Juvenile hormone mediates developmental integration between exaggerated traits and supportive traits in the horned flour beetleGnatocerus cornutus

Abstract

SUMMARY Sexually selected exaggerated traits are often coupled with modifications in other nontarget traits. In insects with weapons, enlargements of nontarget characters that functionally support the weapon often occur (i.e. supportive traits). The support of sexual traits requires developmental coordination among functionally related multiple traits—an explicit example of morphological integration. The genetic theory predicts that developmental integration among different body modules, for which development is regulated via different sets of genes, is likely to be coordinated by pleiotropic factors. However, the developmental backgrounds of morphological integrations are largely unknown. We tested the hypothesis that the juvenile hormone (JH), as a pleiotropic factor, mediates the integration between exaggerated and supportive traits in an armed beetle Gnatocerus cornutus. During combat, males of this beetle use exaggerated mandibles to lift up their opponents with the supportive traits, that is, the head and prothoracic body parts. Application of methoprene, a JH analog (JHA), during the larval to prepupal period, induced the formation of large mandibles relative to the body sizes in males. Morphometric examination of nontarget traits elucidated an increase in the relative sizes of supportive traits, including the head and prothoracic body parts. In addition, reductions in the hind wing area and elytra length, which correspond to flight and reproductive abilities, were detected. Our findings are consistent with the genetic theory and support the idea that JH is a key pleiotropic factor that coordinates the developmental integration of exaggerated traits and supportive characters, as well as resource allocation trade‐offs.

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

“…Conversely, at the onset of metamorphosis, application of JH induces horn development in small males (Emlen and Nijhout, 1999). The exaggerated mandibles of male stag beetles, Cyclommatus metallifer , and horned flour beetles, Gnatocerus cornutus , are likewise sensitive to JH (Gotoh et al, 2011; Okada et al, 2012). Application of JH mimics induces large mandibles relative to body size for both species (Gotoh et al, 2011; Okada et al, 2012).…”

“…The exaggerated mandibles of male stag beetles, Cyclommatus metallifer , and horned flour beetles, Gnatocerus cornutus , are likewise sensitive to JH (Gotoh et al, 2011; Okada et al, 2012). Application of JH mimics induces large mandibles relative to body size for both species (Gotoh et al, 2011; Okada et al, 2012). Furthermore, in the horned flour beetle, while JH increases relative mandible size, it decreases the relative size of other structures such as the elytra and hind wings (Okada et al, 2012).…”

“…Application of JH mimics induces large mandibles relative to body size for both species (Gotoh et al, 2011; Okada et al, 2012). Furthermore, in the horned flour beetle, while JH increases relative mandible size, it decreases the relative size of other structures such as the elytra and hind wings (Okada et al, 2012). This suggests that IIS/TOR signaling modifies JH and ecdysone concentrations in response to nutrition (Figure 5).…”

Histone deacetylases control module-specific phenotypic plasticity in beetle weapons

“…Hypervariability of exaggerated traits is widely found in animal taxa, and it is thought to be the result of heightened nutrition sensitivity (13,14,35,36). Module-specific response to insulin signaling is a plausible mechanism that regulates trait variability (13,15), but the mechanism underlying module specificity needs to be elucidated (15).…”

“…Dosage was optimized to produce maximal nonlethal effects by the stated criteria (TSA: 46 ng per larva, 5AzaC: 3.48 μg per larva), and drugs were injected into the larvae by using Nanoject II (Drummond Scientific) under CO 2 anesthesia. The injected larvae were individually isolated in 24-well culture plates (Thermo Scientific), so that they could develop into prepupae (the adult morphogenetic stage) within 3-4 d (36,54). No food was provided after the treatment.…”