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. This allows them to generate a steep osmotic gradient to draw water from within the rectum and return it to the body. Within the cryptonephridial tubules a seemingly novel cell type, the leptophragmata, is considered to play a key role in transporting potassium chloride to generate this osmotic gradient. Nothing was known about the developmental mechanisms or evolution of these unusual renal cells. Here we investigate the mechanisms underpinning development of the leptophragmata in the red flour beetle,Tribolium castaneum. We find that leptophragmata express and require ateashirt/tiptoptranscription factor gene, as do the secondary renal cells ofDrosophila melanogasterwhich lack a cryptonephridial arrangement. We also find an additional transcription factor, Dachshund, is required to establish leptophragmata identity and to distinguish them from the secondary cells inTribolium'snon-cryptonephridial region of renal tubule. Dachshund is also expressed in a sub-population of secondary cells inDrosophila. So leptophragmata, which are unique to the beetle lineage, appear to have originated from a specific renal cell type present ancestrally, and specified by a conserved repertoire of transcription factors.