Mechanisms regulating nutrition-dependent developmental plasticity through organ-specific effects in insects

Abstract

Nutrition, via the insulin/insulin-like growth factor (IIS)/Target of Rapamycin (TOR) signaling pathway, can provide a strong molding force for determining animal size and shape. For instance, nutrition induces a disproportionate increase in the size of male horns in dung and rhinoceros beetles, or mandibles in staghorn or horned flour beetles, relative to body size. In these species, well-fed male larvae produce adults with greatly enlarged horns or mandibles, whereas males that are starved or poorly fed as larvae bear much more modest appendages. Changes in IIS/TOR signaling plays a key role in appendage development by regulating growth in the horn and mandible primordia. In contrast, changes in the IIS/TOR pathway produce minimal effects on the size of other adult structures, such as the male genitalia in fruit flies and dung beetles. The horn, mandible and genitalia illustrate that although all tissues are exposed to the same hormonal environment within the larval body, the extent to which insulin can induce growth is organ specific. In addition, the IIS/TOR pathway affects body size and shape by controlling production of metamorphic hormones important for regulating developmental timing, like the steroid molting hormone ecdysone and sesquiterpenoid hormone juvenile hormone. In this review, we discuss recent results from Drosophila and other insects that highlight mechanisms allowing tissues to differ in their sensitivity to IIS/TOR and the potential consequences of these differences on body size and shape.

Drosophila melanogaster larvae make nutritional choices that minimize developmental time

“…Nutrition affects reproductive performance differently in males and females in cockroaches, Nauphoeta cinerea, field crickets, Teleogryllus commodus, and fruit flies, D. melanogaster, and this is accompanied by a sex-specific shift in foraging choice (Maklakov et al, 2009(Maklakov et al, , 2008Reddiex et al, 2013;South et al, 2011). Furthermore, many life history characters, like body and organ size, result from the larval nutritional environment (Koyama et al, 2013;Mirth and Riddiford, 2007;Mirth and Shingleton, 2012;Nijhout, 2003a,b;Nijhout et al, 2013;Shingleton et al, 2007;Stern and Emlen, 1999). Finally, imbalanced larval nutrition affects dietary choices in later larval and adult stages in butterflies (Lee et al, 2012;Mevi-Schütz and Erhardt, 2003).…”

“…These larvae live and feed on rotting fruit, obtaining much of their protein and lipid from the yeast communities that aid decomposition (Begon, 1982). The nutrition derived from their food regulates their growth (Bakker, 1959;Tu and Tatar, 2003), their development time (Bakker, 1959;Beadle et al, 1938;Koyama et al, 2013;Mirth et al, 2009;Shingleton et al, 2005Shingleton et al, , 2009Stieper et al, 2008), and the development of their reproductive organs (David, 1970;Tu and Tatar, 2003). Protein consumption, not carbohydrate consumption, regulates body and tissue growth in larvae (Britton and Edgar, 1998;Colombani et al, 2003), whereas both protein and carbohydrates contribute to variation in developmental timing (Schwarz et al, 2013).…”

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

“…Hence, IIS interacts with other principal signaling pathways, i.e., (1) Target of Rapamycin (TOR), a nutrient sensing responder, (2) JH, the main regulator of development and reproduction, and (3) Forkhead box protein O (FOXO), a transcription factor involved in stress tolerance, diapause, longevity and growth (Vafopoulou, 2014). In consequence, IIS participates in the regulation of insect polyphenism and caste differentiation of eusocial species (e.g., Koyama et al, 2013; Xu et al, 2015). For instance, nutrient sensing triggers IIS activation which induces elevation of JH titers necessary for queen development in honeybee larvae (Mutti et al, 2011).…”

Nutritional control of insect reproduction

“…The role of insulin and TOR in nutritional regulation of insect growth and development, particularly that of Drosophila melanogaster , has been studied in great detail [1, 2, 3]. These studies have laid a foundation for our understanding of the mechanisms underlying the nutritional control.…”