Takane Ozawa, Tomoko Mizuhara, Masataka Arata, Masakazu Shimada, Teruyuki Niimi, Kensuke Okada, Yasukazu Okada, and Kunihiro Ohta

GENETICS

Significance

Nutritional conditions during early development influence the plastic expression of adult phenotypes. Because heightened nutrition sensitivity often characterizes the development of exaggerated traits, there should be molecular mechanisms underlying trait-specific variability. This study reveals the molecular mechanisms underlying the expression of nutrition-sensitive mandibles in the beetle Gnatocerus cornutus. We found that epigenetic regulators, such as histone deacetylases (HDACs) and polycomb group (PcG) proteins, contribute specifically to the plastic expression of male mandibles, with little contribution to other body modules. In addition, HDAC1 and HDAC3 perturbation resulted in opposite phenotypic effects on mandible and wing modules. Our findings provide molecular evidence of a link between distinct epigenetic modifications and module-specific phenotypic plasticity of exaggerated traits.

Abstract

Nutritional conditions during early development influence the plastic expression of adult phenotypes. Among several body modules of animals, the development of sexually selected exaggerated traits exhibits striking nutrition sensitivity, resulting in positive allometry and hypervariability distinct from other traits. Using de novo RNA sequencing and comprehensive RNA interference (RNAi) for epigenetic modifying factors, we found that histone deacetylases (HDACs) and polycomb group (PcG) proteins preferentially influence the size of mandibles (exaggerated male weapon) and demonstrate nutrition-dependent hypervariability in the broad-horned flour beetle, Gnatocerus cornutus. RNAi-mediated HDAC1 knockdown (KD) in G. cornutus larvae caused specific curtailment of mandibles in adults, whereas HDAC3 KD led to hypertrophy. Notably, these KDs conferred opposite effects on wing size, but little effect on the size of the core body and genital modules. PcG RNAi also reduced adult mandible size. These results suggest that the plastic development of exaggerated traits is controlled in a module-specific manner by HDACs.

See: http://www.pnas.org/content/113/52/15042.abstract.html?etoc

PNAS December 27 2016; vol.113; no.52: 15042–15047

Fig. 1. Trait-specific variabilities in weapon, somatic, and genital traits. (A) Male polymorphism under different nutritional conditions in the broad-horned flour beetle, G. cornutus. (B) Morphometric landmarks were used. EW, elytra width; FL, femur length; FW, femur width; GL, genitalia length; GW: gena width; MPW, maximum prothorax width; PW, prothorax width. FL and FW are landmarked for fore, middle, and hind legs as fore femur length (FFL), middle femur length (MFL), hind femur length (HFL), fore femur width (FFW), middle femur width (MFW), and hind femur width (HFW). (C) Allometric growth of each body module in G. cornutus males. Trait sizes are plotted against body size (EW) in the log–log scale. Y = a + bX, where b is a coefficient of regression. Note that the mandible exhibits hyperallometry, the genitalia show hypoallometry, and the wing and leg show isometry. The allometric relationships of other parts are indicated in SI Appendix, Table S1.