One major concern related to climate change is that elevated temperatures will drive increases in parasite outbreaks. Increasing temperature is known to alter host traits and host–parasite interactions, but we know relatively little about how these are connected mechanistically—that is, about how warmer temperatures impact the relationship between epidemiologically relevant host traits and infection outcomes. Here, we used a zooplankton–fungus ( Daphnia dentifera–Metschnikowia bicuspidata ) disease system to experimentally investigate how temperature impacted physical barriers to infection and cellular immune responses. We found that Daphnia reared at warmer temperatures had more robust physical barriers to infection but decreased cellular immune responses during the initial infection process. Infected hosts at warmer temperatures also suffered greater reductions in fecundity and lifespan. Furthermore, the relationship between a key trait—gut epithelium thickness, a physical barrier—and the likelihood of terminal infection reversed at warmer temperatures. Together, our results highlight the complex ways that temperatures can modulate host–parasite interactions and show that different defense components can have qualitatively different responses to warmer temperatures, highlighting the importance of considering key host traits when predicting disease dynamics in a warmer world. This article is part of the theme issue ‘Infectious disease ecology and evolution in a changing world’.

Symbiosis is increasingly recognized as a dynamic relationship, with the net outcome falling along a continuum from mutualism to parasitism. A key example of this comes from a recently discovered microsporidian symbiont ofDaphnia, the net impact of which was found to vary from negative to positive. We investigated the taxonomic position of this microsporidian and the morphology of infected hosts, as well as the virulence, ecology and host range of the symbiont; we also provide information about its culturing methods. The genetic data indicates that the microsporidian symbiont belongs toOrdospora pajunii, a newly described microsporidian parasite ofDaphnia. We show thatO. pajuniiinfection damages the gut, causing infected epithelial cells to lose microvilli and then rupture. The prevalence of this microsporidian can be high (up to 100% in the lab and 77% of adults in the field). Its overall virulence seems low in most cases, but some genotypes suffer reduced survival and reproduction. Susceptibility and virulence are strongly host-genotype dependent. We found that North AmericanO. pajuniiare able to infect multipleDaphniaspecies, including the European speciesD. longispina, as well as the genusCeriodaphnia. We propose theDaphnia-O. pajuniisymbiosis as a valuable system for studying the mechanisms of context-dependent shifts between mutualism and parasitism, as well as for understanding how symbionts might alter host interactions with resources.

One major concern related to climate change is that elevated temperatures will drive increases in parasite outbreaks. Increasing temperature is known to alter host traits and host-parasite interactions, but we know relatively little about how these are connected mechanistically – that is, about how elevated temperatures impact the relationship between epidemiologically relevant host traits and infection outcomes. Here, we used a zooplankton-fungus (Daphnia dentifera-Metschnikowia bicuspidata) disease system to investigate whether temperature interacted with host susceptibility traits in determining infection outcomes. We did this by exposing D. dentifera to M. bicuspidata or leaving them unexposed at either control (20°C) or warming temperatures (24°C) in a fully factorial design. We found that elevated temperatures altered the physical barrier and immune responses to parasites during the initial infection process, and that infected hosts at elevated temperatures suffered a greater reduction of fecundity and lifespan. Furthermore, the relationship between a key trait – gut epithelium thickness, which is a physical barrier – and the likelihood of terminal infection reversed at warmer temperatures. Together, our results highlight the complex ways that temperatures can modulate host-parasite interactions, and the importance of considering key host susceptibility traits when predicting disease dynamics in a warmer world.This article is part of the theme issue ‘Infectious disease and evolution in a changing world’.

Transgenerational plasticity can help organisms respond rapidly to changing environments. Most prior studies of transgenerational plasticity in host–parasite interactions have focused on the host, leaving us with a limited understanding of transgenerational plasticity of parasites. We tested whether exposure to elevated temperatures while spores are developing can modify the ability of those spores to infect new hosts, as well as the growth and virulence of the next generation of parasites in the new host. We exposed Daphnia dentifera to its naturally co-occurring fungal parasite Metschnikowia bicuspidata, rearing the parasite at cooler (20°C) or warmer (24°C) temperatures and then, factorially, using those spores to infect at 20 and 24°C. Infections by parasites reared at warmer past temperatures produced more mature spores, but only when the current infections were at cooler temperatures. Moreover, the percentage of mature spores was impacted by both rearing and current temperatures, and was highest for infections with spores reared in a warmer environment that infected hosts in a cooler environment. In contrast, virulence was influenced only by current temperatures. These results demonstrate transgenerational plasticity of parasites in response to temperature changes, with fitness impacts that are dependent on both past and current environments.

Organisms are increasingly facing multiple stressors, which can simultaneously interact to cause unpredictable impacts compared with a single stressor alone. Recent evidence suggests that phenotypic plasticity can allow for rapid responses to altered environments, including biotic and abiotic stressors, both within a generation and across generations (transgenerational plasticity). Parents can potentially “prime” their offspring to better cope with similar stressors or, alternatively, might produce offspring that are less fit because of energetic constraints. At present, it remains unclear exactly how biotic and abiotic stressors jointly mediate the responses of transgenerational plasticity and whether this plasticity is adaptive. Here, we test the effects of biotic and abiotic environmental changes on within‐ and transgenerational plasticity using a Daphnia – Metschnikowia zooplankton‐fungal parasite system. By exposing parents and their offspring consecutively to the single and combined effects of elevated temperature and parasite infection, we showed that transgenerational plasticity induced by temperature and parasite stress influenced host fecundity and lifespan; offsprings of mothers who were exposed to one of the stressors were better able to tolerate elevated temperature, compared with the offspring of mothers who were exposed to neither or both stressors. Yet, the negative effects caused by parasite infection were much stronger, and this greater reduction in host fitness was not mitigated by transgenerational plasticity. We also showed that elevated temperature led to a lower average immune response, and that the relationship between immune response and lifetime fecundity reversed under elevated temperature: the daughters of exposed mothers showed decreased fecundity with increased hemocyte production at ambient temperature but the opposite relationship at elevated temperature. Together, our results highlight the need to address questions at the interface of multiple stressors and transgenerational plasticity and the importance of considering multiple fitness‐associated traits when evaluating the adaptive value of transgenerational plasticity under changing environments.