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.
Chemical communication underlies the sophisticated colony organization of social insects. In these insects, cuticular hydrocarbons (CHCs) play central roles in nestmate, task, and caste recognition, which contribute to maintenance of the social and reproductive division of labor. Queen-specific CHCs reflect queen fertility status and function as a queen recognition pheromone, triggering aggregation responses around the queens. However, there are only a few studies about the royal recognition mechanism in termites, and particularly, no study has reported about queen-specific CHCs in the species using asexual queen succession (AQS) system, in which the primary queen is replaced by neotenic queens produced parthenogenetically. In this study, we identified the CHC pheromone for neotenic queen recognition in the AQS termite species Reticulitermes speratus. Gas chromatography-mass spectrometry analyses revealed that the relative amount of n-pentacosane was disproportionately greater in the CHC profiles of queens than in the CHC profiles of kings, soldiers, and workers. Furthermore, we investigated the cuticular chemicals of the queen aggregate workers; bioassays demonstrated that n-pentacosane shows a worker arrestant activity in the presence of workers’ cuticular extract. These results suggest that R. speratus workers identify whether each individual is a neotenic queen by recognizing the relatively higher ratio of n-pentacosane in the conspecific CHC background. Moreover, they suggest that termites have evolved queen recognition behavior, independently of social hymenopterans.
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