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

Abstract

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’.

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

“…We scanned the anterior and posterior of the gut, where spores are most likely found penetrating into the host's body cavity (Stewart Merrill et al, 2019). We counted the number of spores, split into two categories (sensu Stewart Merrill et al, 2019): embedded spores (i.e., partially embedded in the gut epithelium; Figure 1b) and hemocoel spores (i.e., penetrated into the body cavity; Figure 1b); this allows us to quantify gut resistance (i.e., the extent to which the gut epithelium acts as a barrier to infecting spores) as the number of embedded spores divided by the total number of attacking spores (embedded spores + hemocoel spores), as done in earlier studies (Stewart Merrill et al, 2019; Sun, Dziuba, Jaye, et al, 2022). Meanwhile, we determined gut epithelium thickness by averaging the height of three haphazardly selected epithelium cells at the anterior end of the gut (Sun, Dziuba, Jaye, et al, 2022).…”

“…This experiment used the “Standard” lab lines of D. dentifera and M. bicuspidata originally isolated from a lake in Barry County, Michigan. We describe the maintenance of the D. dentifera and M. bicuspidata used in this study in more detail elsewhere (Sun, Dziuba, Jaye, et al, 2022). Immediately prior to this experiment, D. dentifera were maintained in standardized conditions (a 16:8 photoperiod at 22°C) for three generations and fed three times a week with a phytoplankton food ( Ankistrodesmus falcatus , 20,000 cells/ml).…”

“…This experiment relates to, but differs from, two other recent experiments. In the first (Sun, Dziuba, Jaye, et al, 2022), we focused on how temperature‐modified trait‐mediated infection outcomes in the F0 generation and did not look across generations. In the second related experiment (Sun, Dziuba, Mclntire, et al, 2022), we looked for evidence of transgenerational plasticity in the parasite (rather than in the host, which is the focus of the present study).…”

Infectious disease ecology and evolution in a changing world

“…To better understand the impact of environmental temperatures on disease outbreaks, two papers focus on changes in mechanisms underpinning the ability of parasites to infect [ 18 ] and of hosts to resist [ 19 ]. In effect, these papers take care to start from the beginning, where the host and parasite first meet, using the planktonic crustacean Daphnia and its bacterial parasites.…”

“…Like most hosts, waterfleas have physical barriers to infection and also have cellular immune responses. In detailed experiments, Sun et al [19] found that warming affected these defence traits differently, with consequences for infection outcomes. Disease spread can also depend on how temperature interacts with traits in host communities [20,21].…”