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Complete metamorphosis (Holometaboly) is a key innovation that underlies the spectacular success of holometabolous insects. Phylogenetic analyses indicate that Holometabola form a monophyletic group that evolved from ancestors exhibiting hemimetabolous development (Hemimetaboly). However, the nature of the changes underlying this crucial transition, including the occurrence of the holometabolan-specific pupal stage, is poorly understood. Using the holometabolous beetle  Tribolium castaneum  as a model insect, here we show that the transient up-regulation of the anti-metamorphic  Krüppel-homolog 1  ( TcKr-h1 ) gene at the end of the last larval instar is critical in the formation of the pupa. We find that depletion of this specific  TcKr-h1  peak leads to the precocious up-regulation of the adult-specifier factor  TcE93  and, hence, to a direct transformation of the larva into the adult form, bypassing the pupal stage. Moreover, we also find that the TcKr-h1-dependent repression of  TcE93  is critical to allow the strong up-regulation of  Broad-complex  ( TcBr-C ), a key transcription factor that regulates the correct formation of the pupa in holometabolous insects. Notably, we show that the genetic interaction between  Kr-h1  and  E93  is also present in the penultimate nymphal instar of the hemimetabolous insect  Blattella germanica , suggesting that the evolution of the pupa has been facilitated by the co-option of regulatory mechanisms present in hemimetabolan metamorphosis. Our findings, therefore, contribute to the molecular understanding of insect metamorphosis, and indicate the evolutionary conservation of the genetic circuitry that controls hemimetabolan and holometabolan metamorphosis, thereby shedding light on the evolution of complete metamorphosis.

The Occurrence of the Holometabolous Pupal Stage Requires the Interaction between E93, Krüppel-Homolog 1 and Broad-Complex