Contribution to understanding the evolution of holometaboly: Transformation of internal head structures during the metamorphosis in the green lacewing Chrysopa pallens (Neuroptera: Chrysopidae)

Abstract

<jats:title>Abstract</jats:title> <jats:p><jats:bold>Background：</jats:bold>Metamorphosis remains one of the most complicated and poorly understood processes in insects. This is particularly so for the very dynamic transformations that take place within the pupal sheath of holometabolous insects. Only few studies address these transformations especially with regard to cranial structures of those holometabolous species where the larval and adult forms have a similar diet. It thus remains unclear to what extent the internal structures undergo histolysis and rebuilding. Here, the development of the brain and skeleto-muscular system of the head of <jats:italic>Chrysopa pallens</jats:italic> (Rambur, 1838) is studied. This species is a predator of aphids in the larval and adult stage.<jats:bold>Results：</jats:bold>We used micro-computed-tomography (µ-CT) to study the transformations of the larval, prepupal and pupal head within the cocoon. We first assessed the morphological differences and similarities between the stages. We then determined the point in time when the compound eyes appear and describe the re-orientation of the head capsule which transforms the prognathous larva into a hypognathous adult. The internal head muscles are distinctly more slender in larvae than adults. In addition, the adults have a significantly larger brain which is likely needed for the processing of the signals obtained by the adults’ vastly expanded sensory organs that are presumably needed for dispersal and mating. Our study shows that the histolysis and modification of the inner muscles and skeletal elements take place within the prepupa. The central nervous system persists throughout metamorphosis but its morphology changes significantly. <jats:bold>Conclusion：</jats:bold>Our study reveals that not only the inner structures, but also the outer morphology continues to change after the final larval moult. The adult cuticle and internal structures form gradually within the cocoon. The histolysis and rebuilding begins with the skeletal elements and is followed by changes in the central nervous system before it concludes with modifications of the musculature. This order of events is likely ancestral for Holometabola because it is also known from Hymenoptera, Diptera, Mecoptera, and Coleoptera.</jats:p>

Evolution of holometaboly revealed by developmental transformation of internal thoracic structures in a green lacewing Chrysopa pallens (Neuroptera: Chrysopidae)

“…Inside cocoon (figs. 2 and 3 of Zhao et al ., 2020). D 1–4: prepupae, immobile adecticous exarate type.…”

“…According to a study on the cephalic structures of C. pallens in Zhao et al . (2020), the disintegration and reconstruction processes of thoracic structures takes place almost simultaneously with those in the head. Notably, the timing of muscle bundle formation (at d 7) is consistent with that of the honey bee, in which the thoracic vertical muscle bundles are present at 150 h after sealing (Oertel, 1930).…”

“…In addition, some thoracic muscles of late pupae are also incompletely attached to the skeletons, such as muscles P6, P7, and P9. The same phenomenon occurs in Coleoptera (Ge et al ., 2015) and Neuroptera (Zhao et al ., 2020). Consequently, we suggest that muscles become well developed only after emergence.…”

“…C. pallens (Rambur, 1838), which was used in Zhao et al . (2020) as a model species, was collected in May 2017 from Langfang, Hebei, People's Republic of China, and raised in a laboratory culture that was maintained at a constant 25 ℃ and approximately 75% relative humidity under a 16 h : 8 h light/dark cycle. The larvae and adults were fed aphids.…”

“…For Neuropterida, Zhao et al . (2020) revealed the transformations of head internal structures of Chrysopa pallens .…”