Data from: Patterns, causes, and consequences of defensive microbiome dynamics across multiple scales

The microbiome can significantly impact host phenotypes and serve as an additional source of heritable genetic variation. While patterns across eukaryotes are consistent with a role for symbiotic microbes in host macroevolution, few studies have examined symbiont-driven host evolution or the ecological implications of a dynamic microbiome across temporal, spatial, or ecological scales. The pea aphid, Acyrthosiphon pisum, and its eight heritable bacterial endosymbionts have served as a model for studies on symbiosis and its potential contributions to host ecology and evolution. But we know little about the natural dynamics or ecological impacts of the heritable microbiome of this cosmopolitan insect pest. Here we report seasonal shifts in the frequencies of heritable defensive bacteria from natural pea aphid populations across two host races and geographic regions. Microbiome dynamics were consistent with symbiont responses to host-level selection and findings from one population suggested symbiont-driven adaptation to seasonally changing parasitoid pressures. Conversely, symbiont levels seemed to influence enemy success when measured across host races, revealing ecological impacts of microbiome divergence. Rapid drops in symbiont frequencies following seasonal peaks suggest microbiome instability in several populations, with potentially large costs of “superinfection” under certain environmental conditions. In summary, the realization of several lab-derived, a priori expectations suggests important natural impacts of defensive symbionts in host-enemy eco-evolutionary feedbacks. Yet both negative findings and unanticipated correlations suggest complexities within this system may limit or obscure symbiont-driven contemporary evolution, a finding of broad significance given the widespread nature of defensive microbes across plants and animals.

微生物组（microbiome）可显著影响宿主表型，并可作为可遗传变异的额外来源。尽管真核生物中的相关模式与共生微生物在宿主宏观进化中的作用相符，但鲜有研究探讨共生体驱动的宿主进化，或动态微生物组在时间、空间及生态尺度上的生态学意义。豌豆蚜（Acyrthosiphon pisum）及其8种可遗传细菌内共生体（endosymbionts）已成为共生关系及其对宿主生态与进化潜在贡献研究的模式系统。但对于这种广布性昆虫害虫的可遗传微生物组的自然动态及其生态学影响，我们仍知之甚少。本研究报道了来自两个宿主生物型及不同地理区域的自然豌豆蚜种群中，可遗传防御细菌的频率季节性变化。微生物组动态与共生体对宿主水平选择的响应一致，且来自某一种群的研究结果表明，共生体驱动宿主适应了季节性变化的寄生性天敌（parasitoid）压力。反之，跨宿主生物型测定时发现，共生体水平似乎会影响天敌的侵染成功率，这揭示了微生物组分化的生态学影响。季节性峰值后共生体频率的快速下降表明多个种群的微生物组存在不稳定性，且在特定环境条件下超感染（superinfection）可能带来巨大代价。综上，多项实验室先验预期得到验证的结果表明，防御型共生体在宿主-天敌的生态进化反馈环中发挥着重要的自然作用。然而，阴性结果与未预期的相关性均表明，该系统内的复杂性可能限制或掩盖了共生体驱动的当代进化；考虑到防御微生物在动植物中广泛分布，这一发现具有广泛的研究意义。