Many insects possess the plastic ability to either develop directly to adulthood, or enter diapause and postpone reproduction until the next year, depending on environmental cues (primarily photoperiod) that signal the amount of time remaining until the end of the growth season. These two developmental pathways often differ in co-adapted life history traits, e.g. with slower development and larger size in individuals headed for diapause. The developmental timing of these differences may be of adaptive importance: if pathways diverge late, the scope for phenotypic differences is smaller, whereas if pathways diverge early, the risk is higher of expressing a maladaptive phenotype if the selective environment changes. Here we explore the effects of changes in photoperiodic information during life on pupal diapause and associated life history traits in the butterfly Pararge aegeria. We find that both pupal diapause and larval development rate are asymmetrically regulated: while exposure to long days late in life (regardless of earlier experiences) was sufficient to produce nondiapause development and accelerate larval development accordingly, more prolonged exposure to short days was required to induce diapause and slow down pre-diapause larval development. While the two developmental pathways diverged early in development, development rates could be partially reversed by altered environmental cues. Meanwhile, pathway differences in body size were more inflexible, despite emerging late in development. Hence, in P. aegeria several traits are regulated by photoperiod, along subtly different ontogenies, into an integrated phenotype that strikes a balance between flexibility and phenotype-environment matching.