Several parasite species have the ability to modify their host's phenotype to their own advantage thereby increasing the probability of transmission from one host to another. This phenomenon of host manipulation is interpreted as the expression of a parasite extended phenotype. Manipulative parasites generally affect multiple phenotypic traits in their hosts, although both the extent and adaptive significance of such multidimensionality in host manipulation is still poorly documented. To review the multidimensionality and magnitude of host manipulation, and to understand the causes of variation in trait value alteration, we performed a phylogenetically corrected meta‐analysis, focusing on a model taxon: acanthocephalan parasites. Acanthocephala is a phylum of helminth parasites that use vertebrates as final hosts and invertebrates as intermediate hosts, and is one of the few parasite groups for which manipulation is predicted to be ancestral. We compiled 279 estimates of parasite‐induced alterations in phenotypic trait value, from 81 studies and 13 acanthocephalan species, allocating a sign to effect size estimates according to the direction of alteration favouring parasite transmission, and grouped traits by category. Phylogenetic inertia accounted for a low proportion of variation in effect sizes. The overall average alteration of trait value was moderate and positive when considering the expected effect of alterations on trophic transmission success (signed effect sizes, after the onset of parasite infectivity to the final host). Variation in the alteration of trait value was affected by the category of phenotypic trait, with the largest alterations being reversed taxis/phobia and responses to stimuli, and increased vulnerability to predation, changes to reproductive traits (behavioural or physiological castration) and immunosuppression. Parasite transmission would thereby be facilitated mainly by changing mainly the choice of micro‐habitat and the anti‐predation behaviour of infected hosts, and by promoting energy‐saving strategies in the host. In addition, infection with larval stages not yet infective to definitive hosts (acanthella) tends to induce opposite effects of comparable magnitude to infection with the infective stage (cystacanth), although this result should be considered with caution due to the low number of estimates with acanthella. This analysis raises important issues that should be considered in future studies investigating the adaptive significance of host manipulation, not only in acanthocephalans but also in other taxa. Specifically, the contribution of phenotypic traits to parasite transmission and the range of taxonomic diversity covered deserve thorough attention. In addition, the relationship between behaviour and immunity across parasite developmental stages and host–parasite systems (the neuropsychoimmune hypothesis of host manipulation), still awaits experimental evidence. Most of these issues apply more broadly to reported cases of host manipulation by other groups of parasites.

中文翻译：

---

寄生虫引起的表型改变的幅度和方向：棘头动物的荟萃分析

几种寄生虫物种有能力根据自己的优势修改宿主的表型，从而增加从一个宿主传播到另一个宿主的可能性。这种宿主操纵现象被解释为寄生虫扩展表型的表达。操纵性寄生虫通常会影响其宿主的多种表型特征，尽管这种多维性在宿主操纵中的程度和适应性意义仍然没有得到很好的记录。为了回顾宿主操纵的多维性和幅度，并了解性状值变化的原因，我们进行了系统发育校正的荟萃分析，重点关注模型分类群：棘头虫寄生虫。棘头虫是一种蠕虫寄生虫门，以脊椎动物为最终宿主，无脊椎动物为中间宿主，并且是为数不多的被预测为祖先的寄生虫群之一。我们从 81 项研究和 13 种棘头动物物种中汇编了 279 项寄生虫引起的表型性状改变的估计值，根据有利于寄生虫传播的改变方向分配一个符号来估计影响大小，并按类别对性状进行分组。系统发育惯性占效应大小变化的比例很小。考虑到改变对营养传播成功的预期影响（有符号的影响大小，在寄生虫感染最终宿主后）时，性状值的总体平均改变是中等和积极的。性状值变化的变化受表型性状类别的影响，最大的变化是反向出租车/恐惧症和对刺激的反应，以及对捕食的脆弱性增加，生殖性状的变化（行为或生理阉割）和免疫抑制。因此，寄生虫传播将主要通过改变微生境的选择和受感染宿主的反捕食行为以及促进宿主的节能策略来促进。此外，尚未感染终宿主（棘轮）的幼虫阶段的感染往往会引起与感染阶段（囊棘）感染相当程度的相反影响，尽管由于估计数量较少，因此应谨慎考虑这一结果。棘轮藻。该分析提出了在未来研究中应考虑的重要问题，研究宿主操纵的适应性意义，不仅在棘头动物中，而且在其他分类群中。具体而言，表型性状对寄生虫传播的贡献以及所涵盖的分类多样性范围值得彻底关注。此外，寄生虫发育阶段和宿主 - 寄生虫系统（宿主操纵的神经心理免疫假说）之间的行为和免疫之间的关系仍在等待实验证据。大多数这些问题更广泛地适用于报告的其他寄生虫群体操纵宿主的案例。表型性状对寄生虫传播的贡献以及所涵盖的分类多样性范围值得彻底关注。此外，寄生虫发育阶段和宿主 - 寄生虫系统（宿主操纵的神经心理免疫假说）之间的行为和免疫之间的关系仍在等待实验证据。大多数这些问题更广泛地适用于报告的其他寄生虫群体操纵宿主的案例。表型性状对寄生虫传播的贡献以及所涵盖的分类多样性范围值得彻底关注。此外，寄生虫发育阶段和宿主 - 寄生虫系统（宿主操纵的神经心理免疫假说）之间的行为和免疫之间的关系仍在等待实验证据。大多数这些问题更广泛地适用于报告的其他寄生虫群体操纵宿主的案例。