1. An understudied aspect of vertebrate ecoimmunology has been the relative contributions of environmental factors (E), genetic background (G), and their interaction (G × E) in shaping immune development and function. Environmental temperature is known to affect many aspects of immune function and alterations in temperature regimes have been implicated in emergent disease outbreaks, making it a critical environmental factor to study in the context of immune phenotype determinants of wild animals.

2. We assessed the relative influences of environmental temperature, genetic background, and their interaction on first-year development of innate and adaptive immune defenses of captive-born garter snakes (Thamnophis elegans) using a reciprocal-transplant laboratory experiment. We used a full-factorial design with snakes from two divergent life-history ecotypes, which are known to differ in immune function in their native habitats, raised under conditions mimicking the natural thermal regime —i.e., warmer and cooler— of each habitat.

3. Genetic background (ecotype) and thermal regime influenced innate and adaptive immune parameters of snakes, but in an immune-component specific manner. We found some evidence of G × E interactions but no indication of adaptive plasticity with respect to thermal environment. At the individual level, the effects of thermal environment on resource allocation decisions varied between the fast- and the slow-paced life-history ecotypes. Under warmer conditions, which increased food consumption of individuals in both ecotypes, the former invested mostly in growth, whereas the latter invested more evenly between growth and immune development.

4. Overall, immune parameters were highly flexible, but results suggest that other environmental factors are likely more important than temperature per se in driving the ecotype differences in immunity previously documented in the snakes under field conditions. Our results also add to the understanding of investment in immune development and growth during early postnatal life under different thermal environments. Our finding of immune-component specific patterns strongly cautions against oversimplification of the highly complex immune system in ecoimmunological studies. In conjunction, these results deepen our understanding of the degree of immunological flexibility wild animals present, information that is ever more vital in the context of rapid global environmental change.