Cuticular nitrogen economy during development in the cockroach Cryptocercus punctulatus and the termite Neotermes jouteli

J Insect Physiol. 2024 Dec 25:104745. doi: 10.1016/j.jinsphys.2024.104745. Online ahead of print.

Abstract

The role of nitrogen during insect development and reproduction is key in the success of a species, and is of primary importance in wood feeding taxa. Based on comparison of xylophagous, one-piece termites to the termite sister group, subsocial wood-feeding cockroaches in the genus Cryptocercus, it has been proposed that the evolution of termite eusociality involved a fundamental shift in nitrogen allocation strategies. Cryptocercus exhibits a nitrogen storage economy, with individuals gradually increasing in size and cuticular density over a years-long developmental period. Termites, however, remain in a juvenilized morphotype with minimal investment into cuticle, suggesting that nitrogen is conserved and circulated according to the needs of the colony via behaviors such as trophallaxis and cannibalism. We examined the nitrogen economy of Cryptocercus punctulatus and the dampwood termite Neotermes jouteli, focusing on cuticular nitrogen investment during development and exuvial nitrogen losses resulting from molting. Cryptocercus progressively changes from a pale, thin, soft cuticle at hatch to a dark, thick, heavily sclerotized cuticle in adults; increases in N/mg cuticle and the quantity of cuticular catecholamines are correlated with these ontogenetic color changes. There were significant differences in the nitrogen content of two successive age classes of early stage juveniles and in their discarded exuvia at molt. Soldier and alate castes of N. jouteli exhibited the highest sclerotization/melanization indices; pseudergates had levels comparable to those measured in Class I (3rd and 4th instar) juveniles of C. punctulatus. Exuvia of N. jouteli contained 0.19 μgN/mg, while exuvia of approximately two- and three-year-old C. punctulatus had 72.9 and 82.6 μgN/mg, respectively. Our data support the hypothesis that the evolution of termite eusociality from subsocial cockroach ancestors was rooted in chronic fitness limitations imposed by their low nitrogen diet.

Keywords: Altricial; Catecholamines; Cryptocercus punctulatus; Eusociality; Exuvia; Molting; Neotermes jouteli; Nitrogen.