Data from: Specificity of multi-modal aphid defenses against two rival parasitoids

Insects are often attacked by multiple natural enemies, imposing dynamic selective pressures for the development and maintenance of enemy-specific resistance. Pea aphids (Acyrthosiphon pisum) have emerged as models for the study of variation in resistance against natural enemies, including parasitoid wasps. Internal defenses against their most common parasitoid wasp, Aphidius ervi, are sourced through two known mechanisms– 1) endogenously encoded resistance or 2) infection with the heritable bacterial symbiont, Hamiltonella defensa. Levels of resistance can range from nearly 0–100% against A. ervi but varies based on aphid genotype and the strain of toxin-encoding bacteriophage (called APSE) carried by Hamiltonella. Previously, other parasitoid wasps were found to commonly attack this host, but North American introductions of A. ervi have apparently displaced all other parasitoids except Praon pequodorum, a related aphidiine braconid wasp, which is still found attacking this host in natural populations. To explain P. pequodorum’s persistence, multiple studies have compared direct competition between both wasps, but have not examined specificity of host defenses as an indirectly mediating factor. Using an array of experimental aphid lines, we first examined whether aphid defenses varied in effectiveness toward either wasp species. Expectedly, both types of aphid defenses were effective against A. ervi, but unexpectedly, were completely ineffective against P. pequodorum. Further examination showed that P. pequodorum wasps suffered no consistent fitness costs from developing in even highly ‘resistant’ aphids. Comparison of both wasps’ egg-larval development revealed that P. pequodorum’s eggs have thicker chorions and hatch two days later than A. ervi’s, likely explaining their differing abilities to overcome aphid defenses. Overall, our results indicate that aphids resistant to A. ervi may serve as reservoirs for P. pequodorum, hence contributing to its persistence in field populations. We find that specificity of host defenses and defensive symbiont infections, may have important roles in influencing enemy compositions by indirectly mediating the interactions and abundance of rival natural enemies.

昆虫常遭受多种天敌的侵袭，这为宿主演化并维持针对特定天敌的抗性带来了动态的选择压力。豌豆蚜（Acyrthosiphon pisum）已成为研究宿主针对包括寄生蜂在内的天敌的抗性变异的经典模式生物。其针对最常见寄生蜂——艾氏蚜茧蜂（Aphidius ervi）的体内防御，已知通过两种机制实现：1）内源编码抗性；2）感染可遗传的细菌共生体哈氏汉密尔顿菌（Hamiltonella defensa）。针对艾氏蚜茧蜂的抗性水平可介于近乎0%至100%之间，其差异取决于豌豆蚜的基因型以及哈氏汉密尔顿菌所携带的编码毒素的噬菌体（简称APSE）的毒株。

此前已有研究发现，多种其他寄生蜂常会侵染该宿主，但北美地区引入的艾氏蚜茧蜂已几乎取代了所有其他寄生蜂类群，仅存相关的茧蜂科蚜茧蜂亚科宽痣蚜茧蜂属的佩夸多宽痣蚜茧蜂（Praon pequodorum），目前仍在自然种群中侵染该宿主。为阐释佩夸多宽痣蚜茧蜂的种群存续机制，已有多项研究对比了两种寄生蜂的直接竞争关系，但尚未探究宿主防御特异性作为间接介导因子的作用。

本研究利用一系列实验豌豆蚜品系，首先探究了豌豆蚜的防御能力对两种寄生蜂是否存在有效性差异。正如预期，豌豆蚜的两种防御机制均对艾氏蚜茧蜂有效，但出乎意料的是，其对佩夸多宽痣蚜茧蜂完全无效。进一步检测发现，即便在高度“抗性”的豌豆蚜体内发育，佩夸多宽痣蚜茧蜂也未出现一致的适合度代价。对比两种寄生蜂的卵至幼虫发育过程发现，佩夸多宽痣蚜茧蜂的卵具有更厚的卵壳，且孵化时间较艾氏蚜茧蜂晚两天，这或可解释二者对抗豌豆蚜防御能力的差异。

综上，本研究结果表明，对艾氏蚜茧蜂具有抗性的豌豆蚜或可成为佩夸多宽痣蚜茧蜂的寄主库，进而助力其在野外种群中存续。本研究发现，宿主防御特异性与防御性共生体感染，可通过间接介导竞争性天敌的相互作用与种群丰度，在调控天敌群落组成方面发挥重要作用。