More Like this

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. 

   more » « less
2. Vertically inherited microbiota and environment‐modifying behaviors indirectly shape the exaggeration of secondary sexual traits in the gazelle dung beetle

   https://doi.org/10.1002/ece3.10666  

   Rohner, Patrick T.; Moczek, Armin P. (November 2023, Ecology and Evolution)

   Abstract Many organisms actively manipulate the environment in ways that feed back on their own development, a process referred to as developmental niche construction. Yet, the role that constructed biotic and abiotic environments play in shaping phenotypic variation and its evolution is insufficiently understood. Here, we assess whether environmental modifications made by developing dung beetles impact the environment‐sensitive expression of secondary sexual traits. Gazelle dung beetles both physically modify their ontogenetic environment and structure their biotic interactions through the vertical inheritance of microbial symbionts. By experimentally eliminating (i) physical environmental modifications and (ii) the vertical inheritance of microbes, we assess the degree to which (sym)biotic and physical environmental modifications shape the exaggeration of several traits varying in their degree and direction of sexual dimorphism. We expected the experimental reduction of a larva's ability to shape its environment to affect trait size and scaling, especially for traits that are sexually dimorphic and environmentally plastic. We find that compromised developmental niche construction indeed shapes sexual dimorphism in overall body size and the absolute sizes of male‐limited exaggerated head horns, the strongly sexually dimorphic fore tibia length and width, as well as the weakly dimorphic elytron length and width. This suggests that environmental modifications affect sex‐specific phenotypic variation in functional traits. However, most of these effects can be attributed to nutrition‐dependent plasticity in size and non‐isometric trait scaling rather than body‐size‐independent effects on the developmental regulation of trait size. Our findings suggest that the reciprocal relationship between developing organisms, their symbionts, and their environment can have considerable impacts on sexual dimorphism and functional morphology. 

   more » « less
3. Histone deacetylases regulate organ-specific growth in a horned beetle

   https://doi.org/10.1186/s13227-024-00223-5  

   Hu, Yonggang; Crabtree, Jordan R; Macagno, Anna_L M; Moczek, Armin P (December 2024, EvoDevo)

   Abstract 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 thathistone 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 diverseHDACsin the structure-specific growth of both sex-shared and sex-specific traits including evolutionarily novel structures in the horned dung beetleOnthophagus taurus. ResultsWe identified fiveHDACmembers whose downregulation yielded highly variable mortality depending on whichHDACmember was targeted. We then show thatHDAC1,3, and4operate in both a gene- and trait-specific manner in the regulation of nutrition-responsiveness of appendage size and shape. Specifically,HDAC 1, 3,or4knockdown diminished wing size similarly while leg development was differentially affected by RNAi targetingHDAC3andHDAC4. In addition, depletion ofHDAC3transcript 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 thatHDAC3andHDAC4pattern 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 amongHDACmembers contribute to morphological diversification of both conventional and recently evolved appendages. More generally, our work raises the possibility thatHDAC-mediated scaling relationships and their evolution may underpin morphological diversification within and across insect species broadly. 

   more » « less
4. Doublesex mediates species-, sex-, environment- and trait-specific exaggeration of size and shape

   https://doi.org/10.1098/rspb.2021.0241  

   Rohner, Patrick T.; Linz, David M.; Moczek, Armin P. (June 2021, Proceedings of the Royal Society B: Biological Sciences)

   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. 

   more » « less
5. Higher heat acclimation ability in a non-native versus a native dung beetle (Onthophagus spp.)

   https://doi.org/10.5061/dryad.sn02v6xc2  

   Mamantov, Margaret A; Sheldon, Kimberly S (January 2025, Dryad)

   Invasive species may be more capable of adjusting to climate warming via phenotypic plasticity than native species since plasticity is thought to increase invasion success. Physiological plasticity via acclimation is one way in which organisms can adjust their thermal tolerance in response to temperature change, but few studies have addressed whether invasive species have greater thermal plasticity compared to native congeners. Here we investigated whether thermal plasticity via temperature acclimation varies between two Onthophagus dung beetle species, the non-native Onthophagus taurus and the native Onthophagus hecate, collected from both Florida and Tennessee, USA. We expected the non-native O. taurus to demonstrate greater plasticity than the native O. hecate; we also predicted that beetles from Florida would have reduced plasticity since their environment is less thermally variable. To examine thermal plasticity, we measured shifts in time until loss of function (i.e., leg mobility) following acclimation to hot or cold temperature treatments. We found that non-native O. taurus from Florida acclimated to warm temperatures, increasing time to loss of function following warm treatments; unexpectedly, O. taurus from Tennessee showed no warm acclimation ability. Onthophagus hecate did not acclimate to warm temperatures in either location. In contrast, both species showed similar levels of cold acclimation. Taken together, our results suggest that the non-native species, O. taurus, will be more capable of using physiological adjustments to respond to climate warming than the native species, O. hecate. 

   more » « less