The evolutionary significance of epigenetic inheritance is controversial. While epigenetic marks such as DNA methylation can affect gene function and change in response to environmental conditions, their role as carriers of heritable information is often considered anecdotal. Indeed, near-complete DNA methylation reprogramming, as occurs during mammalian embryogenesis, is a major hindrance for the transmission of nongenetic information between generations. Yet it remains unclear how general DNA methylation reprogramming is across the tree of life. Here we investigate the existence of epigenetic inheritance in the honey bee. We studied whether fathers can transfer epigenetic information to their daughters through DNA methylation. We performed instrumental inseminations of queens, each with four different males, retaining half of each male’s semen for whole genome bisulfite sequencing. We then compared the methylation profile of each father’s somatic tissue and semen with the methylation profile of his daughters. We found that DNA methylation patterns were highly conserved between tissues and generations. There was a much greater similarity of methylomes within patrilines (i.e., father-daughter subfamilies) than between patrilines in each colony. Indeed, the samples’ methylomes consistently clustered by patriline within colony. Samples from the same patriline had twice as many shared methylated sites and four times fewer differentially methylated regions compared to samples from different patrilines. Our findings indicate that there is no DNA methylation reprogramming in bees and, consequently, that DNA methylation marks are stably transferred between generations. This points to a greater evolutionary potential of the epigenome in invertebrates than there is in mammals.

表观遗传的进化意义存在争议。虽然 DNA 甲基化等表观遗传标记可以影响基因功能并根据环境条件而发生变化，但它们作为遗传信息载体的作用通常被认为是轶事。事实上，在哺乳动物胚胎发生过程中发生的近乎完全的DNA甲基化重编程是非遗传信息在代际间传递的主要障碍。然而，目前尚不清楚 DNA 甲基化重编程在整个生命树中的普遍情况。在这里，我们研究了蜜蜂表观遗传的存在。我们研究了父亲是否可以通过 DNA 甲基化将表观遗传信息传递给女儿。我们对蜂王进行了仪器授精，每个蜂王有四个不同的雄性，保留每个雄性的一半精液进行全基因组亚硫酸氢盐测序。然后，我们将每个父亲的体细胞组织和精液的甲基化谱与其女儿的甲基化谱进行了比较。我们发现 DNA 甲基化模式在组织和世代之间高度保守。父系（即父女亚科）内的甲基化组的相似性比每个群体中父系之间的相似性要大得多。事实上，样本的甲基化组在菌落内一致地按父系聚集。与来自不同父系的样本相比，来自同一父系的样本具有两倍的共享甲基化位点和四倍的差异甲基化区域。我们的研究结果表明，蜜蜂中不存在 DNA 甲基化重编程，因此，DNA 甲基化标记在世代之间稳定转移。这表明无脊椎动物的表观基因组比哺乳动物具有更大的进化潜力。