The Genomic Basis of Social Parasitism: A Geographical Mosaic of Behavioural, Chemical, and Environmental Adaptations in a Widespread Host-Parasite System

Coevolutionary dynamics in host-parasite systems are driven by reciprocal selection and environmental pressures. When parasite and host are closely related and have similar evolutionary potentials, evolution may follow parallel trajectories, affecting the same traits and underlying genes. We investigate coevolution and its genomic basis in the dulotic ant parasite Temnothorax americanus and its host T. longispinosus across a broad climatic gradient using population genomics, genome-wide association and transcriptome analyses. Population genomics revealed a striking contrast: panmictic host populations versus structured parasite populations, consistent with geographic mosaic dynamics. Genomic responses to parasite prevalence were strongly asymmetric: hosts showed strong selection on immune and structural defence genes, potentially with pleiotropic social functions. Parasites exhibited weaker signals, often in regulatory genes linked to behavioural shifts critical for raiding. Both species displayed shared genomic signatures of climate adaptation (e.g., desiccation resistance, stress response), suggesting convergent physiological responses. Genes associated with host-parasite encounters (mechanosensation, circadian rhythms, venom) also showed parallel selection. Behavioural traits such as aggression showed limited genomic signals but potentially higher transcriptional plasticity. Associations with chemical traits revealed shared selection on genes involved in cuticular hydrocarbon biosynthesis and chemosensory perception, indicating evolutionary coupling of signal production and perception. Constitutive gene expression patterns diverged: host expression correlated with parasite prevalence, while parasite expression was more strongly linked to climate, reflecting contrasting regulatory pressures. Our study demonstrates how differing population structures, asymmetric reciprocal selection, and environmental context shape divergent genomic trajectories of coadaptation, reflecting distinct evolutionary architectures across a heterogeneous landscape.

宿主-寄生虫互作系统中的协同进化动力学由互惠选择（reciprocal selection）与环境压力共同驱动。当寄生虫与宿主亲缘关系较近且进化潜力相近时，二者的进化可能呈现平行轨迹，作用于同一性状及其底层调控基因。
本研究采用群体基因组学（population genomics）、全基因组关联分析（genome-wide association）及转录组分析（transcriptome analyses）方法，在宽泛的气候梯度范围内，针对蓄奴蚁寄生虫美洲钝切叶蚁（Temnothorax americanus）及其宿主长刺钝切叶蚁（T. longispinosus）的协同进化过程及其基因组基础展开探究。
群体基因组学分析揭示了显著差异：宿主种群为泛交种群（panmictic population），而寄生虫种群则呈现结构化特征，这与地理镶嵌进化动力学（geographic mosaic dynamics）的理论预期相符。
宿主针对寄生虫感染率的基因组响应呈现显著不对称性：宿主在免疫与结构防御基因上受到强烈选择压力，这类基因可能同时具备多效性（pleiotropic）的社会功能。寄生虫的基因组响应信号则相对较弱，相关基因多为与劫掠行为关键转变相关的调控基因。
两个物种均呈现出与气候适应相关的共有基因组特征（例如抗干旱性、应激响应），表明二者存在趋同的生理进化响应。与宿主-寄生虫互作相关的基因（如机械感知基因、昼夜节律基因、毒液基因）同样呈现平行选择信号。
诸如攻击行为等行为性状的基因组选择信号较为有限，但却可能具备更高的转录可塑性（transcriptional plasticity）。与化学性状相关的关联分析显示，两类物种在表皮碳氢化合物生物合成及化学感知相关基因上受到共同选择，这表明信号产生与信号感知存在进化耦合关系。
组成型基因表达模式则呈现分化：宿主的基因表达与寄生虫感染率显著相关，而寄生虫的基因表达则更多与气候因素紧密关联，这反映出二者受到截然不同的调控压力。
本研究阐明了不同的种群结构、不对称的互惠选择以及环境背景如何塑造协同适应的差异化基因组进化轨迹，反映出异质景观下截然不同的进化架构。