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ABSTRACT Sex‐specific trait expression represents a striking dimension of morphological variation within and across species. The mechanisms instructing sex‐specific organ development have been well studied in a small number of insect model systems, suggesting striking conservation in some parts of the somatic sex determination pathway while hinting at possible evolutionary lability in others. However, further resolution of this phenomenon necessitates additional taxon sampling, particularly in groups in which sexual dimorphisms have undergone significant elaboration and diversification. Here, we functionally investigate the somatic sex determination pathway in the gazelle dung beetleDigitonthophagus gazella, an emerging model system in the study of the development and evolution of sexual dimorphisms. We find that RNA interference (RNAi) targetingtransformer (tra)caused chromosomal females to develop morphological traits largely indistinguishable from those normally only observed in males, and thattra^RNAiis sufficient to induce splicing of the normally male‐specific isoform ofdoublesexin chromosomal females, while leaving males unaffected. Further,intersex^RNAiwas found to phenocopy previously described RNAi phenotypes ofdoublesexin female but not male beetles. These findings match predictions derived from models of the sex determination cascade as developed largely through studies inDrosophila melanogaster. In contrast, efforts to targettransformer2via RNAi resulted in high juvenile mortality but did not appear to affectdoublesexsplicing, whereas RNAi targetingSex‐lethaland two putative orthologs ofhermaphroditeyielded no obvious phenotypic modifications in either males or females, raising the possibility that the function of a subset of sex determination genes may be derived in select Diptera and thus nonrepresentative of their roles in other holometabolous orders. Our results help illuminate how the differential evolutionary lability of the somatic sex determination pathway has contributed to the extraordinary morphological diversification of sex‐specific trait expression found in nature. 

Phenotypic plasticity is thought to be an important driver of diversification and adaptation to environmental variation, yet the genomic mechanisms mediating plastic trait development and evolution remain poorly understood. The Scarabaeinae, or true dung beetles, are a species-rich clade of insects recognized for their highly diversified nutrition-responsive development including that of cephalic horns—evolutionarily novel, secondary sexual weapons that exhibit remarkable intra- and interspecific variation. Here, we investigate the evolutionary basis for horns as well as other key dung beetle traits via comparative genomic and developmental assays. We begin by presenting chromosome-level genome assemblies of three dung beetle species in the tribe Onthophagini (> 2500 extant species) includingOnthophagus taurus,O.sagittarius, andDigitonthophagus gazella. Comparing these assemblies to those of seven other species across the order Coleoptera identifies evolutionary changes in coding sequence associated with metabolic regulation of plasticity and metamorphosis. We then contrast chromatin accessibility in developing head horn tissues of high- and low-nutritionO.taurusmales and females and identify distinctcis-regulatory architectures underlying nutrition- compared to sex-responsive development, including a large proportion of recently evolved regulatory elements sensitive to horn morph determination. Binding motifs of known and new candidate transcription factors are enriched in these nutrition-responsive open chromatin regions. Our work highlights the importance of chromatin state regulation in mediating the development and evolution of plastic traits, demonstrates gene networks are highly evolvable transducers of environmental and genetic signals, and provides new reference-quality genomes for three species that will bolster future developmental, ecological, and evolutionary studies of this insect group.