Comparative morphology of the distal segments of Malpighian tubules in cicadas and spittlebugs, with reference to their functions and evolutionary indications to Cicadomorpha (Hemiptera: Auchenorrhyncha)

Abstract

Morphology of Malpighian tubules from fourteen representatives in Cicadoidea and Cercopoidea are investigated. Among which the distal segments that perform a modified glandular function during nymphal stages are investigated in particular using both scanning and transmission electron microscopies. The examined species show regional differentiation along the Malpighian tubules. The terminal parts end as separate rods in Cercopoidea, whereas they are united in pairs and enveloped by a peritoneal sheath shortly before reaching the rectum in Cicadoidea. Ultra-morphologically, the distal segments in Cercopoidea consist of numerous large protuberances containing a few small nodules, and the distal segments in Cicadinae of Cicadoidea comprise numerous large protuberances containing several small nodules. Species of subfamilies Cicadettinae (except Karenia caelatata) and Tettigadinae have undulated distal segments devoid of any protuberances and nodules. The Malpighian tubules of the Karenia cicadas, remarkably without timbals and with questionable systematic placement, morphologically resemble the Cicadinae more than the Cicadettinae (=Tibicininae auct.), indicating it is more reasonable to place this genus into Cicadinae instead of Cicadettinae. Ultrastructurally, numerous secretory granules, secretory vacuoles and rough endoplasmic reticula exist in the distal segments of nymphal spittlebugs, and abundant secretory vacuoles exist in the same region of nymphal cicadas. The secretory structures can secrete productions which may help to create favorable watery conditions for nymphal spittlebugs and cicadas (e.g., inhibiting the growth of certain soil fungi, buffering the pH conditions, and neutralizing the toxic ammonia). In contrast, the distal segments of adult spittlebugs and cicadas are devoid of secretory granules and secretory vacuoles. This suggests that nymphal Malpighian tubules in both cicadas and spittlebugs function to secondary secretion, and become mere excretive organs in adult stage. Analysis of the morphology, layout, and ultrastructure of the Malpighian tubules in Cicadomorpha support the major relationships within this infraorder as “Membracoidea+(Cicadoidea+Cercopoidea)”.