Environment-dependent phenotypic expression, also known as phenotypic plasticity is exhibited to some degree by all organisms. Natural selection can act on the ability to respond to the environment allowing individuals to maintain fitness across heterogeneous environments. However, phenotypic plasticity can also potentially slow the rate of adaptive evolution within a population or result in maladaptive phenotypes. Despite the widespread occurrence and consequence for adaptive evolution, the genetic architecture and specific molecular variants that underlie phenotypic plasticity remain largely unknown. To evaluate patterns of plasticity and the genes that mediate the plastic response this work utilizes Drosophila melanogaster and its close sister specie Drosophila simulans. Individual lines collected from natural populations of D. melanogaster and D. simulans have previously been shown to exhibit phenotypic plasticity for several traits in response to changes in temperature and nutrition. However, these studies do not address patterns of plasticity across heterogeneous environments. To establish that the strength of the plastic response varies within and among natural populations isofemale lines of D. melanogaster and D. simulans were collected from three locations along the east coast and exposed to various larval rearing environment. The geographic pattern in the strength of the plastic response is only present in some traits and absent in others, which highlights the modular nature of phenotypic plasticity. To identify a gene that is able to modulate plasticity across several life history traits this work takes advantage of a candidate gene approach. A previously identified genetic polymorphism in the couch potato (cpo) gene in D. melanogaster mediates the propensity to diapause is shown in this work to affect the individual's ability to respond plastically across several life history traits. The patterns observed in the investigation of cpo parallel the patterns of plasticity observed in natural populations. Thus, polymorphism in cpo gene may play an important role in the meditation of plasticity in natural populations. These findings provide insight into plasticity within natural populations and the genes that underlie the strength of the plastic response.