Metamorphosis of a clock: Remodeling of the circadian timing system in the brain of Rhodnius prolixus (Hemiptera) during larval‐adult development

Abstract

The rhythmic phenomena expressed by organisms change over their lifetimes, but little is known of accompanying reorganization of the central circadian timing system in the brain. Especially dramatic changes in overt rhythms and morphology occur during transformation of larval insects into the adult form (metamorphosis). In Rhodnius prolixus, both the physiology of metamorphosis and its hormonal control are known in detail. Here we report changes in the brain timing system as revealed by pigment dispersing factor immunohistochemistry and confocal microscopy. Most of the features of the larval system are retained, but new clock cells differentiate and the arborizations of their axons increase in complexity, as do pathways connecting the lateral (LNs) and dorsal (DNs) groups of clock neurons. Early in metamorphosis, the LNs increase from 8 to 11 in number, becoming five small and six large LNs. Two large LNs then migrate to new positions in the protocerebrum. Another clock cell differentiates in the posterior protocerebrum. Each change occurs at a characteristic concentration of the ecdysteroid molting hormones that regulate metamorphosis. Clock cell axons invade the mushroom body and corpus allatum and travel down the ventral nerve cord. New overt rhythms develop during metamorphosis, in which these structures participate. The neuroendocrine cells of the brain receive more extensive branches of clock cell axons than in larvae. These increases in size and complexity of the circadian system during metamorphosis imply a greater complexity and diversity of outputs from it to both behavioral and hormonal rhythms in the adult.

The involvement of the brain region containing pigment-dispersing factor-immunoreactive neurons in the photoperiodic response of the bean bugRiptortus pedestris

“…These neurons correspond to PDFMe neurons (also called LNs) in other insects (Homberg et al, 1991;Nässel et al, 1991;Sato et al, 2002;Sehadová et al, 2003;Abdelsalam et al, 2008;Vafopoulou et al, 2010). In the cluster, different-sized cells were observed, as reported in other insects (Abdelsalam et al, 2008;Weiss et al, 2009;Sumiyoshi et al, 2011;Vafopoulou and Steel, 2012). The diameter of the largest cell body in the cluster was 14.8±0.65 μm (mean ± s.e.m., N=13), whereas that of the smallest one was 7.7±0.41 μm (N=10), and they were significantly different (Mann-Whitney test, P<0.01).…”

“…In addition, some branches from the bundle ran into the medulla. These patterns were not observed even in R. prolixus, which belongs to the same suborder as R. pedestris (Vafopoulou et al, 2010;Vafopoulou and Steel, 2012); therefore, they might be unique to R. pedestris.…”

“…The neuroarchitecture of PDF-ir neurons has been described for the brains of various insect species (Homberg et al, 1991;Nässel et al, 1993;Závodská et al, 2003;Abdelsalam et al, 2008;Sumiyoshi et al, 2011;Vafopoulou et al, 2010;Vafopoulou and Steel, 2012). Three major clusters have been identified in the optic lobe: a cluster located at the anterior edge of the medulla (PDFMe), a cluster at the…”

“…La, lamina; Me, medulla. Vafopoulou et al, 2010;Vafopoulou and Steel, 2012). In R. pedestris, however, the axons ran on the surface of the medulla by forming a thick bundle and fanned out at the lamina.…”

“…Other than PDF-ir cell clusters in the optic lobe, several PDF-ir (or PDH-ir) neurons in the protocerebrum have been identified in some insects, and their species-specific functions have been discussed (Homberg et al, 1991;Nässel et al, 1993;Závodská et al, 2003;Vafopoulou and Steel, 2012). In R. pedestris, several PDFir cells in the protocerebrum were also detected.…”