Departments of Entomology and Biology, Penn State University, PA 16802, USA.
BMC Ecol. 2011 May 9;11:13. doi: 10.1186/1472-6785-11-13.
Parasites that manipulate host behavior can provide prominent examples of extended phenotypes: parasite genomes controlling host behavior. Here we focus on one of the most dramatic examples of behavioral manipulation, the death grip of ants infected by Ophiocordyceps fungi. We studied the interaction between O. unilateralis s.l. and its host ant Camponotus leonardi in a Thai rainforest, where infected ants descend from their canopy nests down to understory vegetation to bite into abaxial leaf veins before dying. Host mortality is concentrated in patches (graveyards) where ants die on sapling leaves ca. 25 cm above the soil surface where conditions for parasite development are optimal. Here we address whether the sequence of ant behaviors leading to the final death grip can also be interpreted as parasite adaptations and describe some of the morphological changes inside the heads of infected workers that mediate the expression of the death grip phenotype.
We found that infected ants behave as zombies and display predictable stereotypical behaviors of random rather than directional walking, and of repeated convulsions that make them fall down and thus precludes returning to the canopy. Transitions from erratic wandering to death grips on a leaf vein were abrupt and synchronized around solar noon. We show that the mandibles of ants penetrate deeply into vein tissue and that this is accompanied by extensive atrophy of the mandibular muscles. This lock-jaw means the ant will remain attached to the leaf after death. We further present histological data to show that a high density of single celled stages of the parasite within the head capsule of dying ants are likely to be responsible for this muscular atrophy.
Extended phenotypes in ants induced by fungal infections are a complex example of behavioral manipulation requiring coordinated changes of host behavior and morphology. Future work should address the genetic basis of such extended phenotypes.
能够操纵宿主行为的寄生虫可以提供显著的延伸表型的例子：寄生虫基因组控制宿主行为。在这里，我们关注行为操纵最显著的例子之一，即被蕈蚊属真菌感染的蚂蚁的死亡握力。我们在泰国雨林中研究了 Ophiocordyceps unilateralis s.l.与其宿主蚂蚁 Camponotus leonardi 之间的相互作用，在那里，受感染的蚂蚁从树冠巢下降到林下植被，在死亡前咬住背面叶脉。宿主死亡率集中在斑块（墓地）中，蚂蚁在离地面约 25 厘米高的幼树苗叶上死亡，那里是寄生虫发育的最佳条件。在这里，我们探讨了导致最终死亡握力的蚂蚁行为序列是否也可以被解释为寄生虫的适应，并描述了一些感染工蚁头部内介导死亡握力表型表达的形态变化。
我们发现感染的蚂蚁表现为僵尸，表现出随机而非定向行走的可预测刻板行为，以及反复抽搐，使它们倒下，从而阻止它们返回树冠。从不稳定的游荡到死亡握力的转变是突然的，并在中午时分同步发生。我们表明，蚂蚁的下颚深入到叶脉组织中，并且下颚肌肉广泛萎缩。这种锁定下颚意味着蚂蚁死后将仍然附着在叶子上。我们进一步提供组织学数据表明，在死亡蚂蚁的头壳内，寄生虫的单细胞阶段密度很高，可能是导致这种肌肉萎缩的原因。
真菌感染诱导的蚂蚁延伸表型是行为操纵的一个复杂例子，需要宿主行为和形态的协调变化。未来的工作应该解决这种延伸表型的遗传基础。
