Studying the costs and benefits of host-parasite interactions is of central importance to shed light on the evolutionary drivers of host life history traits. Although gregarines (Apicomplexa: Sporozoa) are one of the most frequent parasites in the gut of invertebrates, the diversity of its potential impacts on a host remains poorly explored. In this study, we addressed this gap in knowledge by investigating the prevalence of natural infections by the gregarine Gregarina ovata and testing how these infections shape a large set of morphological, behavioural and physiological traits in the European earwig Forficula auricularia. Our results first show that G. ovata was present in 76.8% of 573 field-sampled earwigs, and that its prevalence was both higher in males compared with females and increased between July and September. The load of G. ovata in the infected individuals was higher in males than females, but this sex difference vanished during the season. Our experiments then surprisingly revealed apparent benefits of G. ovata infections. Food-deprived hosts survived longer when they exhibited high compared with low gregarine loads. Moreover, the presence of gregarines was associated with a reduced phenoloxidase activity, indicating a lower immune resistance or a higher immune tolerance of the infected hosts. By contrast, we found no effect of G. ovata presence and number on earwigs’ development (eye distance, forceps length), activity, food consumption or resistance against a fungal pathogen. Overall, our findings suggest that G. ovata could be involved in a mutualistic relationship with the European earwig. Given the ubiquitous presence of gregarines among invertebrates, our data also suggest that this common member of insect gut flora could have a broad and positive role in the life history of many host species.

研究宿主-寄生虫相互作用的成本和收益对于阐明宿主生活史特征的进化驱动因素至关重要。尽管 gregarines (Apicomplexa: Sporozoa) 是无脊椎动物肠道中最常见的寄生虫之一，但其对宿主的潜在影响的多样性仍未得到很好的探索。在这项研究中，我们通过调查 gregarine Gregarina ovata自然感染的流行率并测试这些感染如何塑造欧洲耳螟Forficula auricularia的大量形态、行为和生理特征，从而弥补了这一知识差距。我们的结果首先表明G. ovata在 573 只实地采样的耳螟中，有 76.8% 存在这种病毒，而且雄性与雌性之间的流行率均高于雌性，并且在 7 月和 9 月之间有所增加。受感染个体中G. ovata的负荷在雄性中高于雌性，但这种性别差异在该季节消失了。我们的实验随后出人意料地揭示了G. ovata感染的明显益处。与低杂草负荷相比，缺乏食物的宿主在高负荷时存活时间更长。此外，gregarines 的存在与酚氧化酶活性降低有关，表明受感染宿主的免疫抵抗力较低或免疫耐受性较高。相比之下，我们发现G. ovata没有影响假耳发育（眼距、镊子长度）、活动、食物消耗或对真菌病原体的抵抗力的存在和数量。总的来说，我们的研究结果表明G. ovata可能与欧洲螟有共生关系。鉴于无脊椎动物中普遍存在的群居动物，我们的数据还表明，昆虫肠道菌群的这一常见成员在许多宿主物种的生活史中可能具有广泛而积极的作用。