Insect Tc-six4 marks a unit with similarity to vertebrate placodes

Cranial placodes are specialized ectodermal regions in the developing vertebrate head that give rise to both neural and non-neural cell types of the neuroendocrine system and the sense organs of the visual, olfactory and acoustic systems. The cranial placodes develop from a panplacodal region which is specifically marked by genes of the eyes absent/eya and two “six homeobox” family members (sine oculis/six1 and six4). It had been believed that cranial placodes are evolutionary novelties of vertebrates. However, data from non-vertebrate chordates suggest that placode-like structures evolved in the chordate ancestor already. Here, we identify a morphological structure in the embryonic head of the beetle Tribolium castaneum with placode-like features. It is marked by the orthologs of the panplacodal markers Tc-six4, Tc-eya and Tc-sine oculis/six1 (Tc-six1) and expresses several genes known to be involved in adenohypophyseal placode development in vertebrates. Moreover, it contributes to both epidermal and neural tissues. We identify Tc-six4 as a specific marker for this structure that we term the insect head placode. Finally, we reveal the regulatory gene network of the panplacodal genes Tc-six4, Tc-eya and Tc-six1 and identify them as head epidermis patterning genes. Our finding of a placode-like structure in an insect suggests that a placode precursor was already present in the last common ancestor of bilaterian animals.

Research Highlights
► Tc-six4 marks a tissue with similarity to vertebrate cranial placodes in insects.
► An Urbilaterian rather than a chordate origin of cranial placodes is suggested.
► Tc-eya activates Tc-six1. Tc-eya+Tc-six1 activate Tc-six4. Tc-six4 represses Tc-six1.
► Tc-eya, Tc-six4 and Tc-six1 (sine oculis) are required for head epidermis pattering.