Fluctuating environments threaten fertility and viability. To better match the immediate, local environment, many organisms adopt alternative phenotypic states, a phenomenon called "phenotypic plasticity." Natural populations that predictably encounter fluctuating environments tend to be more plastic than conspecific populations that encounter a constant environment, suggesting that phenotypic plasticity can be adaptive. Despite pervasive evidence of such "adaptive phenotypic plasticity," gene regulatory mechanisms underlying plasticity remains poorly understood. Here we test the hypothesis that environment-dependent phenotypic plasticity is mediated by epigenetic factors. To test this hypothesis, we exploit the adaptive reproductive arrest of Drosophila melanogaster females, called diapause. Using an inbred line from a natural population with high diapause plasticity, we demonstrate that diapause is determined epigenetically: only a subset of genetically identical individuals enter diapause and this diapause plasticity is epigenetically transmitted for at least three generations. Upon screening a suite of epigenetic marks, we discovered that the active histone marks H3K4me3 and H3K36me1 are depleted in diapausing ovaries. Using ovary-specific knockdown of histone mark writers and erasers, we demonstrate that H3K4me3 and H3K36me1 depletion promotes diapause. Given that diapause is highly polygenic, that is, distinct suites of alleles mediate diapause plasticity across distinct genotypes, we also investigated the potential for genetic variation in diapause-determining epigenetic marks. Specifically, we asked if these histone marks were similarly depleted in diapause of a genotypically distinct line. We found evidence of divergence in both the gene expression program and histone mark abundance. This study reveals chromatin determinants of phenotypic plasticity and suggests that these determinants may be genotype-dependent, offering new insight into how organisms may exploit and evolve epigenetic mechanisms to persist in fluctuating environments.

中文翻译：

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组蛋白甲基化调节果蝇的生殖滞育。

波动的环境威胁着生育力和生存能力。为了更好地匹配直接的局部环境，许多生物体采用替代的表型状态，这种现象称为“表型可塑性”。可预见地遇到波动环境的自然种群往往比遇到恒定环境的同种种群更具可塑性，这表明表型可塑性具有适应性。尽管有普遍的证据表明这种“适应性表型可塑性”，但可塑性背后的基因调控机制仍然知之甚少。在这里，我们检验了环境依赖性表型可塑性是由表观遗传因素介导的假设。为了检验这一假设，我们利用雌性果蝇的适应性繁殖停滞（称为滞育）。使用来自具有高滞育可塑性的自然群体的近交系，我们证明滞育是由表观遗传决定的：只有遗传相同的个体的子集进入滞育，并且这种滞育可塑性通过表观遗传传递至少三代。通过筛选一系列表观遗传标记，我们发现活性组蛋白标记 H3K4me3 和 H3K36me1 在滞育卵巢中被耗尽。使用组蛋白标记写入器和擦除器的卵巢特异性敲低，我们证明 H3K4me3 和 H3K36me1 耗尽会促进滞育。鉴于滞育是高度多基因的，即不同的等位基因套件介导不同基因型的滞育可塑性，我们还研究了决定滞育的表观遗传标记的遗传变异的潜力。具体来说，我们询问这些组蛋白标记是否在基因型不同的系的滞育中同样被耗尽。我们发现基因表达程序和组蛋白标记丰度存在差异的证据。这项研究揭示了表型可塑性的染色质决定因素，并表明这些决定因素可能是基因型依赖性的，为生物体如何利用和进化表观遗传机制以在波动的环境中持续存在提供了新的见解。