From molecules to societies and back again: the relationship between social evolution and genome evolution

社会性的兴起代表了进化论中的一次重大转变，这让生物学家困惑了几个世纪。群居昆虫表现出生殖利他主义：工蚁放弃繁殖，以帮助它们的母亲繁殖。目前关于社会性如何以及为什么进化的理论假定了一种简单的进化模式，即社会性的进化独立于基因组进化而进行。然而，越来越多的证据表明，社会性昆虫基因组的衍生特征反映了社会性引起的变化。社会行为是否改变了基因组进化的模式，从而增强或在某些情况下限制了社会等位基因的传播？ 我们的团队领导了一项开创性的研究，将蜜蜂基因组结构的特征与工蜂特征的进化联系起来。在接下来的五年里，我们计划通过回答以下问题来揭示社会进化和基因组进化之间缺失的联系： 1)社会性会增加遗传负荷吗？据预测，社会人口的有效规模将大幅减少，这削弱了自然选择的力量。因此，社会基因组预计会包含更多略微有害的突变，这些突变会降低适合度(即更高的基因负载)。我们将比较许多群居昆虫和独居昆虫的基因组序列中的遗传多样性和有害突变的频率，以验证这一假设。 2)社会性是否会增加突变率和偏见？皇后往往寿命长，减数分裂重组率高；这两个特征预计都会影响突变过程--这是一个基本的进化参数。我们将量化和对比群居昆虫和独居昆虫基因组中的突变偏向。我们还将直接估计蜜蜂基因组的突变率，并研究突变是否与高重组和/或高寿命有关。 3)性别决定负荷是否限制了社会性的演变？蚂蚁、蜜蜂和黄蜂有一种性别决定形式，在小种群中施加了大量的遗传负荷。这种遗传负荷可能会限制或逆转社会性的进化：我们将使用模拟模型来检验这一假设，这些模型明确地解释了社会进化过程中的性别决定。 4)蜜蜂亲缘识别的机制和进化基础是什么？我们将使用目标基因组测序、碳氢化合物气味线索的化学分析和蜜蜂工作者的行为分析的新组合来研究这一社会进化的前驱特征。 我提出的研究有很大的潜力来改变生物学家对社会性的思考方式，因为它阐明了社会行为如何影响基因组进化的模式，这些模式是反馈的，并改变了社会群体的进化轨迹。这里提出的变革性研究将帮助我们理解动物社会性的兴起和稀有。

The rise of sociality represented a major transition in evolution that puzzled biologists for centuries. Social insects exhibit reproductive altruism: workers forgo reproduction to help their mother reproduce. Current theories for how and why sociality evolved assume a simple model of evolution where the evolution of sociality proceeds independently of genome evolution. However, there is a growing body of evidence showing that derived features of social insect genomes reflect changes caused by sociality. Does social behaviour alter patterns of genome evolution in ways that can enhance or, in some cases, limit the spread of social alleles? Our group has led pioneering studies that linked features of genome structure with the evolution of worker traits in honey bees. Over the next five years, we plan to uncover the missing links between social evolution and genome evolution by answering the following questions: 1) Does sociality increase genetic loads? Social populations are predicted to have large reductions in effective size, which weakens the strength of natural selection. As a consequence, social genomes are expected to harbour more slightly deleterious mutations that reduce fitness (i.e. higher genetic load). We will compare genetic diversity and the frequency of deleterious mutations in the sequenced genomes of many social and solitary insects to test this hypothesis. 2) Does sociality increase mutation rates and biases? Queens tend to be long lived and tend to have high rates of meiotic recombination; both features are expected to influence the mutational process – a fundamental evolutionary parameter. We will quantify and contrast mutational biases in social versus solitary insect genomes. We will also directly estimate the mutation rate in honey bee genomes and study if mutation is linked to high recombination and/or high longevity. 3) Does the sex-determination load limit the evolution of sociality? Ants, bees and wasps have a form of sex determination that imposes a substantial genetic load in small populations. This genetic load may limit or reverse the evolution of sociality: we will test this hypothesis using simulation models that explicitly account for sex determination during social evolution. 4) What is the mechanistic and evolutionary basis of kin-recognition in bees? We will study this precursor trait for social evolution using a novel combination of targeted genome sequencing, chemical analysis of hydrocarbon scent cues, and behavioral assays of honey bee workers. My proposed research has a great potential for changing the way biologists think about sociality by illuminating how social behaviour influences patterns of genome evolution that ‘feedback’ and alter the evolutionary trajectory of social populations. The transformational research proposed herein will help us understand both the rise and rarity of sociality in animals.