Using the evolution of the stickleback family of subarctic fish as a touchstone, we explore the effect of new discoveries about regulatory genetics, developmental plasticity, and epigenetic inheritance on the conceptual foundations of the Modern Evolutionary Synthesis. Identifying the creativity of natural selection as the hallmark of the Modern Synthesis, we show that since its inception its adherents have pursued a variety of research projects that at first seemed to conflict with its principles, but were accommodated. We situate challenges coming from developmental biology in a dialectic between innovation and tradition, suggesting on the basis of past episodes that even if developmental plasticity and epigenetic inheritance are aligned with its principles the Modern Synthesis (and its image in the public reception of evolution) will be significantly affected.