“A genomic imprinting model of termite caste determination: Not genetic but epigenetic inheritance influences offspring caste fate”

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Kenji Matsuura, Nobuaki Mizumoto, Kazuya Kobayashi, Tomonari Nozaki, Tadahide Fujita, Toshihisa Yashiro, Taro Fuchikawa, Yuki Mitaka, and Edward L. Vargo (June 2018)

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Parental phenotypes influence caste differentiation of offspring through genomic imprinting in termites

King and queen of a termite Reticulitermes speratus
(Credit: Kenji Matsuura)

Is royalty an inherited trait in social insects? In termites, parental phenotypes influence the caste fate of the offspring. For example, female offspring of sexually matured queens and worker-derived males develop exclusively into queens, as do parthenogenetically produced daughters. Such heritable effects on caste propensity has been recognized as an evidence of genetic caste determination. Matsuura and colleagues (2018) demonstrate that parental phenotypes influence the social status of the offspring not through genetic inheritance but through genomic imprinting. They conducted extensive field survey and genetic analysis of the termite Reticulitermes speratus and concluded that the caste system of this species cannot be explained by genetic caste determination models. Alternatively, they documented a genomic imprinting caste determination system in termites, in which queen- and king-specific epigenetic marks antagonistically influence the sexual development of offspring and thus determine their caste fate. Their work emphasizes that the genomic imprinting model accounts for all known empirical data on caste differentiation in termites and explains the evolutionary processes underlying diverse reproductive systems. According to the genomic imprinting model, the worker caste is seen as a ‘neuter’ caste whose sexual development is suppressed due to counterbalanced maternal and paternal imprinting. This model opens new avenues for understanding the evolution of caste systems in social insects.


Abstract

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.