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Rajakumar, R.

Publications and source records attributed to Rajakumar, R..

7 recordsLinked to original sources

Ecdysone Antagonizes Growth and Juvenile Hormone-Dependent Soldier Caste Identity in Camponotus floridanus

From tardigrades to lobsters, ecdysone is the critical steroid hormone regulating ecdysis across Panarthropoda. In insects, the sesquiterpenoid hormone called juvenile hormone (JH) prolongs the juvenile state, and together, ecdysone and JH regulate growth and developmental timing. The complex worker caste system in ants has elaborated multiple times and is composed of individuals exhibiting an array of size and allometry variation. While we have accumulated a great deal of knowledge related to the role of JH in influencing size and caste identity in ants, the role of ecdysone in caste development remains poorly understood. Here we show in Camponotus floridanus that ecdysone negatively regulates size, can block soldier determination, and there is an antagonistic relationship between JH and ecdysone. First, we show that during the worker-soldier switchpoint sensitivity window of development, ecdysone is capable of negatively influencing head size, body size, head-to-body allometry, and unexpectedly extends developmental timing. We then show at the molecular level that as expected, developing soldiers upregulate ecdysone degradation, yet surprisingly, developing soldiers also upregulate ecdysone synthesis and the reception of ecdysone signalling. We next investigated the interaction between JH and ecdysone signaling and found that the two hormones antagonize each other at both the molecular and phenotypic levels. Furthermore, in contrast to other insects, we uncovered that ecdysone signaling is negatively regulated by temperature. Beyond its role in size regulation, we also provide preliminary data suggesting that the interaction of JH and ecdysone may have sex inducing properties, generating male-like anomalies. Altogether, our findings show that ecdysone blocks JH-dependent soldier development and we propose that the dynamic regulation of ecdysone synthesis, reception, and degradation may be the basis for the complex sigmoid-like head-to-body allometry found in this species as well as several others across ants. More generally, the evolutionary tinkering of antagonistic growth hormones, their regulation and interaction, and opposing responses to environmental cues, may be a major source for size diversity across developmentally plastic organisms.

developmental biology↗

The Environmental, Endocrine, and Epigenetic Basis of Size Plasticity in a Superorganism

From plants to animals, genomes are responsive to environmental variation, the interaction of which can influence developmental processes and facilitate profound consequences on life-history and evolution. The interplay between genes and the environment is known to be mediated by the action of endocrine and epigenetic mechanisms including histone modifications. Ant development is plastic: environmental changes can induce diverse phenotypes, generating different castes that distinguish individuals by size, behaviour, and reproduction. While recent work has demonstrated that hormonal and epigenetic mechanisms underlie caste-specific trait variation in ants, the interplay of these mechanisms, and the process by which they mediate environmental changes to produce distinct trait variation, remains enigmatic. Here, we use the invasive fire ant Solenopsis invicta, dubbed a superorganism and known for its extreme worker caste size variation, to investigate the interplay between endocrine and epigenetic mechanisms in response to environmental variation. We found that sizing and developmental timing are both thermally and nutritionally plastic, influenced by juvenile hormone, ecdysone, histone (de)acetylation, and histone (de)methylation, and that these mediators interact and are thermally and nutritionally plastic. Surprisingly, fire ants break the Temperature-Size Rule, ecdysone makes ants bigger faster, and histone methylation disruption unexpectedly makes ants smaller. These and other findings suggest that an endocrine-epigenetic axis mediates thermal and nutritional plasticity underlying the extreme size variation that has evolved in the complex worker caste system in fire ants. More generally, we propose that an environment-endocrine-epigenetic (E3) approach will provide an integrative perspective on the development and evolution of adaptive phenotypes.

developmental biology↗

Keeping an Eye on Plasticity Genes: Insulin/TOR Pathway Components Mediating Nutritional Plasticity of Eyes Within and Between Sex

The eyes of insects exhibit extreme morphological variation through changes in size and shape. While the model organism Drosophila melanogaster has been used to elucidate the underlying gene networks and cell-signalling pathways that regulate the patterning and growth of the eye, insight into the regulators of nutrient-dependent growth and allometry within and between the sexes remains poorly understood. Here we show that perturbations of different nodes of the Insulin/TOR pathway modulate the impact of nutritional variation on the growth of the eye to varying degrees, and that this is further influenced by sex. When starved, wild-type flies decrease in eye size and body size isometrically in females, yet males change eye-to-body size allometrically. Subsequently we used eye-specific RNAi to knockdown each component of the Insulin/TOR pathway to characterize the influence each component has in modulating nutritional plasticity of the sizing properties of the eye. Surprisingly, this resulted in a range of size and scaling variation, components modulating the plastic response on eye size mean, eye-to-body slope, intercept, as well as eye size variance, some effects ranging in magnitude from shutting off plasticity to amplifying, and some which were sex-limited. Therefore, components of the Insulin/TOR pathway vary in their degree and ability to influence the effect of nutritional variation on eye growth within and between sexes in terms of average size, allometry at both the level of intercept and slope, as well as the degree of variance. More generally, the morphospace and allometry of a trait can evolve within and across the sexes through modifications of plasticity genes that mediate gene-by-environment interactions.

genetics↗

Evolution and Regulation of Decoupled Dimorphic Scaling Patterns in Ants

Allometric evolution, changing how morphological traits scale disproportionately to body size, has fuelled adaptive radiations. In ants, allometry has facilitated the repeated evolution of a worker-soldier caste system. Here we reveal an unexpected scaling pattern, and its superorganismal regulation, within the hyperdiverse genus Pheidole. We discovered that antennal sizing between the small worker and the big soldier is identical, lacking inter-caste scaling (antennae-body scaling is decoupled) yet retaining intra-caste scaling. Furthermore, we have pinpointed the evolutionary origin of this decoupling. Finally, manipulations of social environment, developmental hormones, and interorgan signalling influences the modularity-integration of trait-body covariation, uncovering head-to-body decoupling and the production of novel nanosoldiers. Collectively, this challenges our previous understandings of trait covariation, modularity, and their regulation, from individual to society and across species.

developmental biology↗

Juvenile Hormone Signalling Underlies the Switchpoint and Differentiation of Soldiers in Camponotus floridanus

Multicellular organisms are composed of various cell types derived from cellular determination and differentiation, which carry out specialized functions in the individual. Ant societies are composed of various castes of individuals derived from caste determination and differentiation, which divide specialized tasks in the colony. From cells to societies, the underlying mechanisms orchestrating determination and differentiation at different biological levels are fundamental in generating biological diversity. While past work has described the developmental process of caste determination and differentiation in ants, the endocrinological and molecular basis for these processes in the genus Camponotus remains unknown. Here we show that minor worker and soldier development is determined by a Juvenile hormone (JH)-mediated minor-soldier switchpoint in C. floridanus. Hormonal treatments identified a sensitivity period when JH can induce bipotential larvae to become soldiers. Induced soldiers phenocopy natural soldiers in size and soldier-specific head-to-body allometry and this is associated with a heterochronic shift in metamorphosis. Furthermore, we molecularly characterize the activity of the JH pathway at the level of synthesis, degradation, reception, and downstream effectors during caste determination and differentiation. Surprisingly, rather than JH synthesis, we found JH reception and JH degradation are the major signalling processes differentially regulated across castes and RNAi of juvenile hormone degradation enzymes generates soldiers. Finally, our data suggests that the hyperdiverse genus Camponotus has independently evolved a JH-mediated minor-soldier switchpoint similar to that known in Pheidole. More generally, the evolution of plastic hormonal regulation may facilitate the origin of developmental determination and differentiation processes underlying complex adaptive phenotypes. Significance StatementAnts live in complex societies like a superorganism where individuals divide reproductive and various non-reproductive labors, which are analogous to the array of functions of germ cells and highly differentiated somatic cells in an organism. While there are over 1500 species of the hyperdiverse genus Camponotus, a genus whose diversity reflects their complex caste system including minor workers and soldiers, the molecular and endocrinological basis for how these castes develop remains unknown. Here we have identified a juvenile hormone (JH) mediated minor-soldier switchpoint during larval development, and have characterized components of the JH signalling pathway that regulate soldier development. This work enables further understanding of how castes are regulated across ants and social insects more broadly.

developmental biology↗

Next generation CRISPR/Cas9 transcriptional activation in Drosophila using flySAM

CRISPR/Cas9-based transcriptional activation (CRISPRa) has recently emerged as a powerful and scalable technique for systematic over-expression genetic analysis in Drosophila melanogaster. We present flySAM, a potent new tool for in vivo CRISPRa, which offers a major improvement over existing strategies in terms of effectiveness, scalability, and ease-of-use. flySAM outperforms existing in vivo CRISPRa strategies, and approximates phenotypes obtained using traditional Gal4-UAS over-expression. Further, because flySAM typically only requires a single sgRNA, it dramatically improves scalability. We use flySAM to demonstrate multiplexed CRISPRa, which has not been previously shown in vivo. In addition, we have simplified the experimental usage of flySAM by creating a single vector encoding both the UAS:Cas9-activator and the sgRNA, allowing for inducible CRISPRa in a single genetic cross. flySAM will thus replace previous CRISPRa strategies as the basis of our growing genome-wide transgenic over-expression resource, TRiP-OE.

genetics↗

The genome of the water strider Gerris buenoi reveals expansions of gene repertoires associated with adaptations to life on the water

The semi-aquatic bugs conquered water surfaces worldwide and occupy ponds, streams, lakes, mangroves, and even open oceans. As such, they inspired a range of scientific studies from ecology and evolution to developmental genetics and hydrodynamics of fluid locomotion. However, the lack of a representative water strider genome hinders thorough investigations of the mechanisms underlying the processes of adaptation and diversification in this group. Here we report the sequencing and manual annotation of the Gerris buenoi (G. buenoi) genome, the first water strider genome to be sequenced so far. G. buenoi genome is about 1 000Mb and the sequencing effort recovered 20 949 predicted protein-coding genes. Manual annotation uncovered a number of local (tandem and proximal) gene duplications and expansions of gene families known for their importance in a variety of processes associated with morphological and physiological adaptations to water surface lifestyle. These expansions affect key processes such as growth, vision, desiccation resistance, detoxification, olfaction and epigenetic components. Strikingly, the G. buenoi genome contains three Insulin Receptors, a unique case among metazoans, suggesting key changes in the rewiring and function of the insulin pathway. Other genomic changes include wavelength sensitivity shifts in opsin proteins likely in association with the requirements of vision in water habitats. Our findings suggest that local gene duplications might have had an important role during the evolution of water striders. These findings along with the G. buenoi genome open exciting research opportunities to understand adaptation and genome evolution of this unique hemimetabolous insect.

genomics↗