Rhinoceros beetle horn development reveals deep parallels with dung beetles.

Takahiro Ohde,Shuji Shigenobu,Teruyuki Niimi,Robert A Zinna,Moe Nakata,Hiroki Gotoh,Shinichi Morita,Takeshi Mizutani,Karen Yuzaki,Yuta Ito,Kenshi Wada,Kouhei Toga,Jema Rushe,Laura Corley Lavine,Mutsuki Mase,Douglas J Emlen,Koji Kadota,Junko Morita,Y Kitano

doi:10.1371/journal.pgen.1007651

Abstract

Beetle horns are attractive models for studying the evolution of novel traits, as they display diverse shapes, sizes, and numbers among closely related species within the family Scarabaeidae. Horns radiated prolifically and independently in two distant subfamilies of scarabs, the dung beetles (Scarabaeinae), and the rhinoceros beetles (Dynastinae). However, current knowledge of the mechanisms underlying horn diversification remains limited to a single genus of dung beetles, Onthophagus. Here we unveil 11 horn formation genes in a rhinoceros beetle, Trypoxylus dichotomus. These 11 genes are mostly categorized as larval head- and appendage-patterning genes that also are involved in Onthophagus horn formation, suggesting the same suite of genes was recruited in each lineage during horn evolution. Although our RNAi analyses reveal interesting differences in the functions of a few of these genes, the overwhelming conclusion is that both head and thoracic horns develop similarly in Trypoxylus and Onthophagus, originating in the same developmental regions and deploying similar portions of appendage patterning networks during their growth. Our findings highlight deep parallels in the development of rhinoceros and dung beetle horns, suggesting either that both horn types arose in the common ancestor of all scarabs, a surprising reconstruction of horn evolution that would mean the majority of scarab species (~35,000) actively repress horn growth, or that parallel origins of these extravagant structures resulted from repeated co-option of the same underlying developmental processes.

Highlights

A variety of morphological novelties have arisen and diversified through the course of animal evolution
In T. dichotomus, sexually dimorphic horn development becomes apparent during the prepupal stage [9]
Given the important functions of transcriptional regulation in animal development, we focused on differentially expressed genes (DEGs) annotated either as transcription factors (TFs) or as signaling molecules for our RNAi screening

Summary

Introduction

A variety of morphological novelties have arisen and diversified through the course of animal evolution. Horns develop from discrete patches of epidermal tissue that detach locally from the cuticle of late-stage third-instar larvae and undergo a burst of proliferation to form a densely folded disc [2, 3]. As in the imaginal discs of Drosophila melanogaster, Manduca sexta, and other insects, the three-dimensional shape of the adult beetle horn forms first as an intricately patterned arrangement of folds in the epidermis, which unfurls as the animal molts from a larva to a pupa [4]. Studies of horn development have focused on the genes responsible for spatial patterning and cell proliferation within these growing horn primordia. Embryonic head patterning genes likely contribute to horn formation in Onthophagus horns [6]

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