly impact whole-organism performance, and thus that the evolution of phenotypic flexibility in a single component part could impart flexibility for the entire system.