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Ropalidia cyathiformis is a primitively eusocial tropical paper wasp usually with a single dominant queen per colony. When the queen is removed, one and only one individual increases her aggression and becomes the new queen of the colony, unchallenged by any other worker. We refer to such a successor as a potential queen (PQ) until she lays her first egg. By removing the queen and successive PQs, we show that there is not just one successor but a strict reproductive hierarchy of up to 3 PQs, who succeed the queen one after the other. Of many variables tested, we found that only the frequency of dominance behaviour is a significant predictor of whether or not an individual is part of the reproductive hierarchy and also of her position in the hierarchy. Dominance behaviour, however, does not perfectly predict the position of an individual in the reproductive hierarchy because we show that an average of three more dominant individuals, are bypassed when an individual becomes the next queen or PQ. This is in contrast to the reproductive hierarchy in the conspecific Ropalidia marginata , where age rather than dominance behaviour is a predictor (though imperfect once again) of an individual’s position in the queue. Taken together, our results suggest that (a) these two sister species have evolved two rather different mechanisms of reproductive caste differentiation, (b) that neither of them strictly conform either to the so-called “temperate” or “tropical” patterns of queen succession seen in most other species studied so far.

Eusocial insects exhibit the most striking example of phenotypic plasticity. There has been a long controversy over the factors determining caste development of individuals in social insects. Here we demonstrate that parental phenotypes influence the social status of offspring not through genetic inheritance but through genomic imprinting in termites. Our extensive field survey and genetic analysis of the termite Reticulitermes speratus show that its breeding system is inconsistent with a genetic caste determination model. We therefore developed a genomic imprinting model, in which queen- and king-specific epigenetic marks antagonistically influence sexual development of offspring. The model accounts for all known empirical data on caste differentiation of R. speratus and other related species. By conducting colony-founding experiments and additively incorporating relevant socio-environmental factors into our genomic imprinting model, we show the relative importance of genomic imprinting and environmental factors in caste determination. The idea of epigenetic inheritance of sexual phenotypes solves the puzzle of why parthenogenetically produced daughters carrying only maternal chromosomes exclusively develop into queens and why parental phenotypes (nymph- or worker-derived reproductives) strongly influence caste differentiation of offspring. According to our model, the worker caste is seen as a “neuter” caste whose sexual development is suppressed due to counterbalanced maternal and paternal imprinting and opens new avenues for understanding the evolution of caste systems in social insects.

Background Nuclear receptors (NRs) constitute a superfamily of transcription factors that regulate diverse biological processes. In insects, NRs not only govern essential physiological functions including metabolism, development, and reproduction, but also play pivotal roles in regulating caste differentiation and division of labor within social insect colonies. Pseudoregma bambucicola is a species of social aphid in which adults exhibit a specialized reproductive division of labor. This unique system produces first-instar nymphs and soldiers, which share an identical genetic background yet exhibit distinct morphological and behavioral traits. Although NRs exhibit pleiotropic regulatory capacities, their roles in the unique developmental patterns of P. bambucicola remain unclear. Results This study identified 21 NR genes based on the genomic data of P. bambucicola and analyzed the duplication and loss events of these genes through phylogenetic analysis. Additionally, differential expression of NR genes was analyzed using transcriptomic data. The TLL exhibited significant differential expression in adults with distinct reproductive behaviors, suggesting its involvement in the regulation of reproductive division of labor. E75 and HNF4 were found to be important for the post-embryonic development of soldiers. Furthermore, quantitative real-time PCR confirmed caste-specific expression patterns of HR4 and HR39 , indicating their potential involvement in morphological differentiation and developmental regulation among castes. Conclusions This study conducted bioinformatic identification of NR genes in the social aphid P. bambucicola , and investigated their potential roles in morphological differentiation and behavioral division through analysis of differential gene expression. The findings provide preliminary evidence for the functional significance of NR genes in social aphids, while offering novel insights for subsequent research exploration.

A key mechanistic hypothesis for the evolution of division of labour in social insects is that a shared set of genes co-opted from a common solitary ancestral ground plan (a genetic toolkit for sociality) regulates caste differentiation across levels of social complexity. Using brain transcriptome data from nine species of vespid wasps, we test for overlap in differentially expressed caste genes and use machine learning models to predict castes using different gene sets. We find evidence of a shared genetic toolkit across species representing different levels of social complexity. We also find evidence of additional fine-scale differences in predictive gene sets, functional enrichment and rates of gene evolution that are related to level of social complexity, lineage and of colony founding. These results suggest that the concept of a shared genetic toolkit for sociality may be too simplistic to fully describe the process of the major transition to sociality. A key hypothesis for the evolution of division of labour in social insects is that a shared set of genes – a genetic toolkit - regulates reproductive castes across species. Here, the authors analyze brain transcriptomes from nine species of social wasps to identify the factors that shape this toolkit.

The honeybee (Apis mellifera) is a highly social insect whose caste differentiation is regulated by epigenetic mechanisms, representing a classic example of phenotypic plasticity in social insects. Although the importance of transposable elements (TEs) in epigenetic research is well recognized, their specific role in honeybee caste differentiation has not been fully explored. This study reveals a novel regulatory mechanism where the microRNA (miRNA) ame-mir-3721-3p, derived from ApME (Apis miniature inverted-repeat TEs), suppresses DNA methyltransferase gene DNMT3, promoting queen-like development in honeybee larvae. Genome-wide analysis identified 43 ApME elements in Apis, with ApMETm15 being particularly abundant and species-specific. These elements gave rise to 6 miRNAs, including ame-mir-3721-3p which showed notable regulatory potential. Target gene prediction and luciferase reporter assays confirmed that ame-mir-3721-3p binds to and suppresses DNMT3 expression. Spatiotemporal expression analysis indicated that ame-mir-3721-3p is significantly upregulated during the critical L3 larval stage, exhibiting a similar expression pattern to DNMT3. Larval feeding experiments with agomir demonstrated that ame-mir-3721-3p suppresses DNMT3 expression and significantly impacts the expression of genes related to the juvenile hormone and ecdysone pathways. Further physiological evidence showed that when larvae were treated with agomir-3721 during the critical caste differentiation window (L3-L4 stage), the emerging adult bees exhibited increased body size, doubled ovarian area, and significantly higher frequency of ovary development, with significant upregulation of ovarian-specific marker genes. These findings provide direct evidence for ame-mir-3721-3p's role in promoting queen-like developmental trajectories during caste differentiation, uncovering a new regulatory pathway in honeybee development and offering insights into epigenetic mechanisms in social insects.

The major environmental determinants of honeybee caste development come from larval nutrients: royal jelly stimulates the differentiation of larvae into queens, whereas beebread leads to worker bee fate. However, these determinants are not fully characterized. Here we report that plant RNAs, particularly miRNAs, which are more enriched in beebread than in royal jelly, delay development and decrease body and ovary size in honeybees, thereby preventing larval differentiation into queens and inducing development into worker bees. Mechanistic studies reveal that amTOR, a stimulatory gene in caste differentiation, is the direct target of miR162a. Interestingly, the same effect also exists in non-social Drosophila. When such plant RNAs and miRNAs are fed to Drosophila larvae, they cause extended developmental times and reductions in body weight and length, ovary size and fecundity. This study identifies an uncharacterized function of plant miRNAs that fine-tunes honeybee caste development, offering hints for understanding cross-kingdom interaction and co-evolution.

The influence of gene expression on female caste determination in social Hymenoptera is one of the best-characterized examples of developmental polyphenism. We used mRNA-seq to profile differentially expressed genes (DEGs) between workers and queens at four development stages (early larvae: 1-day-old larvae; mid larvae: 5-day-old larvae; late larvae: 9-day-old larvae; and 7-day-old adult bee) of Bombus terrestris. When DEGs of different female castes were compared, it was found that there were more DEGs at the mid larval and adult stages than at other stages. Caste differentiation may be linked to candidate genes such as Vitellogenin, Kr-h1, Dnmt3, Hexamerin, Yellow, and Chymotrypsin-2. Additionally, the gene expression profiles were observed differently among the four development stages. Comparing one stage to the next showed that, more number of DEGs were found in queens than workers. In the investigation of how gene expression affects larval caste determination, WGCNA showed that five modules were closely associated with larval caste determination. The functions of genes were mainly enriched in energy metabolism and energy production within mitochondria, suggesting that the energy requirements during the larval development process varied between caste determination. The current study sheds light on the patterns of gene expression in the female caste of Bombus terrestris, which will be useful for future research on polyphenism through differential gene expressions.

Background Reproductive division of labor in eusocial insects is a striking example of a shared genetic background giving rise to alternative phenotypes, namely queen and worker castes. Queen and worker phenotypes play major roles in the evolution of eusocial insects. Their behavior, morphology and physiology underpin many ecologically relevant colony-level traits, which evolved in parallel in multiple species. Results Using queen and worker transcriptomic data from 16 ant species we tested the hypothesis that conserved sets of genes are involved in ant reproductive division of labor. We further hypothesized that such sets of genes should also be involved in the parallel evolution of other key traits. We applied weighted gene co-expression network analysis, which clusters co-expressed genes into modules, whose expression levels can be summarized by their ‘eigengenes’. Eigengenes of most modules were correlated with phenotypic differentiation between queens and workers. Furthermore, eigengenes of some modules were correlated with repeated evolution of key phenotypes such as complete worker sterility, the number of queens per colony, and even invasiveness. Finally, connectivity and expression levels of genes within the co-expressed network were strongly associated with the strength of selection. Although caste-associated sets of genes evolve faster than non-caste-associated, we found no evidence for queen- or worker-associated co-expressed genes evolving faster than one another. Conclusions These results identify conserved functionally important genomic units that likely serve as building blocks of phenotypic innovation, and allow the remarkable breadth of parallel evolution seen in ants, and possibly other eusocial insects as well.

Background The insect cuticle is mainly composed of exocuticle and endocuticle layers that consist of a large number of structural proteins. The thickness and synthesis of the exocuticle depend on different castes that perform various functions in alates, workers and soldiers. However, it is not clear whether the soft endocuticle is involved in the division of labour in termite colonies. To reveal the structural characteristics of the endocuticle in different castes, we investigated the thickness of endocuticle layers in alates, workers and soldiers of the termite Reticulitermes aculabialis , and then we sequenced their transcriptome and detected the endocuticle protein genes. The differential expression levels of the endocuticular protein genes were confirmed in the three castes. Results We found that there was a great difference in the thickness of the endocuticle among the alates, soldiers and workers. The thickest endocuticle layers were found in the heads of the workers 7.88 ± 1.67 μm. The endocuticle layer in the head of the workers was approximately three-fold and nine-fold thicker than that in the heads of soldiers and alates, respectively. The thinnest endocuticle layers occurred in the head, thorax and abdomen of alates, which were 0.86 ± 0.15, 0.76 ± 0.24 and 0.52 ± 0.17 μm thick, respectively, and had no significant differences. A total of 43,531,650 clean sequencing reads was obtained, and 89,475 unigenes were assembled. Of the 70 identified cuticular protein genes, 10 endocuticular genes that belong to the RR-1 family were selected. qRT-PCR analysis of the five endocuticular genes (SgAbd-2, SgAbd-9, Abd-5, SgAbd-2-like and Abd-4-like) revealed that the endocuticle genes were more highly expressed in workers than in soldiers and alates. Conclusion These results suggest that SgAbd and Abd are the key components of the endocuticle. We infer that the thicker endocuticle in workers is helpful for them to perform their functions against environmental stress.

The hallmark of social insects is their caste system: reproduction is primarily monopolized by queens, whereas workers specialize in the other tasks required for colony growth and survival. Pheromones produced by reining queens have long been believed to be the prime factor inhibiting the differentiation of new reproductive individuals. However, there has been very little progress in the chemical identification of such inhibitory pheromones. Here we report the identification of a volatile inhibitory pheromone produced by female neotenics (secondary queens) that acts directly on target individuals to suppress the differentiation of new female neotenics and identify n-butyl-n-butyrate and 2-methyl-1-butanol as the active components of the inhibitory pheromone. An artificial pheromone blend consisting of these two compounds had a strong inhibitory effect similar to live neotenics. Surprisingly, the same two volatiles are also emitted by eggs, playing a role both as an attractant to workers and an inhibitor of reproductive differentiation. This dual production of an inhibitory pheromone by female reproductives and eggs probably reflects the recruitment of an attractant pheromone as an inhibitory pheromone and may provide a mechanism ensuring honest signaling of reproductive status with a tight coupling between fertility and inhibitory power. Identification of a volatile pheromone regulating caste differentiation in a termite provides insights into the functioning of social insect colonies and opens important avenues for elucidating the developmental pathways leading to reproductive and nonreproductive castes.