Can hot temperatures limit disease transmission? A test of mechanisms in a zooplankton-fungus system

Abstract

316 / 350 WORDS) 23 1. Thermal ecology theory predicts that transmission of infectious diseases should respond 24 unimodally to temperature, i.e., be maximized at intermediate temperatures and 25 constrained at extreme low and high temperatures. However, empirical evidence linking 26 hot temperatures to decreased transmission in nature remains limited. 272. We tested the hypothesis that hot temperatures constrain transmission in a zooplankton-28 fungus (Daphnia dentifera-Metschnikowia bicuspidata) disease system where autumnal 29 epidemics typically start after lakes cool from their peak summer temperatures. This 30 pattern suggested that maximally hot summer temperatures could be inhibiting disease 31 spread. 32 3. Using a series of lab experiments, we examined the effects of high temperatures on five 33 mechanistic components of transmission. We found that (1) high temperatures increased 34 exposure to parasites by speeding up foraging rate but (2) did not alter infection success 35 post-exposure. (3) High temperatures lowered parasite production (due to faster host 36 death and an inferred delay in parasite growth). (4) Parasites made in hot conditions were 37 less infectious to the next host (instilling a parasite 'rearing' or 'trans-host' effect of 38 temperature during the prior infection). (5) High temperatures in the free-living stage also 39 reduce parasite infectivity, either by killing or harming parasites. 40 4. We then assembled the five mechanisms into an index of disease spread. The resulting 41 unimodal thermal response was most strongly driven by the rearing effect. Transmission 42 peaked at intermediate-hot temperatures (25-26°C) and then decreased at maximally hot 43temperatures (30-32°C). However, transmission at these maximally hot temperatures only 44 trended slightly lower than the baseline control (20°C), which easily sustains epidemics 45 3 in laboratory conditions and in nature. Overall, we conclude that while exposure to hot 46 epilimnetic temperatures does somewhat constrain disease, we lack evidence that this 47 effect fully explains the lack of summer epidemics in this natural system. This work 48 demonstrates the importance of experimentally testing hypothesized mechanisms of 49 thermal constraints on disease transmission. Furthermore, it cautions against drawing 50 conclusions based on field patterns and theory alone. 51 4 INTRODUCTION 52

Host–parasite dynamics shaped by temperature and genotype: Quantifying the role of underlying vital rates

“…In another study, Shocket et al. (2019) nicely illustrate how temperature increases can have contrasting effects on various components of parasite transmission, increasing host–parasite contact while decreasing parasite spore yield. It is these varying sensitivities and potentially contrasting effects that emphasize the importance of integrating single components, in order to quantify how changes in single components translate into changes in population fitness, and to get a more mechanistic understanding in the processes underlying population‐level responses.…”

“…For instance, temperature alters host–parasite interactions, both through interactive effects of temperature and parasitism on host performance (Greenspan et al., 2017; Hector et al., 2019; Padfield et al., 2020), as well as through temperature effects on parasite dynamics themselves (Cohen et al., 2019; Gehman et al., 2018; Morley & Lewis, 2014). Depending on how these thermal effects play out in a specific system, where both hosts and their parasites typically show unimodal responses to temperature (Dell et al., 2011; Kirk et al., 2018; Mordecai et al., 2019; Shocket et al., 2019), infections may become more prevalent and more severe under climate change in some systems (Altizer et al., 2013; Hall et al., 2006; Harvell et al., 2002; Lafferty, 2009; Lafferty & Mordecai, 2016; Mouritsen et al., 2005). This could threaten the persistence of natural populations even more than previously believed (Pounds et al., 2006; Harvell et al., 2002; Labaude et al., 2017; Mokany et al., 2019).…”

“…We expect heat stress to reduce an individual's ability to cope with infection (Hector et al., 2019), acting through multiple vital rates. Finally, temperature‐mediated changes in parasite resistance (Figure 1) could even further intensify the severity of infection at higher temperatures, but could also reduce the impact, if temperature exceeds optimum temperatures of the parasite (Gehman et al., 2018; Kirk et al., 2020; Mordecai et al., 2019; Shocket et al., 2019).…”

Thermal limits in the face of infectious disease: How important are pathogens?

“…For a host, thermal acclimation can improve both host thermal limits and resistance to infection (Allen & Little, 2011; Garbutt et al, 2014), although correlated increases in pathogen virulence can negate these beneficial changes (Greenspan et al, 2017). Likewise, pathogens reared under warmer temperatures have been shown to be more infectious to their subsequent host (Altman et al, 2016; Shocket, Vergara, et al, 2018), although hot temperatures prior to contacting a host can lead to a decrease in infectiousness (Shocket et al, 2019). How prior thermal experience affects host thermal limits during infection will therefore depend on the interaction between both host and pathogen thermal plasticity; something which models of disease dynamics parameterized from constant temperature experiments will not be able to account for (see also Raffel et al, 2013).…”

Can hot temperatures limit disease transmission? A test of mechanisms in a zooplankton–fungus system

“…Data and code are deposited in the Dryad Digital Repository: https://doi.org/10.5061/dryad.6mf734p (Shocket, Magnante, Duffy, Cáceres, & Hall, ).…”