Department of Entomology, University of Georgia, Georgia, Athens, USA.
Mol Ecol. 2023 Feb;32(4):936-950. doi: 10.1111/mec.16801. Epub 2022 Dec 20.
Insects often harbour heritable symbionts that provide defence against specialized natural enemies, yet little is known about symbiont protection when hosts face simultaneous threats. In pea aphids (Acyrthosiphon pisum), the facultative endosymbiont Hamiltonella defensa confers protection against the parasitoid, Aphidius ervi, and Regiella insecticola protects against aphid-specific fungal pathogens, including Pandora neoaphidis. Here, we investigated whether these two common aphid symbionts protect against a specialized virus A. pisum virus (APV), and whether their antifungal and antiparasitoid services are impacted by APV infection. We found that APV imposed large fitness costs on symbiont-free aphids and these costs were elevated in aphids also housing H. defensa. In contrast, APV titres were significantly reduced and costs to APV infection were largely eliminated in aphids with R. insecticola. To our knowledge, R. insecticola is the first aphid symbiont shown to protect against a viral pathogen, and only the second arthropod symbiont reported to do so. In contrast, APV infection did not impact the protective services of either R. insecticola or H. defensa. To better understand APV biology, we produced five genomes and examined transmission routes. We found that moderate rates of vertical transmission, combined with horizontal transfer through food plants, were the major route of APV spread, although lateral transfer by parasitoids also occurred. Transmission was unaffected by facultative symbionts. In summary, the presence and species identity of facultative symbionts resulted in highly divergent outcomes for aphids infected with APV, while not impacting defensive services that target other enemies. These findings add to the diverse phenotypes conferred by aphid symbionts, and to the growing body of work highlighting extensive variation in symbiont-mediated interactions.
昆虫通常携带可遗传的共生体，为其提供针对专门化的自然天敌的防御，但当宿主面临同时存在的威胁时，共生体保护的情况却鲜为人知。在豌豆蚜（Acyrthosiphon pisum）中，兼性内共生菌 Hamiltonella defensa 可提供针对寄生蜂 Aphis ervi 的保护，而 Regiella insecticola 则可保护蚜虫免受特定的真菌病原体的侵害，包括 Pandora neoaphidis。在这里，我们研究了这两种常见的蚜虫共生体是否能抵御专门的病毒 A. pisum virus (APV)，以及它们的抗真菌和抗寄生蜂服务是否会受到 APV 感染的影响。我们发现，APV 给无共生体的蚜虫带来了巨大的适应代价，而在同时拥有 H. defensa 的蚜虫中，这种代价会更高。相比之下，APV 的滴度显著降低，而 R. insecticola 的蚜虫感染 APV 的代价则基本消除。据我们所知，R. insecticola 是第一个被证明能抵御病毒病原体的蚜虫共生体，也是第二个被报道具有这种能力的节肢动物共生体。相比之下，APV 感染并没有影响 R. insecticola 或 H. defensa 的保护服务。为了更好地了解 APV 的生物学特性，我们生成了五个基因组并研究了传播途径。我们发现，垂直传播的适度速率，再加上通过食物植物的水平转移，是 APV 传播的主要途径，尽管寄生蜂也会发生横向转移。共生体的存在与否对传播没有影响。综上所述，兼性共生体的存在和物种身份导致感染 APV 的蚜虫出现了高度不同的结果，而对针对其他敌人的防御服务没有影响。这些发现增加了蚜虫共生体赋予的多样化表型，并增加了越来越多的强调共生体介导的相互作用广泛变化的工作。
