Thermal ecology in a parasitoid attacking an adult life stage host: Recovery, sex effects and hidden costs of warming

IF 5.1 1区 环境科学与生态学 Q1 ECOLOGY
Functional Ecology Pub Date : 2026-03-31 Epub Date: 2026-03-04 DOI:10.1111/1365-2435.70286
Katherine H. Malinski
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However, most of this literature examines agriculturally relevant host–parasitoid systems, for example parasitoids of aphid or larval Lepidopteran hosts, and immature host life stages, for example egg, larva or nymph (Malinski et al., <span>2024</span>). Because host life stages differ in mobility, sex, reproduction and other biological aspects, it is important to understand how climate change impacts host–parasitoid dynamics in parasitoids of different host life stages. The 2025 study by Baudino and colleagues (Baudino et al., <span>2025</span>) brings much needed attention to the understudied system of adult host stage parasitism.</p><p>Baudino et al. (<span>2025</span>) examined the ecological outcomes of a host–parasitoid interaction between the braconid parasitoid wasp <i>Dinocampus coccinellae</i> and the invasive harlequin ladybird beetle <i>Harmonia axyridis</i> host across low (18°C), optimal (24°C) and high (30°C) temperatures. In this host–parasitoid system, <i>D. coccinellae</i> attacks adult hosts and uses a symbiotic RNA virus (<i>D. coccinellae</i> paralysis virus, DcPV) to induce temporary host paralysis prior to parasitoid emergence (Dheilly et al., <span>2015</span>; Maure et al., <span>2011</span>). After parasitoids complete development, some hosts recover normal feeding and reproductive behaviour, making host recovery a central life-history trait in this system. Host recovery is rare in host–parasitoid systems and therefore understudied: most existing reports are observational and seldom quantitative. By explicitly quantifying host recovery alongside other host and parasitoid fitness components, Baudino et al. (<span>2025</span>) add nuance and novelty to our understanding of host–parasitoid interactions and thermal ecology.</p><p>Consistent with patterns observed in most parasitoids, the authors found that elevated temperature proved detrimental to parasitoid success. While parasitoids frequently completed development at 18°C and, to a lesser extent, at 24°C, none successfully emerged at 30°C. This failure was driven primarily by increased mortality of late-instar larvae in the high temperature group, potentially resulting from parasitoid failure to exit the host body. Ontogenetic variation in thermal sensitivity is increasingly recognized as a key constraint on parasitoid fitness (Malinski et al., <span>2024</span>; Moore et al., <span>2021</span>, <span>2022</span>; Valls et al., <span>2020</span>), and this study is consistent with other work showing this late larval developmental timepoint may impose critical constraints on parasitoid thermal tolerance (Moore et al., <span>2022</span>). Other relevant literature suggests that the sperm production stage of parasitoid development can function as a thermal constraint in different ways (Bressac et al., <span>2023</span>; El-Sabrout et al., <span>2021</span>). Additional work disentangling the mechanisms of high temperature disruption to host–parasitoid interactions across ontogeny is needed to improve predictions of climate change effects on parasitoid fitness and host population responses.</p><p>The phenomenon of host recovery from parasitism is a unique and understudied area of host–parasitoid ecology. Sex is rarely considered in studies of parasitoids attacking immature hosts, where it is often impossible to determine prior to eclosion. By working with adult hosts, this study reveals sex-specific vulnerabilities that may have important demographic consequences for host populations. Baudino et al. (<span>2025</span>) showed that host recovery probability was severely reduced at high temperatures, but this effect was difficult to assess given the low corresponding parasitoid survival at these temperatures. Interestingly, the researchers found an interaction between host sex and temperature on recovery of hosts, where the majority of infected females recovered at 18°C and 24°C, but in males this was only true for 24°C. Why are female hosts better able to recover at low temperatures than males? Authors discuss recovery as a function of the host's ability to suppress the DcPV in nerve tissues (Dheilly et al., <span>2015</span>) and speculate on the biology of host sex as a potential mediator: high temperatures may impair the ability of host nerve cells to recover from viral infection, while lower energetic reserves in males could exacerbate recovery costs at low temperature (Davis et al., <span>2006</span>). These hypotheses align with a broader body of work suggesting that parasitoid-associated symbionts, including viruses, may be a key vulnerability under heat stress which mediate thermal mismatches between hosts and parasitoids (Seehausen et al., <span>2017</span>; Malinski et al., <span>2023</span>). The mechanisms driving these interactive temperature-sex effects on host recovery, and the role symbionts play in these effects, warrant further investigation.</p><p>Testing these laboratory findings in field conditions is an important next step in this research. <i>Dinocampus coccinellae</i> frequently parasitizes overwintering ladybirds (Baudino et al., <span>2025</span>), suggesting that phenology and heat exposure across the season may influence ecological outcomes. Additionally, further examination into the host–parasitoid thermal ecology of adult host life stages is needed to create a holistic understanding of parasitoid climate change biology. 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引用次数: 0

Abstract

How climate change affects species interactions is a major issue in the field of ecology. Parasitoids play key ecological and economic roles as top-down controllers of herbivorous insect pests. A large body of research has shown that climate change disrupts host–parasitoid interactions, which can result in significant ecological shifts in the surrounding community (Kankaanpää et al., 2020; Malinski et al., 2023; Moore et al., 2021; Pardikes et al., 2022; Parker & Kingsolver, 2024; Schreven et al., 2017; Tougeron & Iltis, 2022; Wenda et al., 2023; Wu et al., 2016). However, most of this literature examines agriculturally relevant host–parasitoid systems, for example parasitoids of aphid or larval Lepidopteran hosts, and immature host life stages, for example egg, larva or nymph (Malinski et al., 2024). Because host life stages differ in mobility, sex, reproduction and other biological aspects, it is important to understand how climate change impacts host–parasitoid dynamics in parasitoids of different host life stages. The 2025 study by Baudino and colleagues (Baudino et al., 2025) brings much needed attention to the understudied system of adult host stage parasitism.

Baudino et al. (2025) examined the ecological outcomes of a host–parasitoid interaction between the braconid parasitoid wasp Dinocampus coccinellae and the invasive harlequin ladybird beetle Harmonia axyridis host across low (18°C), optimal (24°C) and high (30°C) temperatures. In this host–parasitoid system, D. coccinellae attacks adult hosts and uses a symbiotic RNA virus (D. coccinellae paralysis virus, DcPV) to induce temporary host paralysis prior to parasitoid emergence (Dheilly et al., 2015; Maure et al., 2011). After parasitoids complete development, some hosts recover normal feeding and reproductive behaviour, making host recovery a central life-history trait in this system. Host recovery is rare in host–parasitoid systems and therefore understudied: most existing reports are observational and seldom quantitative. By explicitly quantifying host recovery alongside other host and parasitoid fitness components, Baudino et al. (2025) add nuance and novelty to our understanding of host–parasitoid interactions and thermal ecology.

Consistent with patterns observed in most parasitoids, the authors found that elevated temperature proved detrimental to parasitoid success. While parasitoids frequently completed development at 18°C and, to a lesser extent, at 24°C, none successfully emerged at 30°C. This failure was driven primarily by increased mortality of late-instar larvae in the high temperature group, potentially resulting from parasitoid failure to exit the host body. Ontogenetic variation in thermal sensitivity is increasingly recognized as a key constraint on parasitoid fitness (Malinski et al., 2024; Moore et al., 2021, 2022; Valls et al., 2020), and this study is consistent with other work showing this late larval developmental timepoint may impose critical constraints on parasitoid thermal tolerance (Moore et al., 2022). Other relevant literature suggests that the sperm production stage of parasitoid development can function as a thermal constraint in different ways (Bressac et al., 2023; El-Sabrout et al., 2021). Additional work disentangling the mechanisms of high temperature disruption to host–parasitoid interactions across ontogeny is needed to improve predictions of climate change effects on parasitoid fitness and host population responses.

The phenomenon of host recovery from parasitism is a unique and understudied area of host–parasitoid ecology. Sex is rarely considered in studies of parasitoids attacking immature hosts, where it is often impossible to determine prior to eclosion. By working with adult hosts, this study reveals sex-specific vulnerabilities that may have important demographic consequences for host populations. Baudino et al. (2025) showed that host recovery probability was severely reduced at high temperatures, but this effect was difficult to assess given the low corresponding parasitoid survival at these temperatures. Interestingly, the researchers found an interaction between host sex and temperature on recovery of hosts, where the majority of infected females recovered at 18°C and 24°C, but in males this was only true for 24°C. Why are female hosts better able to recover at low temperatures than males? Authors discuss recovery as a function of the host's ability to suppress the DcPV in nerve tissues (Dheilly et al., 2015) and speculate on the biology of host sex as a potential mediator: high temperatures may impair the ability of host nerve cells to recover from viral infection, while lower energetic reserves in males could exacerbate recovery costs at low temperature (Davis et al., 2006). These hypotheses align with a broader body of work suggesting that parasitoid-associated symbionts, including viruses, may be a key vulnerability under heat stress which mediate thermal mismatches between hosts and parasitoids (Seehausen et al., 2017; Malinski et al., 2023). The mechanisms driving these interactive temperature-sex effects on host recovery, and the role symbionts play in these effects, warrant further investigation.

Testing these laboratory findings in field conditions is an important next step in this research. Dinocampus coccinellae frequently parasitizes overwintering ladybirds (Baudino et al., 2025), suggesting that phenology and heat exposure across the season may influence ecological outcomes. Additionally, further examination into the host–parasitoid thermal ecology of adult host life stages is needed to create a holistic understanding of parasitoid climate change biology. For example, in the D. coccinellae–H. axyridis system, hosts are paralysed by the DcPV, presumably eliminating behavioural thermoregulation and negating adult mobility effects on parasitism or host recovery. Whether parasitoids of adult hosts that do not induce paralysis show similar thermal sensitivities remains an open and intriguing question.

In sum, this important study addressed two broad gaps in host–parasitoid ecology. First, this research demonstrated how warming can alter host–parasitoid interactions in parasitoids of beetles and parasitoids attacking adult life stages, which are severely understudied relative to the dominance of Lepidopteran and aphid systems in agricultural contexts. Second, authors extend their study beyond typically lethal outcomes of parasitism and the narrow focus on host survival. By including parasitoid fitness metrics and the host trait of recovery, which may be central to population dynamics, the authors integrate multiple fitness components across both species to set a useful standard for future work. This work broadens our understanding of host–parasitoid thermal ecology and underscores the need to diversify the systems used to predict ecological responses in a rapidly warming world.

The author declares no conflicts of interest.

There is no data associated with this article.

寄生物攻击成年寄主的热生态:恢复、性效应和变暖的隐性成本
气候变化如何影响物种间的相互作用是生态学领域的一个主要问题。寄生蜂作为草食性害虫自上而下的控制者,具有重要的生态和经济作用。大量研究表明,气候变化破坏了宿主-拟寄生虫的相互作用,这可能导致周围社区发生重大的生态变化(Kankaanpää等人,2020;Malinski等人,2023;Moore等人,2021;Pardikes等人,2022;Parker等人;Kingsolver, 2024; Schreven等人,2017;Tougeron等人;Iltis, 2022; Wenda等人,2023;Wu等人,2016)。然而,这些文献大多研究了与农业相关的寄主-拟寄生虫系统,例如蚜虫或鳞翅目幼虫寄主的拟寄生虫,以及未成熟寄主的生命阶段,例如卵、幼虫或若虫(Malinski et al., 2024)。由于寄主生命阶段在移动性、性别、繁殖等生物学方面存在差异,因此了解气候变化如何影响寄主-寄主在不同寄主生命阶段的寄主-寄主动态具有重要意义。Baudino及其同事(Baudino et al., 2025)的2025研究对尚未得到充分研究的成年寄主阶段寄生系统提出了迫切需要的关注。Baudino等人(2025)研究了在低温(18°C)、最佳温度(24°C)和高温(30°C)条件下,瓢虫小蜂Dinocampus coccinellae和入侵瓢虫Harmonia axyridis宿主之间的寄主-寄主相互作用的生态结果。在这个宿主-拟寄生虫系统中,球菌球菌攻击成年宿主,并利用一种共生RNA病毒(球菌球菌麻痹病毒,DcPV)在拟寄生虫羽化之前诱导宿主暂时麻痹(Dheilly等,2015;Maure等,2011)。在拟寄生物发育完成后,一些寄主恢复正常的摄食和繁殖行为,使寄主恢复成为该系统的核心生活史特征。宿主恢复在宿主-寄生系统中很少见,因此研究不足:大多数现有报告都是观察性的,很少有定量的。Baudino等人(2025)通过明确量化宿主恢复以及其他宿主和寄生蜂适应性成分,为我们对宿主-寄生蜂相互作用和热生态学的理解增添了细微差别和新颖性。与在大多数寄生蜂中观察到的模式一致,作者发现温度升高对寄生蜂的成功是有害的。虽然寄生蜂经常在18°C和较小程度上在24°C下完成发育,但在30°C下没有成功出现。这种失败主要是由于高温组后期幼虫的死亡率增加,可能是由于寄生蜂未能离开寄主体。热敏感性的个体发生变化越来越被认为是寄生蜂适合度的关键制约因素(Malinski等人,2024;Moore等人,2021,2022;Valls等人,2020),该研究与其他研究一致,表明幼虫发育晚的时间点可能对寄生蜂的热耐受性施加关键制约(Moore等人,2022)。其他相关文献表明,拟寄生虫发育的精子产生阶段可以通过不同方式发挥热约束作用(Bressac et al., 2023; El-Sabrout et al., 2021)。为了更好地预测气候变化对拟寄生物适应性和寄主种群反应的影响,还需要进一步的工作来解开高温破坏宿主-拟寄生物相互作用的机制。寄主从寄生中恢复的现象是寄主-寄生生态学中一个独特的研究领域。在研究类寄生物攻击未成熟寄主的过程中,性别很少被考虑,因为在寄主羽化之前往往无法确定。通过与成年寄主合作,本研究揭示了可能对寄主人口产生重要人口影响的性别特异性脆弱性。Baudino等人(2025)的研究表明,在高温下,寄主恢复的概率会严重降低,但考虑到在高温下相应的寄生蜂存活率较低,这种影响很难评估。有趣的是,研究人员发现了宿主性别和温度对宿主恢复的相互作用,其中大多数受感染的雌性在18°C和24°C时恢复,但雄性只有在24°C时才恢复。为什么雌性寄主比雄性寄主更能在低温下恢复?作者讨论了恢复作为宿主抑制神经组织中DcPV的能力的功能(Dheilly等人,2015),并推测宿主性别生物学作为潜在的介质:高温可能会损害宿主神经细胞从病毒感染中恢复的能力,而雄性较低的能量储备可能会加剧低温下的恢复成本(Davis等人,2006)。 这些假设与更广泛的研究一致,这些研究表明,包括病毒在内的与寄生虫相关的共生体可能是热应激下的关键脆弱性,热应激介导宿主和寄生虫之间的热不匹配(Seehausen等人,2017;Malinski等人,2023)。驱动这些相互作用的温度-性别对宿主恢复的影响的机制,以及共生体在这些影响中所起的作用,值得进一步研究。在现场条件下测试这些实验室发现是本研究的重要下一步。Dinocampus coccinellae经常寄生在越冬的瓢虫身上(Baudino et al., 2025),这表明整个季节的物候和热暴露可能会影响生态结果。此外,需要进一步研究成虫生命阶段的寄主-寄生蜂热生态,以建立对寄生蜂气候变化生物学的整体理解。例如,在球菌球菌球菌- h。在寄生系统中,宿主被DcPV麻痹,可能消除了行为体温调节,并否定了成虫的流动性对寄生或宿主恢复的影响。不引起麻痹的成年寄主的拟寄生虫是否表现出类似的热敏性仍然是一个开放和有趣的问题。总之,这项重要的研究解决了宿主-寄生虫生态学的两个广泛空白。首先,本研究证明了变暖如何改变甲虫寄生蜂和攻击成虫阶段寄生蜂的宿主-寄生蜂相互作用,相对于农业环境中鳞翅目和蚜虫系统的优势,这方面的研究严重不足。其次,作者将他们的研究扩展到寄生的典型致命后果和对宿主生存的狭隘关注之外。通过包括寄生蜂的适应性指标和宿主的恢复特征,这可能是种群动态的核心,作者整合了两个物种的多种适应性成分,为未来的工作设定了有用的标准。这项工作拓宽了我们对宿主-寄生虫热生态学的理解,并强调了在快速变暖的世界中,用于预测生态反应的系统多样化的必要性。作者声明无利益冲突。没有与这篇文章相关的数据。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
Functional Ecology
Functional Ecology 环境科学-生态学
CiteScore
9.00
自引率
1.90%
发文量
243
审稿时长
4 months
期刊介绍: Functional Ecology publishes high-impact papers that enable a mechanistic understanding of ecological pattern and process from the organismic to the ecosystem scale. Because of the multifaceted nature of this challenge, papers can be based on a wide range of approaches. Thus, manuscripts may vary from physiological, genetics, life-history, and behavioural perspectives for organismal studies to community and biogeochemical studies when the goal is to understand ecosystem and larger scale ecological phenomena. We believe that the diverse nature of our journal is a strength, not a weakness, and we are open-minded about the variety of data, research approaches and types of studies that we publish. Certain key areas will continue to be emphasized: studies that integrate genomics with ecology, studies that examine how key aspects of physiology (e.g., stress) impact the ecology of animals and plants, or vice versa, and how evolution shapes interactions among function and ecological traits. Ecology has increasingly moved towards the realization that organismal traits and activities are vital for understanding community dynamics and ecosystem processes, particularly in response to the rapid global changes occurring in earth’s environment, and Functional Ecology aims to publish such integrative papers.
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