Watching the days go by: Asymmetric regulation of caterpillar development by changes in photoperiod.

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 alternative pathways often differ in co-adapted life-history traits, for example, with slower development and larger size in individuals headed for diapause. The developmental timing of these differences may be of adaptive importance: If traits diverge early, the potential for phenotypic differences between the pathways is greater, whereas if traits diverge late, the risk may be lower of expressing a maladaptive phenotype if the selective environment changes during development. 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 prediapause 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. These results show how several traits may be shaped by the same environmental cue (photoperiod), but along subtly different ontogenies, into an integrated phenotype.

Diapause induction and relaxed selection on alternative developmental pathways in a butterfly.

Seasonal phenotypic plasticity entails differential trait expression depending on the time of season. The facultative induction of winter diapause in temperate insects is a developmental switch mechanism often leading to differential expression in life-history traits. However, when there is a latitudinal shift from a bivoltine to univoltine life cycle, selection for pathway-specific expression is disrupted, which may allow drift towards less optimal trait values within the non-selected pathway. We use field- and experimental data from five Swedish populations of Pararge aegeria to investigate latitudinal variation in voltinism, local adaptation in the diapause switch and footprints of selection on pathway-specific regulation of life-history traits and sexual dimorphism in larval development. Field data clearly illustrated how natural populations gradually shift from bivoltinism to univoltinism as latitude increases. This was supported experimentally as the decrease in direct development at higher latitudes was accompanied by increasing critical daylengths, suggesting local adaptation in the diapause switch. The differential expression among developmental pathways in development time and growth rate was significantly less pronounced in univoltine populations. Univoltine populations showed no significant signs of protandry during larval development, suggesting that erosion of the direct development pathway under relaxed selection has led to the loss of its sex-specific modifications.

Asymmetric life-history decision-making in butterfly larvae.

In temperate environments, insects appearing in several generations in the growth season typically have to decide during the larval period whether to develop into adulthood, or to postpone adult emergence until next season by entering a species-specific diapause stage. This decision is typically guided by environmental cues experienced during development. An early decision makes it possible to adjust growth rate, which would allow the growing larva to respond to time stress involved in direct development, whereas a last-minute decision would instead allow the larva to use up-to-date information about which developmental pathway is the most favourable under the current circumstances. We study the timing of the larval pathway decision-making between entering pupal winter diapause and direct development in three distantly related butterflies (Pieris napi, Araschnia levana and Pararge aegeria). We pinpoint the timing of the larval diapause decision by transferring larvae from first to last instars from long daylength (inducing direct development) to short daylength conditions (inducing diapause), and vice versa. Results show that the pathway decision is typically made in the late instars in all three species, and that the ability to switch developmental pathway late in juvenile life is conditional; larvae more freely switched from diapause to direct development than in the opposite direction. We contend that this asymmetry is influenced by the additional physiological preparations needed to survive the long and cold winter period, and that the reluctance to make a late decision to enter diapause has the potential to be a general trait among temperate insects.