Data from: Can social partnerships influence the microbiome? insights from ant farmers and their trophobiont mutualists.

Mutualistic interactions with microbes have played a crucial role in the evolution and ecology of animal hosts. However, it is unclear what factors are most important in influencing particular host-microbe associations. While closely related animal species may have more similar microbiota than distantly related ones due to phylogenetic contingencies, social partnerships with other organisms, such as those in which one animal farms another, may also influence an organism’s symbiotic microbiome. We studied a mutualistic network of Brachymyrmex and Lasius ants farming several honeydew-producing Prociphilus aphids and Rhizoecus mealybugs to test whether the mutualistic microbiomes of these interacting insects are primarily correlated with their phylogeny or with their shared social partnerships. Our results confirm a phylogenetic signal in the microbiomes of aphid and mealybug trophobionts, with each species harboring species-specific endosymbiont strains of Buchnera (aphids), Tremblaya and Sodalis (mealybugs), and Serratia (both mealybugs and aphids) despite being farmed by the same ants. This is likely explained by strict vertical transmission of trophobiont endosymbionts between generations. In contrast, the ants’ microbiome is potentially shaped by their social partnerships, with ants that farm the same trophobionts also sharing strains of sugar-processing Acetobacteraceae bacteria, known from other honeydew-feeding ants and which likely reside extracellularly in the ants’ guts. These ant-microbe associations are arguably more ‘open’ and subject to horizontal transmission or social transmission within ant colonies. These findings suggest that the role of social partnerships in shaping a host’s symbiotic microbiome can be variable, and is likely dependent on how the microbes are transmitted across generations.

微生物与宿主的共生相互作用，在动物宿主的演化与生态过程中发挥了至关重要的作用。然而，目前尚不清楚哪些因素对特定宿主-微生物共生关联的影响最为关键。尽管由于系统发育偶然性，亲缘关系较近的动物物种的微生物群相较于远缘物种更为相似，但与其他生物的社会伙伴关系——例如一方驯养另一方的共生关系——同样可能影响宿主的共生微生物组。我们以短尾蚁属（Brachymyrmex）和毛蚁属（Lasius）的蚂蚁为研究对象，它们驯养了多种产蜜露的西圆尾蚜属（Prociphilus）蚜虫和粉蚧属（Rhizoecus）粉蚧，借此构建共生研究网络，旨在探究这些相互作用昆虫的共生微生物组主要与其系统发育相关，还是与其共有的社会伙伴关系相关。研究结果证实，蚜虫与粉蚧的营养共生体微生物组存在系统发育信号：尽管这些共生体均由同一批蚂蚁驯养，但每个物种均携带有物种特异性的内共生菌株，其中蚜虫的内共生菌为布赫纳氏菌属（Buchnera），粉蚧的为特雷布莱亚菌属（Tremblaya）和索氏菌属（Sodalis），而沙雷氏菌属（Serratia）则同时存在于粉蚧与蚜虫体内。这一现象很可能是由营养共生体内共生菌在代际间的严格垂直传播所导致的。与之相反，蚂蚁的微生物组则可能由其社会伙伴关系塑造：驯养同一类营养共生体的蚂蚁，会共享一类参与糖代谢的醋杆菌科（Acetobacteraceae）菌株——这类细菌已在其他取食蜜露的蚂蚁中被发现，且大概率以胞外形式存在于蚂蚁的肠道中。可以说，这些蚂蚁-微生物共生关联更为“开放”，易发生水平传播或蚁群内的社会传播。上述研究结果表明，社会伙伴关系在塑造宿主共生微生物组过程中所发挥的作用并非固定不变，而是很可能取决于微生物在代际间的传播方式。