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Nadolski, E. M.

Publications and source records attributed to Nadolski, E. M..

3 recordsLinked to original sources

Trait-specific chromatin architectures channel pleiotropic genes toward sexually dimorphic development in horned beetles

Sex-responsive trait development generates much of the phenotypic variation found in natural populations and diversifies rapidly among closely-related taxa. Furthermore, rather than exhibiting equal sexual dimorphism across all traits, organisms are mosaics of tissues that vary in their degree of dimorphism. Yet, how these mosaic patterns are generated remains largely an open question, as sexually dimorphic traits have typically been studied individually in select model systems. In this study, we compare gene regulatory landscapes across five traits that differ in the degree of morphological sexual dimorphism in the bull-headed dung beetle Onthophagus taurus by assaying tissue-specific gene expression and chromatin accessibility at the onset of pupal development when future adult form is specified. We identify a modest number of pleiotropic regulators associated with sex differences across traits, yet uncover a high degree of sex- and trait-specificity in chromatin architecture within developing tissues. We then confirm the role of the sex determination factor doublesex in the regulation of sex differences through expression of sex-specific isoforms, and uncover trait- and sex-specific sets of Doublesex binding sites likely underpinning context specific sexual dimorphisms. Further, we identify and functionally validate the transcription factor ventral veinless as a regulator of sexually dimorphic development. Our findings suggest that in contrast to doublesex, ventral veinless does not exhibit sex-biased expression, yet exerts its sex-specific regulation via sets of differentially accessible binding sites. This work furthers our understanding of the molecular mechanisms instructing the development of sex differences and provides novel insights illustrating how transcriptional activity and chromatin remodeling interact to generate sexual dimorphism in a trait-specific manner. More generally, our work contributes to a growing body of knowledge on how development integrates cues such as sex determination to enable highly similar genomes to yield diverse phenotypic outcomes.

developmental biology↗

Divergent Hox cluster collinearity in horned beetles reveals adult head patterning function of labial

Hox genes play critical roles in specifying the regionalization of the body axis across metazoa, with the exception of the anterior dorsal head of bilaterian animals, which instead is instructed by a deeply conserved set of non-Hox regulators. The anterior dorsal head is also a hot spot of evolutionary diversification, raising the question as to the developmental-genetic underpinnings of such innovation. Onthophagine dung beetles develop evolutionarily novel and highly diversified horns on the dorsal head used as weapons during intrasexual conflicts. Preliminary RNAseq data unexpectedly documented Hox gene expression in the dorsal head of premetamorphic onthophagine larvae. Motivated by this observation, we aimed to (i) investigate the genomic content and arrangement of the Hox cluster across three onthophagine species, and (ii) assess expression patterns and (iii) potential functions of the anterior Hox genes labial, proboscipedia, and Deformed in patterning the adult beetle head and cephalic horns. We document an unexpected, derived Hox cluster configuration in the Onthophagus sagittarius genome, a species with apomorphic cephalic horn morphology. Yet despite this genomic rearrangement, embryonic expression patterns of labial and proboscipedia as well as the adult segment patterning functions of proboscipedia and Deformed were found to be conserved. In contrast, labial RNAi revealed an adult head patterning function outside horn-forming regions previously undescribed for any insect. Lastly, we show that electrosurgical ablation of the presumptive larval labial-expressing head region phenocopies this conspicuous adult labial RNAi defect. We discuss the implications of these data for current models of insect head development and diversification.

developmental biology↗

Male is the default sex: functional significance of the sex determination cascade in horned dung beetles

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 beetle Digitonthophagus gazella, an emerging model system in the study of the development and evolution of sexual dimorphisms. We find that RNA interference (RNAi) targeting transformer (tra) caused chromosomal females to develop morphological traits largely indistinguishable from those normally only observed in males, and that traRNAi is sufficient to induce splicing of the normally male-specific isoform of doublesex in chromosomal females, while leaving males unaffected. Further, intersexRNAi was found to phenocopy previously described RNAi phenotypes of doublesex in female but not male beetles. These findings match predictions derived from models of the sex determination cascade as developed largely through studies in Drosophila melanogaster. In contrast, transformer2RNAi resulted in larval mortality and was not sufficient to affect doublesex splicing, whereas RNAi targeting Sex-lethal and two putative orthologs of hermaphrodite yielded 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 non-representative 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.

developmental biology↗