Genome-wide detection of selection and adaptation in a slavemaking ant and its co-evolving host

敌对物种之间的共同进化可以推动进化军备竞赛--共同适应的互惠循环。测序技术的最新进展使得现在可以在非模型系统的基因组水平上研究进化适应的分子基础。在这个项目中，我们专注于一个研究得很好的寄主-寄生虫系统，该系统由专性的社会寄生虫美洲淡马胸蚁及其相关的寄主长胸蚁组成，对于这个系统，存在着充分的共同进化和局部适应的证据。在我们的第一个资助阶段，我们使用转录转录技术研究了三个奴役蚂蚁和它们的三个寄主种Temnothorax的奴隶袭击和宿主防御行为背后的基因。我们检测到候选基因在奴隶袭击和选择过程中上调。首先，RNAi实验揭示了它们在控制袭击行为方面的潜在功能。我们发现物种之间几乎没有重叠，无论是在差异表达的基因之间还是在选择中的基因之间，都表明了物种特有的进化轨迹。第一个种群水平的项目表明，宿主反应和脑基因表达取决于奴隶制造者的来源，即奴隶制造者群体中寄生虫的流行情况。在第二个资助阶段，我们建议更进一步，在全基因组水平上研究共同进化的分子基础。这是可能的，因为我们最近获得并注释了我们的两个主要模式物种的基因组。我们将使用一个“自然实验”的种群，在这个实验中，宿主和寄生虫以共生或异地进化。我们建议研究适应的遗传背景，选择的类型和强度，以及主要调节区或蛋白质编码基因是否对共适应重要。我们将使用全基因组Pool-Seq和来自12个寄主和8个寄生虫种群的蚂蚁基因组重测序相结合的方法来确定选择和连锁的基因和区域。我们将表征所有种群的化学特征(角质碳氢化合物和Dufour腺体分泌物)和组织特异性基因表达，以便能够进行全基因组关联研究，并将基因组信息与化学、转录和行为表型联系起来。通过分析相似选择机制下的多个种群，我们可以揭示协同进化是在不同的地点采取不同的途径，还是平行发生。一旦我们确定了感兴趣的候选基因座，我们将进行功能性RNAi分析，以实验表征它们对表型的影响。总体而言，我们的研究将有助于更好地理解共同进化过程中适应的遗传机制。

Coevolution between antagonistic species can drive evolutionary arms races - reciprocal cycles of coadaptation. Recent advances in sequencing technologies allow now to study the molecular basis of evolutionary adaptations on a genomic level in non-model systems. In this project, we focus on a well-studied host-parasite system consisting of the slavemaking ant Temnothorax americanus, an obligate social parasite, and its related host Temnothorax longispinosus, for which ample evidence for coevolution and local adaptation exists. During our 1stfunding phase, we used transcriptomics to investigate, which genes underlie slave raiding and host defense behavior in three slavemaking ants and their three host species of the genus Temnothorax. We detected candidate genes upregulated during slave raids and under selection. First RNAi experiments revealed their potential function in controlling raiding behaviors. We found little overlap between species, both among the differentially expressed genes and those under selection, indicating species-specific evolutionary trajectories. A first population-level project demonstrated that host responses and brain gene expression depends on slavemaker origin, that is parasite prevalence of the slavemaker population. In the 2nd funding phase, we propose to go a step further and investigate the molecular basis of coevolution on a genome-wide level. This is possible as we recently obtained and annotated the genomes of our two main model species. We will use populations of a “natural experiment”, in which host and parasite evolve in sympatry (=coevolve) or allopatry. We propose to study the genetic background of adaptations, the types and strength of selection and whether mainly regulatory regions or protein-coding genes are important for coadaptation. We will use a combination approach of genome-wide Pool-Seq and Resequencing ant genomes from 12 host and 8 parasite populations to determine genes and regions under selection and linkage. We will characterize chemical traits (cuticular hydrocarbons and Dufour gland secretions) and tissue-specific gene expression of all populations to be able conduct a genome-wide association study and link the genomic information to chemical, transcriptomic and behavioral phenotypes. By analyzing multiple populations under similar selective regimes, we can reveal whether coevolution takes different avenues in different locales or whether it occurs in parallel. Once we have identified interesting candidate loci, we will conduct functional RNAi analyses to characterize their effect on the phenotype experimentally. Overall, our study will contribute to a better understanding of genetic mechanisms of adaptation during coevolution.