Date from: Top-down effects from parasitoids may mediate plant defense and plant fitness

Plants face many environmental stresses that can impact their survival,
development, and fitness. Insects are the most diverse, abundant and
threatening herbivores in nature. As a consequence, plants produce direct
chemical and physical defenses to reduce herbivory. They also release
volatiles to recruit natural enemies that indirectly protect them from
herbivory. The recruitment of parasitic wasps can benefit plant fitness
because they ultimately kill their insect hosts. Recently, studies showed
that parasitoids can indirectly mediate plant defenses by modulating
herbivore oral secretions. In addition to the direct benefits of
parasitoids in terms of reducing herbivore survival, we tested if the
reduction in induced defenses by parasitized caterpillars compared to
non-parasitized caterpillars may reduce the costs associated with defense
expression. We provide evidence that tomato plants treated with saliva
from parasitized caterpillars have significantly higher fitness parameters
including increased flower numbers (16.3%) and heavier fruit weight (15%),
compared to plants treated with saliva from non-parasitized caterpillars.
Since plants were grown without actual herbivores, the higher values for
these fitness parameters were due to lower costs of induced defenses and
not due to reduced herbivory by parasitized caterpillars. Furthermore, the
resulting seed germination time was shorter and the germination rate was
higher when the maternal plants were previously exposed to parasitized
herbivore treatment compared to control (non-treated) plants. Overall,
application of saliva did not result in transgenerational priming of
offspring defense responses. However, offspring of parents exposed to
caterpillar saliva had lower constitutive levels and higher induced levels
of trypsin inhibitor than offspring from unexposed parents. This study
shows that the saliva of parasitized caterpillars can modulate plant
defenses and further demonstrates that the lower induction of plant
defenses is associated with elevated plant fitness in the absence of
herbivore feeding, suggesting that induced plant defenses are
costly.

植物面临诸多可影响其存活、生长发育与适合度（fitness）的环境胁迫。昆虫是自然界中多样性最高、丰度最大且威胁性最强的植食性昆虫（herbivores）。为此，植物演化出直接化学防御与物理防御以降低植食危害；同时还会释放挥发性物质，招募天敌来间接保护自身免受植食危害。寄生蜂（parasitic wasps）可通过杀死寄主昆虫，最终提升植物适合度。近期研究表明，寄生性天敌（parasitoids）可通过调控植食性昆虫的口分泌液，间接介导植物防御反应。除寄生性天敌通过降低植食昆虫存活率带来的直接益处外，本研究还检验了如下问题：相较于未被寄生的毛虫（caterpillars），被寄生毛虫所诱导的植物防御水平更低，这是否能够降低防御表达的相关成本。我们提供的研究证据显示：与用未被寄生毛虫唾液处理的番茄植株相比，经被寄生毛虫唾液处理的番茄植株，其适合度指标显著更高——开花数提升16.3%，单果重量增加15%。由于实验中番茄植株未受到实际植食性昆虫取食，上述适合度指标的提升源于防御诱导成本的降低，而非被寄生毛虫的植食危害减少。此外，相较于未处理的对照组，当母代植株此前暴露于被寄生植食昆虫处理组时，其子代的种子萌发时间更短、萌发率更高。总体而言，唾液处理并未引发后代防御反应的跨代预激发（transgenerational priming）。不过，相较于未暴露于毛虫唾液的亲本后代，暴露于毛虫唾液的亲本后代，其胰蛋白酶抑制剂（trypsin inhibitor）的组成型表达水平更低，而诱导型表达水平更高。本研究证实，被寄生毛虫的唾液可调控植物防御反应，并进一步表明：在无植食性昆虫取食的情境下，植物防御的较低诱导水平与更高的植株适合度呈正相关，这也提示诱导型植物防御是存在成本的。