A Genomic Imprinting Model of Termite Caste Determination: Not Genetic but Epigenetic Inheritance Influences Offspring Caste Fate

A Genomic Imprinting Model of Termite Caste Determination: Not Genetic but Epigenetic Inheritance Influences Offspring Caste Fate
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DOI:
10.1086/697238
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发表时间:
2018-06-01
影响因子:
2.9
通讯作者:
Vargo, Edward L.
Vargo, Edward L.
中科院分区:
环境科学与生态学2区
文献类型:
--
作者:
Matsuura, Kenji;Mizumoto, Nobuaki;Vargo, Edward L.

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真社会性昆虫表现出表型可塑性的最突出的例子。社会性昆虫中决定个体种姓发展的因素一直存在争议。在这里,我们表明,父母的表型影响后代的社会地位,而不是通过遗传遗传,但通过基因组印记在白蚁。我们对散白蚁的广泛实地调查和遗传分析表明,其繁殖系统与遗传种姓决定模型不一致。因此,我们开发了一个基因组印记模型,其中女王和国王特定的表观遗传标记拮抗性影响后代的性发育。该模型可以解释所有已知的关于R. speratus和其他相关物种。通过进行殖民地建立实验和添加剂将相关的社会环境因素纳入我们的基因组印记模型,我们显示了基因组印记和环境因素在种姓决定的相对重要性。性表型的表观遗传的想法解决了为什么单性生殖产生的女儿只携带母系染色体专门发展成皇后和为什么父母的表型(若虫或工人衍生的生殖)强烈影响后代的种姓分化的难题。根据我们的模型,工人种姓被视为一个中性种姓,其性发育受到抑制,由于平衡的母亲和父亲的印记,并打开了新的途径,了解社会昆虫种姓制度的演变。
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.