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Molecular basis of reproductive plasticity of termite workers under environmental stresses

ABSTRACT: Eusociality is an important step in animal evolution that increases the level of biological complexity. The reproductive plasticity of termite female workers provides colonies with the tremendous flexibility to respond to environmental (social) stresses. Here, we established an “inhibition-activation-reinhibition” research model of the reproductive transformation of female workers using three Reticulitermes species. We identified the functional genes involved in the transformation process, explaining why the transformation of workers to reproductives in R. aculabialis were not triggered under the same isolation conditions. Transposable elements in the brains of workers promote the transformation of workers into reproductives. The metabolic levels were associated with changes in stress caused by female reproduction and the nest environment. Strikingly, we confirmed that when female workers experience severe environmental stresses that affect their survival, they do not initiate reproductive transformation, even if there is no female reproductive in the nests. Furthermore, based on the regulatory network of molecules, we constructed machine learning models to demonstrate how numerous genes co-regulate the reproductive plasticity of workers and to predict the fertility of colonies. Among these, deep neural network models had the highest prediction accuracy and generalization, indicating that workers carry a wealth of information about their colony at the molecular level. We suggest that combined molecular function and deep learning model analysis for caste differentiation, reproductive plasticity, colony development and adaptation will provide a methodology for revealing complex gene regulatory networks that respond to environmental changes in social insects. Our findings are essential for understanding the reproductive plasticity of humans and other social animals to respond to environmental changes and social stresses.

ORGANISM(S): Reticulitermes Labralis

SUBMITTER: Xiaohong Su

PROVIDER: PXD060499 | iProX | Wed Jan 29 00:00:00 GMT 2025

REPOSITORIES: iProX

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Project description:In many animals living in groups the reproductivestatus of individuals is determined by their social status. In specieswith social hierarchies, the death of dominant individuals typicallyupheaves the social hierarchy and provides an opportunity for subordinateindividuals to improve their social status. Such a phenomenon occursin the monogyne form of the fire ant\emph{, Solenopsis invicta, }wherecolonies typically contain a single wingless reproductive queen, thousandsof workers and hundreds of winged non-reproductive virgin queens.Upon the death of the mother queen, many virgin queens shed theirwings and initiate reproductive development instead of departing ona mating flight. Workers progressively execute almost all of themover the following weeks. The workers base their collective decisionon pheromonal cues associated with the onset of reproductive developmentof the virgin queens which occurs after orphaning. To examine the factors that determine which virgin queens are executed and which survive, we set up artificial competitions between queens from different colonies. Using microarrays, we found that queens from winning colonies showed higher mitochondrial as well as organ development activities 24 hours after orphaning than did queens from colonies that lost the competitions. Furthermore, queens from colonies where queens shed their wings faster after orphaning were more likely to survive competitions. Finally, higher wing shedding speed is linked to higher mitochondrial activity. Eight competitions were initially conducted between queens form pairs of colonies. Six competitions clearly identified one winning colony and one losing colony. We thus have microarray data for six competitions (ie biological replicates), with one winning and one losing colony within each competition. Thus 12 colonies total. For each colony, RNA extracted from five queens was pooled, and hybridized against an unrelated common reference RNA that had been made from a pool of many S. invicta individuals of all castes and developmental stages. Lab work was conducted in blocks (by competition) with randomized order within competition to avoid introducing bias. No technical replication was performed.

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Molecular basis of reproductive plasticity of termite workers under environmental stresses

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