Eat to reproduce: a key role for the insulin signaling pathway in adult insects

Abstract

Insects, like all heterotrophic organisms, acquire from their food the nutrients that are essential for anabolic processes that lead to growth (larval stages) or reproduction (adult stage). In adult females, this nutritional input is processed and results in a very specific output, i.e., the production of fully developed eggs ready for fertilization and deposition. An important role in this input-output transition is attributed to the insulin signaling pathway (ISP). The ISP is considered to act as a sensor of the organism's nutritional status and to stimulate the progression of anabolic events when the status is positive. In several insect species belonging to different orders, the ISP has been demonstrated to positively control vitellogenesis and oocyte growth. Whether or not ISP acts herein via a mediator action of lipophilic insect hormones (ecdysteroids and juvenile hormone) remains debatable and might be differently controlled in different insect orders. Most likely, insulin-related peptides, ecdysteroids and juvenile hormone are involved in a complex regulatory network, in which they mutually influence each other and in which the insect's nutritional status is a crucial determinant of the network's output. The current review will present an overview of the regulatory role of the ISP in female insect reproduction and its interaction with other pathways involving nutrients, lipophilic hormones and neuropeptides.

Gene Expression Dynamics in Major Endocrine Regulatory Pathways along the Transition from Solitary to Social Life in a Bumblebee, Bombus terrestris

“…Since transcripts of both B. terrestris insulin-related peptides are the most abundant in reproducing queens, the IIS in bumblebees is apparently correlated with upregulated JH signaling and high nutritional and reproductive status, as is also reported for solitary insects (Badisco et al, 2013). This is supported by increased IGF-1 expression in reproducing queens, which correlates with the pattern of Vg in the same tissues, especially in brain and hypopharyngeal glands, flight muscles and fat body (compare Figures 3A–C, 4A–C).…”

“…The highest expression occurred in the ovaries of all females. The high expression levels in the gonads might point at a role in reproduction, because IIS controls synthesis of JHs and ecdysteroids, i.e., the main regulators of insect reproductive physiology (reviewed in Antonova et al, 2012; Badisco et al, 2013). Yet, it is clear that InR-2 plays not a single role, given the widespread expression across almost all tissues.…”

“…It is tempting to propose that the extremely high expression of InR-1 in all tissues of virgins and diapausing queens compared to all other samples is related to their high food (energy) intake prior to diapause by virgins and its consequent preservation by diapausing queens (Badisco et al, 2013). By contrast, reproducing queens have relatively low level of InR-1 transcripts, indicating that they are not storing nutrients but rather spending them.…”

“…The first group belongs to the functional homologs of the vertebrate insulin. Insulin-like peptides and insulin/insulin-like growth factors (ILPs/IGFs) make up together a complex signaling network (IIS), which is tightly interconnected with JH signaling (reviewed in e.g., Antonova et al, 2012; Badisco et al, 2013). The second group comprises functionally well described energy mobilizing factors of the adipokinetic hormone family (AKHs), functionally equivalent to the mammalian glucagon (Kim and Rulifson, 2004).…”

Transcriptome profiling in the damselfly Ischnura elegans identifies genes with sex-biased expression

“…Insect hormones have long been studied due to their importance in physiology, development and behaviour [55, 56]. Several studies on insect hormones have pinpointed their role in (i) the regulation of muscle activity such as in myotropic peptides, (ii) the regulation of reproduction, growth, and development, (iii) the pheromone biosynthesis (iv), diapause hormones, and (v) the stimulation or inhibition of tanning and of colour change (reviewed in [57]).…”