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1. Genome evolution and divergence in cis-regulatory architecture is associated with condition-responsive development in horned dung beetles

   https://doi.org/10.1371/journal.pgen.1011165  

   Davidson, Phillip L; Moczek, Armin P (March 2024, PLOS Genetics)

   Duncan, Elizabeth J (Ed.)

   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. 

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2. The draft genome sequence of the Japanese rhinoceros beetle Trypoxylus dichotomus septentrionalis towards an understanding of horn formation

   https://doi.org/10.1038/s41598-023-35246-w  

   Morita, Shinichi; Shibata, Tomoko F; Nishiyama, Tomoaki; Kobayashi, Yuuki; Yamaguchi, Katsushi; Toga, Kouhei; Ohde, Takahiro; Gotoh, Hiroki; Kojima, Takaaki; Weber, Jesse N; et al (December 2023, Scientific Reports)

   Abstract The Japanese rhinoceros beetleTrypoxylus dichotomusis a giant beetle with distinctive exaggerated horns present on the head and prothoracic regions of the male.T. dichotomushas been used as a research model in various fields such as evolutionary developmental biology, ecology, ethology, biomimetics, and drug discovery. In this study, de novo assembly of 615 Mb, representing 80% of the genome estimated by flow cytometry, was obtained using the 10 × Chromium platform. The scaffold N50 length of the genome assembly was 8.02 Mb, with repetitive elements predicted to comprise 49.5% of the assembly. In total, 23,987 protein-coding genes were predicted in the genome. In addition, de novo assembly of the mitochondrial genome yielded a contig of 20,217 bp. We also analyzed the transcriptome by generating 16 RNA-seq libraries from a variety of tissues of both sexes and developmental stages, which allowed us to identify 13 co-expressed gene modules. We focused on the genes related to horn formation and obtained new insights into the evolution of the gene repertoire and sexual dimorphism as exemplified by the sex-specific splicing pattern of thedoublesexgene. This genomic information will be an excellent resource for further functional and evolutionary analyses, including the evolutionary origin and genetic regulation of beetle horns and the molecular mechanisms underlying sexual dimorphism. 

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3. Beetle horns evolved from wing serial homologs

   https://doi.org/10.1126/science.aaw2980  

   Hu, Yonggang; Linz, David M.; Moczek, Armin P. (November 2019, Science)

   Understanding how novel complex traits originate is a foundational challenge in evolutionary biology. We investigated the origin of prothoracic horns in scarabaeine beetles, one of the most pronounced examples of secondary sexual traits in the animal kingdom. We show that prothoracic horns derive from bilateral source tissues; that diverse wing genes are functionally required for instructing this process; and that, in the absence of Hox input, prothoracic horn primordia transform to contribute to ectopic wings. Once induced, however, the transcriptional profile of prothoracic horns diverges markedly from that of wings and other wing serial homologs. Our results substantiate the serial homology between prothoracic horns and insects wings and suggest that other insect innovations may derive similarly from wing serial homologs and the concomitant establishment of structure-specific transcriptional landscapes. 

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4. Utilizing geometric morphometrics to investigate gene function during organ growth: Insights through the study of beetle horn shape allometry

   https://doi.org/10.1111/ede.12464  

   Rohner, Patrick T.; Hu, Yonggang; Moczek, Armin P. (December 2023, Evolution & Development)

   Abstract Static allometry is a major component of morphological variation. Much of the literature on the development of allometry investigates how functional perturbations of diverse pathways affect the relationship between trait size and body size. Often, this is done with the explicit objective to identify developmental mechanisms that enable the sensing of organ size and the regulation of relative growth. However, changes in relative trait size can also be brought about by a range of other distinctly different developmental processes, such as changes in patterning or tissue folding, yet standard univariate biometric approaches are usually unable to distinguish among alternative explanations. Here, we utilize geometric morphometrics to investigate the degree to which functional genetic manipulations known to affect thesizeof dung beetle horns also recapitulate the effect of hornshapeallometry. We reasoned that the knockdown phenotypes of pathways governing relative growth should closely resemble shape variation induced by natural allometric variation. In contrast, we predicted that if genes primarily affect alternative developmental processes, knockdown effects should align poorly with shape allometry. We find that the knockdown effects of several genes (e.g.,doublesex, Foxo) indeed closely aligned with shape allometry, indicating that their corresponding pathways may indeed function primarily in the regulation of relative trait growth. In contrast, other knockdown effects (e.g.,Distal‐less,dachs) failed to align with allometry, implicating these pathways in potentially scaling‐independent processes. Our findings moderate the interpretation of studies focusing on trait length and highlight the usefulness of multivariate approaches to study allometry and phenotypic plasticity. 

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5. Wing serial homologues and the diversification of insect outgrowths: insights from the pupae of scarab beetles

   https://doi.org/10.1098/rspb.2020.2828  

   Hu, Yonggang; Moczek, Armin P. (January 2021, Proceedings of the Royal Society B: Biological Sciences)

   null (Ed.)

   Modification of serially homologous structures is a common avenue towards functional innovation in developmental evolution, yet ancestral affinities among serial homologues may be obscured as structure-specific modifications accumulate over time. We sought to assess the degree of homology to wings of three types of body wall projections commonly observed in scarab beetles: (i) the dorsomedial support structures found on the second and third thoracic segments of pupae, (ii) the abdominal support structures found bilaterally in most abdominal segments of pupae, and (iii) the prothoracic horns which depending on species and sex may be restricted to pupae or also found in adults. We functionally investigated 14 genes within, as well as two genes outside, the canonical wing gene regulatory network to compare and contrast their role in the formation of each of the three presumed wing serial homologues. We found 11 of 14 wing genes to be functionally required for the proper formation of lateral and dorsal support structures, respectively, and nine for the formation of prothoracic horns. At the same time, we document multiple instances of divergence in gene function across our focal structures. Collectively, our results support the hypothesis that dorsal and lateral support structures as well as prothoracic horns share a developmental origin with insect wings. Our findings suggest that the morphological and underlying gene regulatory diversification of wing serial homologues across species, life stages and segments has contributed significantly to the extraordinary diversity of arthropod appendages and outgrowths. 

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