Juvenile Hormone Regulates Extreme Mandible Growth in Male Stag Beetles

Abstract

The morphological diversity of insects is one of the most striking phenomena in biology. Evolutionary modifications to the relative sizes of body parts, including the evolution of traits with exaggerated proportions, are responsible for a vast range of body forms. Remarkable examples of an insect trait with exaggerated proportions are the mandibular weapons of stag beetles. Male stag beetles possess extremely enlarged mandibles which they use in combat with rival males over females. As with other sexually selected traits, stag beetle mandibles vary widely in size among males, and this variable growth results from differential larval nutrition. However, the mechanisms responsible for coupling nutrition with growth of stag beetle mandibles (or indeed any insect structure) remain largely unknown. Here, we demonstrate that during the development of male stag beetles (Cyclommatus metallifer), juvenile hormone (JH) titers are correlated with the extreme growth of an exaggerated weapon of sexual selection. We then investigate the putative role of JH in the development of the nutritionally-dependent, phenotypically plastic mandibles, by increasing hemolymph titers of JH with application of the JH analog fenoxycarb during larval and prepupal developmental periods. Increased JH signaling during the early prepupal period increased the proportional size of body parts, and this was especially pronounced in male mandibles, enhancing the exaggerated size of this trait. The direction of this response is consistent with the measured JH titers during this same period. Combined, our results support a role for JH in the nutrition-dependent regulation of extreme mandible growth in this species. In addition, they illuminate mechanisms underlying the evolution of trait proportion, the most salient feature of the evolutionary diversification of the insects.

Dopamine is a key regulator in the signalling pathway underlying predator-induced defences inDaphnia

“…These include caste determination in social insects [35], photoperiodic adaptation of reproductive modes in aphids [36], seasonal pattern formation in butterflies [37], as well as the development of colour in caterpillars [38], horns in scarab beetles [39,40] and morphological defences in Daphnia [11,16]. All of these are mediated by juvenile hormones and often dopamine-signalling pathways [41][42][43][44], as supported by the data presented here.…”

The function of appendage patterning genes in mandible development of the sexually dimorphic stag beetle

“…We previously reported that JH promotes mandible enlargement, and that larger males have higher JH titers than smaller males during the prepupal period (Gotoh et al 2011). The effects of dac knockdown on mandible size exhibited a significant interaction with body size (Fig.…”

“…Methods for rearing, breeding and inducing large and small males are described in Gotoh et al 2011 andGotoh et al 2014.…”

“…Recently, the male-specific mandible enlargement in the sexually dimorphic stag beetle Cyclommatus metallifer was found to be controlled by both nutrition-dependent juvenile hormone (JH) effects and through the sex-specific sex determination cascade (Gotoh et al 2011(Gotoh et al , 2014(Gotoh et al , 2016. Males of this species exhibit extremely enlarged mandibles and larger males have disproportionally larger mandibles than smaller males (Fig.…”

“…These size differences between males are caused by differential JH titers during the prepupa period, suggesting that it is the critical period for mandible growth, Fig. 1F (Gotoh et al 2011). Females also have mandibles but they are not modified or enlarged compared to the mandibles of other beetles (Fig.…”