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

This topic is “a first for GEITP” (!!) : studying developmental evolution in the dung beetle. In our 16 years of existence, GEITP is certain that we’ve never discussed gene regulation in the dung beetle before…!! ☹

This is a horned dung beetle, they are known to be the strongest insect in the world, They Can Lift 200-1141 Times Their Own Body Weight. These Insects Tend to be 0.75

But, even the genomes of beetles can “sense” environmental pressures (signals such as nutrition from food), and then, downstream, genetic networks are altered in order to produce morphological changes (e.g., size and shape of head horns) that will make the animal more likely to survive (e.g., success in fighting off other males before breeding) in its changing environment.

Recall that epigenetic regulation of genes includes DNA methylation, RNA-interference, histone modifications and chromatin-remodeling. This study involves histone-marking and chromatin-remodeling — inferred by DNA sequence differences in regions of the genome responsible for the horn morphology phenotype of these beetles. ☹

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 (horns on the head) — which are evolutionarily novel, secondary sexual weapons that exhibit remarkable intra- and inter-specific variation. Authors [see attached] investigated the evolutionary ”basis for horns,” as well as other key dung-beetle traits, via comparative genomic and developmental assays.

Phenotypic plasticity is defined as “the capacity of a single genotype to produce multiple phenotypes in response to environmental variation” and constitutes a ubiquitous property of multicellular life. Plasticity is thought to be an important driver of adaptation — allowing organisms to maintain high fitness in the face of environmental adversity and variability, as well as of diversification via evolutionary changes in the genetic architectures underlying plastic trait formation.

The ecological and evolutionary significance of phenotypic plasticity has received much attention, and diverse genes and signal transduction pathways have been identified as important mediators of plastic development across biological systems. In addition to coding sequence, epigenetic modifications such as histone marking are predicted to provide important mechanisms of plastic gene expression regulation. Furthermore, recent quantitative trait locus (QTL) analysis, combined with genome editing by CRISPR-Cas9, has begun to establish first causal connections between several cis-regulatory elements and the plastic development of nematode feeding structures. Yet, despite these advances, the genomic basis underlying developmental plasticity and its evolution, and in particular the role of the non-coding genome and chromatin architecture in regulating conditional responses in trait formation, remain largely unknown.

One group of animals that exhibit an extreme degree of phenotypic plasticity are the true dung beetles (Scarabaeinae) (yes, it’s spelled correctly ), a very diverse clade (>6,000 extant species) found on every continent except Antarctica. The extraordinary evolutionary success of this group is attributable at least in part to their ability to exploit an abundant resource inaccessible to most other insects — i.e., dung. For nearly every species, the acquisition and utilization of dung is essential to each aspect of these beetles’ life history. This includes not only consuming dung as a food source (coprophagy), but also as a resource for larval food provisioning and nest construction, thereby enabling a single offspring to complete development from egg to adult, within the confines of an underground brood-ball.

One key adaptation aiding in this strategy is a highly diversified degree of nutrition-responsive (plastic) development. In the case of dung beetles, nutrition-responsive development is a flexible developmental response to variable and limited larval food quality and quantity — resulting in a wide range of adult body sizes, which in turn has fueled the evolution of alternative, body size-dependent morphological, physiological, and behavioral phenotypes. Accordingly, phenotypic plasticity is predicted to be an evolutionary driver for many dung beetle adaptations.

Furthermore — due to their diversity, abundance, pronounced environment-sensitive development, and unique feeding and reproductive traits — dung beetles have thus long served as important models for behavioral (e.g., status-dependent selection and sperm competition models), developmental (e.g., mechanisms of plasticity), evolutionary (e.g., the origins of evolutionary novelties), and ecological studies (e.g., meta-population theory, nutrient recycling, soil aeration). However, despite the significance of dung beetles in both basic and applied science, a reference-quality genomic resource for any member of this insect group has so far been lacking.

Among the most conspicuous morphological trait of dung beetles are head horns — novel, highly diversified secondary sexual weapons used in reproductive competition. Horns vary tremendously in shape, size, and number across and within species, mediate widespread sexual dimorphisms, and exhibit a high degree of nutrition-responsive development among conspecific males (i.e., animals within the same species). Most commonly, horn development is limited to, and often exaggerated, in males whereas females are (usually) hornless.

Intriguingly, head horns lack homology to any other appendage or body part among Insecta, and as such qualify as an evolutionary novelty even by the strictest of definitions — yet gains, losses, and modifications to horn structure are common among even closely related species. Thus, beetle horns exhibit a high degree of evolutionary lability and represent a powerful natural system for understanding how complex traits originate and diversify.

This study began by presenting

chromosome-level genome assemblies of three dung beetle species in the tribe Onthophagini (>2500 extant species) — including Onthophagus taurus, O. sagittarius, and Digitonthophagus gazella. Comparing these assemblies (to those of seven other species across the order Coleoptera) identified evolutionary changes in coding sequence associated with metabolic regulation of plasticity and metamorphosis. Authors then contrasted chromatin accessibility in developing head horn tissues of high- and low-nutrition O. taurus males and females and identified distinct cis-regulatory architectures underlying nutrition — compared to sex-responsive development, including a large proportion of recently evolved regulatory elements sensitive to horn morphology determination.

Binding motifs of known, and new candidate, transcription factors were identified and are enriched in these nutrition-responsive open chromatin regions. This study highlights the importance of chromatin-state regulation in mediating the development and evolution of plastic traits, demonstrates that gene networks are highly evolvable transducers of environmental and genetic signals, and provides new reference-quality genomes for three species that will strengthen future developmental, ecological, and evolutionary studies of this insect group.
DwN
PLoS Genet March 2024; 20: e1011165
COMMENT:
Christine has sent GEITP a <> about this topic of the dung beetle. But — how many GEITPers will “understand” this joke…?? How many of us have read fictional novels written by Franz Kafka (1993-1924)…??

“I feel a metamorphosis coming on…”
F. Kafka ☹

Answer to my question above: Franz Kafka’s message in his short novel, The Metamorphosis, deals with modernist themes — such as isolation and the absurdity of life. In the story, the main character, Gregor, has devoted himself to his family. And the absurd situation of becoming an insect has left Gregor alienated from other humans…

DwN

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