Department of BioSciences, Rice University, Houston, Texas 77005.
Scripps Institution of Oceanography, University of California San Diego, La Jolla, California 92037.
J Parasitol. 2023 Jul 1;109(4):362-376. doi: 10.1645/23-35.
Some parasites manipulate their host's phenotype to enhance predation rates by the next host in the parasite's life cycle. Our understanding of this parasite-increased trophic transmission is often stymied by study-design challenges. A recurring difficulty has been obtaining uninfected hosts with a coevolutionary history with the parasites, and conducting experimental infections that mimic natural processes. In 1996, Lafferty and Morris provided what has become a classic example of parasite-increased trophic transmission; they reported a positive association between the intensity of a brain-infecting trematode (Euhaplorchis californiensis) in naturally infected California killifish (Fundulus parvipinnis) and the frequency of conspicuous behaviors, which was thought to explain the documented 10-30× increase in predation by the final host birds. Here, we address the primary gap in that study by using experimental infections to assess the causality of E. californiensis infection for increased conspicuous behaviors in F. parvipinnis. We hatched and reared uninfected F. parvipinnis from a population co-occurring with E. californiensis, and infected them 1-2 times/week over half their life span with E. californiensis and a small cyathocotylid trematode (SMCY) that targets the host's muscle tissue. At 3 time points throughout the hosts' lives, we quantified several conspicuous behaviors: contorting, darting, scratching, surfacing, and vertical positioning relative to the water's surface. Euhaplorchis californiensis and SMCY infection caused 1.8- and 2.5-fold overall increases in conspicuous behaviors, respectively. Each parasite was also associated with increases in specific conspicuous behaviors, particularly 1.9- and 1.4-fold more darting. These experimental findings help solidify E. californiensis-F. parvipinnis as a classic example of behavioral manipulation. Yet our findings for E. californiensis infection-induced behavioral change were less consistent and strong than those previously documented. We discuss potential explanations for this discrepancy, particularly the idea that behavioral manipulation may be most apparent when fish are actively attacked by predators. Our findings concerning the other studied trematode species, SMCY, highlight that trophically transmitted parasites infecting various host tissues are known to be associated with conspicuous behaviors, reinforcing calls for research examining how communities of trophically transmitted parasites influence host behavior.
一些寄生虫会操纵宿主的表型，以提高其在寄生虫生命周期中的下一宿主的捕食率。我们对这种寄生虫增强营养传播的理解常常受到研究设计挑战的阻碍。一个反复出现的困难是获得与寄生虫具有共同进化历史的未感染宿主，并进行模拟自然过程的实验感染。1996 年，拉弗蒂和莫里斯提供了一个寄生虫增强营养传播的经典例子；他们报告说，在自然感染加利福尼亚食肝吸虫（Euhaplorchis californiensis）的加利福尼亚小鲈（Fundulus parvipinnis）中，这种脑寄生虫的感染强度与明显行为的频率之间存在正相关，这被认为解释了记录到的最终宿主鸟类捕食率提高了 10-30 倍的现象。在这里，我们通过使用实验感染来评估 E. californiensis 感染对 F. parvipinnis 明显行为增加的因果关系，从而解决了该研究中的主要差距。我们从与 E. californiensis 共同出现的种群中孵化和饲养未感染的 F. parvipinnis，并在其一半的寿命内每周感染 1-2 次 E. californiensis 和一种针对宿主肌肉组织的小型 cyathocotylid 吸虫（SMCY）。在宿主生命的三个时间点，我们量化了几种明显的行为：扭曲、猛冲、抓挠、浮出水面和相对于水面的垂直定位。Euhaplorchis californiensis 和 SMCY 感染分别导致明显行为总体增加 1.8 倍和 2.5 倍。每种寄生虫也与特定明显行为的增加有关，特别是猛冲增加了 1.9-1.4 倍。这些实验结果有助于巩固 E. californiensis-F. parvipinnis 作为行为操纵的经典范例。然而，我们发现 E. californiensis 感染引起的行为变化不如以前记录的那么一致和强烈。我们讨论了这种差异的潜在解释，特别是行为操纵可能在鱼类受到捕食者积极攻击时最为明显的观点。我们关于另一种研究的吸虫物种 SMCY 的发现，强调了感染各种宿主组织的营养传播寄生虫与明显行为有关，这进一步呼吁研究检查营养传播寄生虫群落如何影响宿主行为。
