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Moczek, A. P.

Publications and source records attributed to Moczek, A. P..

6 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↗

The dung beetle microbiome complements host metabolism and nutrition

Many multicellular organisms rely on communities of microbial organisms to properly benefit from their diets, for instance by assisting in the breakdown of complex polysaccharides, the synthesis of essential resources, detoxification, or even preventing putrefaction. Dung beetles commonly rely on herbivore dung as their main source of nutrition, a diet rich in recalcitrant, hard-to-digest plant polysaccharides yet poor in essential amino acids, which animals typically cannot synthesize on their own. The work presented here investigates the potential role of the host-associated microbial community in allowing these insects to thrive on their nutrient-poor diet. Specifically, we investigated if the microbiota of the bull-headed dung beetle, Onthophagus taurus, may be capable of synthesizing amino acids and breaking down complex plant polysaccharides. To do so we functionally annotated genes within metagenomically assembled genomes (MAGs) obtained via shotgun-metagenomic sequencing. The annotation of these MAGs revealed that bacteria found in association with O. taurus possess the metabolic potential necessary to bridge the gap between host metabolic needs and the limitations imposed by their diet. Specifically, O. taurus microbiota contain amino acid biosynthesis pathways and genes encoding cellulases and xylanases, both of which are absent in the beetle genome. Further, multiple functionally relevant bacterial taxa identified here have also been observed in other studies across diverse dung beetle species, possibly suggesting a conserved pool of dung beetle symbionts and metabolic functions. ImportanceHost-symbiont interactions allow animals to take advantage of incomplete and/or challenging diets and niches. The work presented here aims to identify the physiological and metabolic means by which host associated microbial species shape the ecology of one of the most speciose genera in the animal kingdom: dung beetles in the genus Onthophagus. Both larva and adult stages of most Onthophagus rely on herbivore dung, a diet rich in recalcitrant, hard-to-digest plant polysaccharides yet poor in essential amino acids, which animals typically cannot synthesize on their own. To utilize such a challenging diet, Onthophagus vertically transmit a maternally derived microbial community which supports normative development in immature individuals and maintenance and reproduction in adults. Taken together, Onthophagus extraordinary diversity, complex ecology, and varied relationship with their microbial associates make them an ideal system to investigate mechanisms and diversification of host-diet-microbiome interactions.

microbiology↗

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↗

Histone deacetylases regulate organ-specific growth in a horned beetle

BackgroundNutrient availability is among the most widespread means by which environmental variability affects developmental outcomes. Because almost all cells within an individual organism share the same genome, structure-specific growth responses must result from changes in gene regulation. Earlier work suggested that histone deacetylases (HDACs) may serve as epigenetic regulators linking nutritional conditions to trait-specific development. Here we expand on this work by assessing the function of diverse HDACs in the structure-specific growth of both sex-shared and sex-specific traits including evolutionarily novel structures in the horned dung beetle Onthophagus taurus. ResultsWe identified five HDAC members whose down-regulation yielded highly variable mortality depending on which HDAC member was targeted. We then show that HDAC1, 3, and 4 operate in both a gene- and trait-specific manner in the regulation of nutrition-responsiveness of appendage size and shape. Specifically, HDAC 1, 3, or 4 knockdown diminished wing size similarly while leg development was differentially affected by RNAi targeting HDAC3 and HDAC4. In addition, depletion of HDAC3 transcript resulted in a more rounded shape of genitalia at the pupal stage and decreased the length of adult aedeagus across all body sizes. Most importantly, we find that HDAC3 and 4 pattern the morphology and regulate the scaling of evolutionarily novel head and thoracic horns as a function of nutritional variation. ConclusionCollectively, our results suggest that both functional overlap and division of labor among HDAC members contribute to morphological diversification of both conventional and recently evolved appendages. More generally, our work raises the possibility that HDAC-mediated scaling relationships and their evolution may underpin morphological diversification within and across insect species broadly.

evolutionary biology↗

The oncometabolite L-2-hydroxyglutarate is a common product of Dipteran larval development

The oncometabolite L-2-hydroxyglutarate (L-2HG) is considered an abnormal product of central carbon metabolism that is capable of disrupting chromatin architecture, mitochondrial metabolism, and cellular differentiation. Under most circumstances, mammalian tissues readily dispose of this compound, as aberrant L-2HG accumulation induces neurometabolic disorders and promotes renal cell carcinomas. Intriguingly, Drosophila melanogaster larvae were recently found to accumulate high L-2HG levels under normal growth conditions, raising the possibility that L-2HG plays a unique role in insect metabolism. Here we explore this hypothesis by analyzing L-2HG levels in 18 insect species. While L-2HG was present at low-to-moderate levels in most of these species (<100 pmol/mg; comparable to mouse liver), Dipteran larvae exhibited a tendency to accumulate high L-2HG concentrations (>100 pmol/mg), with the mosquito Aedes aegypti, the blow fly Phormia regina, and three representative Drosophila species harboring concentrations that exceed 1 nmol/mg - levels comparable to those measured in mutant mice that are unable to degrade L-2HG. Overall, our findings suggest that one of the largest groups of animals on earth commonly generate high concentrations of an oncometabolite during juvenile growth, hint at a role for L-2HG in the evolution of Dipteran development, and raise the possibility that L-2HG metabolism could be targeted to restrict the growth of key disease vectors and agricultural pests.

developmental biology↗