Something old, something new: the origins of an unusual renal cell underpinning a beetle water-conserving mechanism.

Abstract

Tenebrionid beetles have been highly successful in colonising environments where water is scarce, underpinned by their unique osmoregulatory adaptations. These include a cryptonephridial arrangement of their organs, in which part of their renal/Malpighian tubules are bound to the surface of the rectum. Within the cryptonephridial tubules, an unusual cell type, the leptophragmata, plays a key physiological role underpinning water conservation. Nothing was known about the developmental mechanisms or evolution of these unusual renal cells. Here, we investigate mechanisms underpinning leptophragmata development in Tribolium castaneum. We find that leptophragmata express and require the Tiptop transcription factor, similar to secondary renal cells in Drosophila melanogaster, which express Teashirt and Tiptop, despite Drosophila lacking a crypronephridial arrangement. An additional transcription factor, Dachshund, is required to establish leptophragmata identity and to distinguish them from the secondary cells in the non-cryptonephridial region of renal tubule of Tribolium. Dachshund is also expressed in a sub-population of secondary cells in Drosophila. Leptophragmata, which are unique to the beetle lineage, appear to have originated from a specific renal cell type present ancestrally and to be specified by a conserved repertoire of transcription factors.