Temperature and pathogen exposure act independently to drive host phenotypic trajectories

et al. 2022

Preprint

Organisms are increasingly facing multiple stressors, which can simultaneously interact to cause unpredictable impacts compared to 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 trans-generational plasticity using a Daphnia-Metschnikowia zooplankton-fungal parasite system. By exposing parents and their offspring consecutively to the single and combined effects of temperature elevation and parasite infection, we showed that transgenerational plasticity induced by temperature and parasite stress influenced host fecundity and lifespan; offspring of mothers that were exposed to one of the stressors were better able to tolerate temperature elevation, compared to offspring of mothers that 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 temperature elevation led to a lower average immune response, but the nature of its relationship with fecundity reversed under elevated temperatures; this suggests that parents that were exposed to parasites can potentially prime their offspring to respond to the joint stressors of both temperature elevation and parasite infection. 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.

Section: Discussioncontrasting

confidence: 99%

Transgenerational plasticity in a zooplankton in response to temperature elevation and parasitism

et al. 2022

Preprint

“…As expected given the virulence of this parasite, hosts that developed terminal infections suffered from shortened lifespan and fecundity loss. Nevertheless, at the moment there is no consensus on whether rising temperatures increase parasite virulence [63], and there is evidence that this will not always be the case [40]. In our study, the decreases in host fitness were particularly acute at warmer temperatures (figure 4).…”

Section: Discussionmentioning

confidence: 52%

“…This resulted in four treatment combinations: 20°C and 24°C in the presence of the parasite ( n = 55 individuals per treatment), and 20°C and 24°C in the absence of the parasite ( n = 45 individuals per treatment). Previous work has shown that 20°C is a favourable thermal condition for optimal growth and reproduction in another species of Daphnia [39,40]. Prior studies on D. dentifera have also used a similar range of temperatures, since these represent ecologically relevant temperatures that are within the thermal tolerance of this species (which cannot be cultured in temperatures of 27°C or higher; [9,38]).…”

Section: Methodsmentioning

confidence: 99%

Temperature modifies trait-mediated infection outcomes in aDaphnia–fungal parasite system

et al. 2023

Phil. Trans. R. Soc. B

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’.

“…Host parents who are challenged by parasites can potentially enhance the immune responses of offspring generation when challenged by the same parasites, a type of transgenerational plasticity also known as “transgenerational immune priming” (Paraskevopoulou et al, 2022 ; Sadd et al, 2005 ; Tetreau et al, 2019 ). However, while it is clear that multiple stressors can interact with one another, and that transgenerational plasticity can impact offspring fitness in the face of stressors, most studies of transgenerational plasticity to date have focused on single biotic or abiotic factors (but see Garbutt et al, 2014 ; Hector et al, 2021 ; Roth & Landis, 2017 ), leaving a gap in understanding transgenerational effects in the context of multiple‐stressor research.…”

Section: Introductionmentioning

confidence: 99%

Transgenerational plasticity in a zooplankton in response to elevated temperature and parasitism

et al. 2023

Ecology and Evolution

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.