Rhinoceros beetle horn development reveals deep parallels with dung beetles

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.

Development and evolution of color patterns in ladybird beetles: A case study in Harmonia axyridis

“…Dorsally restricted gene expression and morphogenetic function in the embryo are widely conserved among most insects, such as flour beetles (Nunes da Fonseca, van der Zee, & Roth, ; iB_09082, iBeetle‐Base, Dönitz et al., ), wasps (Buchta, Özüak, Stappert, Roth, & Lynch, ), honeybees (Wilson, Kenny, & Dearden, ), and grasshoppers (Dong & Friedrich, ), but not in milkweed bugs (Sachs et al., ). In addition, the expression or function of adult dorsal plate patterning in late development is also conserved in some insects, such as mosquitoes and flies (reviewed in Simpson & Marcellini, ) and rhinoceros beetles (Ohde et al., ). On the other hand, the function of patterning in the forewing blade, as in H. axyridis , has not been reported in the other insects investigated so far.…”

Integrating evolutionarily novel horns within the deeply conserved insect head

“…Indeed, when we examine those genes differentially expressed across the entire posterior of the head in both sexes ( Fig. 2e, 17 genes shared), we find genes such as hedgehog (hh), cubitus interruptus, orthodenticle (otd), odd-skipped family genes, and Wingless/Wnt signaling components-all of which have been implicated in horn formation either here (Wnt signaling-see below) or in previous studies [11,21,22]. Third, we cannot exclude the possibility that other developmental time points could possess more clearly definable horn inducing networks, a caveat which would necessitate sampling of greater diversity of developmental stages in future studies.…”

“…Lastly, all three genes are latently expressed, but non-functional, in the anterior head of O. taurus and possibly many other species, but have been recruited uniquely in O. sagittarius to facilitate the integration of the speciesspecific, novel head horns within the anterior head. Although we presently lack the phylogenetic resolution to confidently distinguish between the second and third scenarios, it is worth noting that rx is functionally required for the formation of the adult anterior head (clypeus and labrum) in Drosophila and that both rx and Sp8 function in the anterior head and head horn formation of the adult rhinoceros beetle, Trypoxylus dichotomus [21,35]. These observations are consistent with deeply ancestral developmental roles of all these genes and thus suggest a secondary loss in O. taurus.…”

Impact of trait exaggeration on sex-biased gene expression and genome architecture in a water strider

“…Among the countless examples of sexual dimorphism, some species have evolved extreme patterns whereby males, generally, develop such drastic phenotypes that they appear exaggerated compared to homologous traits in the other sex or to other body parts 7–10 . These growth-related sexual traits have received lots of attention in developmental genetics, but we still lack a general understanding of the genomic regulation underlying their development 7,11–21 .…”