Contrasting Infection Strategies in Generalist and Specialist Wasp Parasitoids of Drosophila melanogaster

Although host–parasitoid interactions are becoming well characterized at the organismal and cellular levels, much remains to be understood of the molecular bases for the host immune response and the parasitoids' ability to defeat this immune response. Leptopilina boulardi and L. heterotoma, two closely related, highly infectious natural parasitoids of Drosophila melanogaster, appear to use very different infection strategies at the cellular level. Here, we further characterize cellular level differences in the infection characteristics of these two wasp species using newly derived, virulent inbred strains, and then use whole genome microarrays to compare the transcriptional response of Drosophila to each. While flies attacked by the melanogaster group specialist L. boulardi (strain Lb17) up-regulate numerous genes encoding proteolytic enzymes, components of the Toll and JAK/STAT pathways, and the melanization cascade as part of a combined cellular and humoral innate immune response, flies attacked by the generalist L. heterotoma (strain Lh14) do not appear to initiate an immune transcriptional response at the time points post-infection we assayed, perhaps due to the rapid venom-mediated lysis of host hemocytes (blood cells). Thus, the specialist parasitoid appears to invoke a full-blown immune response in the host, but suppresses and/or evades downstream components of this response. Given that activation of the host immune response likely depletes the energetic resources of the host, the specialist's infection strategy seems relatively disadvantageous. However, we uncover the mechanism for one potentially important fitness tradeoff of the generalist's highly immune suppressive infection strategy.

尽管宿主-寄生蜂互作（host–parasitoid interactions）在个体与细胞水平已得到较为充分的表征，但宿主免疫应答以及寄生蜂对抗该免疫应答的能力的分子基础仍有诸多亟待阐明之处。布氏潜蝇茧蜂（Leptopilina boulardi）与异足潜蝇茧蜂（L. heterotoma）是两种近缘、对黑腹果蝇（Drosophila melanogaster）具有高侵染性的天然寄生蜂，二者在细胞水平展现出截然不同的侵染策略。本研究借助新构建的强毒近交株系，进一步表征了这两种蜂的侵染特性在细胞水平的差异；随后利用全基因组芯片（whole genome microarrays），比较了黑腹果蝇对每种寄生蜂的转录应答（transcriptional response）。研究发现，被专性寄生黑腹果蝇类群的L. boulardi（菌株Lb17）侵染的果蝇，会上调大量编码蛋白水解酶（proteolytic enzymes）、Toll通路与JAK/STAT通路组分以及黑化级联（melanization cascade）的基因，作为细胞与体液先天免疫应答的组成部分；而被泛化型寄生蜂L. heterotoma（菌株Lh14）侵染的果蝇，在本研究检测的侵染后时间点中，似乎并未启动免疫相关的转录应答，这可能源于其血细胞（hemocytes，宿主免疫细胞）被寄生蜂毒液快速介导裂解。综上，特化型寄生蜂似乎会触发宿主全面的免疫应答，但又会抑制或逃逸该应答的下游组分。鉴于宿主免疫应答的激活大概率会消耗宿主的能量资源，特化型的侵染策略似乎相对不利。不过，本研究揭示了泛化型这种高度免疫抑制的侵染策略所存在的一种潜在重要的适合度权衡（fitness tradeoff）机制。