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Abstract: The Scarabaeinae, or true dung beetles, are a hyper-diverse clade of insects of ecological, evolutionary, and agricultural significance and have long served as informative models of evolutionary ecology and development. Perhaps the most conspicuous of their unique traits are head horns, novel structures that serve as secondary sexual weapons, exhibit extraordinary developmental plasticity, and have fueled one of the most dramatic morphological radiations in the animal kingdom. In this study, we investigate the evolutionary basis for dung beetle traits - including horns - via comparative genomic and developmental assays. We present chromosome-level genome assemblies of three dung beetle species in the species-rich Onthophagini tribe (> 2500 extant species) including Onthophagus taurus, Onthophagus sagittarius, and Digitonthophagus gazella. Contrasting these assemblies with seven other species across the order Coleoptera identifies rapidly evolving gene families associated with metabolic regulation of developmental plasticity and metamorphosis. Intraspecific comparisons of chromatin accessibility in developing head horns of O. taurus identify distinct cis-regulatory architectures underlying sex- and nutrition-responsive development of this novel trait, including a large proportion of recently evolved regulatory elements sensitive to horn morph determination. Binding motifs of diverse developmental transcription factors are enriched in these nutrition-responsive open chromatin regions, including the early embryonic patterning gene twist. Using RNA interference (RNAi), we show twist has been co-opted into the beetle horn regulatory network to mediate differential horn morphogenesis in alternate male morphs via its interactions with nutrition-sensitive DNA-binding sites, highlighting the utility of this approach in identifying new developmental regulators of morphological evolution. These results demonstrate gene networks are highly evolvable transducers of environmental and genetic signals critical for the formation and diversification of developmental traits, established in part by condition-responsive chromatin accessibility. Further, this work provides new reference-quality genome assemblies of three dung beetles that will bolster future developmental, ecological, and evolutionary studies of this insect group. TechnicalInfo: # Genome evolution is associated with nutrition-responsive regulatory development in horned dung beetles This dataset includes genome annotation files generated for a de-novo genome assembly project of dung beetle genomes. This project includes de-novo genome assemblies for *Onthophagus taurus* (Otau), *Onthophagus sagittarius* (Osag), and *Digitonthophagus gazella* (Dgaz). ### FILE TYPES For each of the three dung beetle species (listed above), the following file eight types are available: 1. *.fasta.gz: (compressed) genome fasta file 2. *_masked.fasta.gz: (compressed) genome fasta file in which repetitive elements are soft-masked (lower-case) 3. *.gtf: GTF file describing the genomic locations of gene features identified within the assembly 4. *_repeats.fa: library of repetitive elements identified in each species' genome 5. *_repeats.gff.gz: (compressed) GFF file describing the genomic location of repetitive elements within the genome 6. *_nucleotides.fasta: fasta file of gene model sequences identified within each species' genome 7. *_proteins.fasta: fasta file of protein model sequences identified within each species' genome (translated version of file #6) 8. *_best_hits.txt: annotations of gene models including the best hit of each model to the RefSeq non-redundant Ecdysozoan protein database and NCBI gene models of the O. taurus v.2 protein models ### OTHER FILES bioinformatic_commands.txt: text file describing the primary steps for bioinformatic analyses carried out in this work. Corresponds to SupplmentaryText1 is the published manuscript.
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Doublesex mediates species-, sex-, environment- and trait-specific exaggeration of size and shape
Context-dependent trait exaggeration is a major contributor to phenotypic diversity. However, the genetic modifiers instructing development across multiple contexts remain largely unknown. We use the arthropod tibia, a hotspot for segmental differentiation, as a paradigm to assess the developmental mechanisms underlying the context-dependent structural exaggeration of size and shape through nutritional plasticity, sexual dimorphism and segmental differentiation. Using an RNAseq approach in the sexually dimorphic and male-polyphenic dung beetle Digitonthophagus gazella , we find that only a small portion (3.7%) of all transcripts covary positively in expression level with trait size across contexts. However, RNAi-mediated knockdown of the conserved sex-determination gene doublesex suggests that it functions as a context-dependent master mediator of trait exaggeration in D. gazella as well as the closely related dung beetle Onthophagus taurus . Taken together, our findings suggest (i) that the gene networks associated with trait exaggeration are highly dependent on the precise developmental context, (ii) that doublesex differentially shapes morphological exaggeration depending on developmental contexts and (iii) that this context-specificity of dsx -mediated trait exaggeration may diversify rapidly. This mechanism may contribute to the resolution of conflict arising from environment-dependent antagonistic selection among sexes and divergent developmental contexts in a wide range of animals.
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- Award ID(s):
- 1901680
- PAR ID:
- 10320559
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 288
- Issue:
- 1953
- ISSN:
- 0962-8452
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1098/rspb.2021.0241
