Migratory species may display striking phenotypic plasticity during individual lifetimes. This may include differential investment in body parts and functions, differential resource use and allocation, and behavioural changes between migratory and non‐migratory phases. While migration‐related phenotypic changes are well‐reported, their underlying mechanisms are usually poorly understood. Here we compare individuals from migratory (reproductive diapause) and non‐migratory (reproductive) phases of closely related aposematic butterfly species to study how sexual dimorphism and migratory behaviour underlie significant morphological tradeoffs, and propose a plausible scenario to explain the migration‐related phenotypic plasticity observed in females of migratory species. We found that female butterflies invested significantly more in their abdominal mass compared to males irrespective of their migratory phase, and underwent a clear shift in their body mass allocation after the switch from the reproductive diapause phase to the reproductive phase. In reproductive phase, females invested much more in reproductive tissue. This switch occurred as a result of increased abdominal mass (i.e. reproductive tissue mass) without significant reduction in the thoracic mass (i.e. flight muscle mass). Migratory males, however, were not significantly different from non‐migratory males in terms of relative investment in flight and reproductive tissues. These patterns were consistent between migratory and non‐migratory aposematic species within and across clades. While migratory habits may influence the physiology and behaviour of both sexes, long‐distance migration affected female morphology much more markedly compared to that of males. These results show the sex‐specific nature of adaptations to migratory behaviour, and suggest that seemingly disparate life‐history traits such as aposematism and migration may have similar influences on the lifetime energetic investments of insects.

Movement may fundamentally alter morphology and reproductive states in insects. In long-distance migrants, reproductive diapause is associated with trade-offs between diverse life-history traits such as flight morphology and lifespan. However, many non-diapausing insects engage in shorter resource-driven dispersals. How diapause and other reproductive states alter flight morphology in migrating versus dispersing insects is poorly understood. To find out, we compared flight morphology in different reproductive states of multiple butterfly species. We found that dispersers consisted of ovulating females with higher egg loads compared with non-dispersing females. This trend was in stark contrast with that of migrating female butterflies in reproductive diapause, which made substantially higher investment in flight tissue compared with reproductively active, non-migrating females. Thus, long-distance migration and shorter resource-driven dispersals had contrasting effects on flight morphology and egg loads. By contrast, male flight morphology was not affected by dispersal, migration or associated reproductive states. Thus, dispersal and migration affected resource allocation in flight and reproductive tissue in a sex-specific manner across relatively mobile versus non-dispersing individuals of different species. These findings suggest that dispersals between fragmented habitats may put extra stress on egg-carrying females by increasing their flight burdens.