Discussion
Organisms are heavily affected by warming temperatures and show short- or long-term biological responses that include advancing phenologies, shifting geographical distribution ranges, and altered physiology (Huey and Kingsolver, 2019; McCarty, 2001; Thomas, 2010; Walther et al., 2002). Warming also affects biological fitness, such that organisms have altered reproduction and/or survival, with important consequences for population dynamics and ecosystem stability (Anderson, 2016; Deutsch et al., 2008; Kingsolver et al., 2013; Sinclair et al., 2016). While the fitness consequences of warming are widely considered to be negative, detailed investigations show a much more varied picture, with both negative and positive effects observed depending e.g. on the thermal tolerance and phenotypic plasticity of the species (Chamaillé-Jammes et al., 2006; Deutsch et al., 2008; Pelini et al., 2012; Weitere et al., 2009).
Here, I studied the fitness consequences of warming across the life cycle of a facultatively sexual freshwater cnidarian H. oligactis, an important predator of zooplankton in freshwater ecosystems. This species reproduces asexually during summer, switches to a sexual mode of reproduction after the temperature drops during autumn and experiences a post-reproductive senescence with increased mortality risk (Sebestyén et al., 2020, 2018). However, some individuals do not initiate sexual reproduction at all, or survive and continue reproducing asexually during the winter. Due to the heat-intolerance of this species (Bosch et al., 1988) and the dependence of sexual reproduction on cold temperature in H. oligactis , I hypothesized that warming might have negative fitness effects and an overall shift from sexual to asexual reproduction. The results paint a more complex picture of fitness effects of warming in Hydra .
Exposure of hydra polyps to simulated summer heat waves had immediate negative effects on the body size of hydra polyps. The reduction of body size with warming in animals is a widespread phenomenon (Gardner et al., 2011; Sheridan and Bickford, 2011), and is thought to be due to altered metabolic requirements and nutrient-dependence (Audzijonyte et al., 2022; Lee et al., 2015), oxygen limitation (Verberk et al., 2021; Walczyńska et al., 2015) or temperature-dependent size-fecundity or size-mortality relationships (Arendt, 2015; Audzijonyte et al., 2022). The size declines observed here were the result of phenotypic flexibility and occurred very quickly (observed after a week of exposure to simulated heat waves), suggesting a likely involvement of heat stress in the shrinkage of hydra polyps. Although such an immediate reduction in body size due to heat stress might not occur in most animals with a relatively fixed adult body size (e.g. insects), several other groups are able to plastically change adult size in response to environmental conditions (see e.g. Thommen et al., 2019 for an example of body size fluctuations in response to food availability in planarians), and in these animals warming, and the associated heatwaves could have an immediate effect on body size, just like in hydra. Furthermore, the changes in body size in hydra are significant because body size at cooling is a strong predictor of subsequent performance in this species: small polyps have delayed sexual maturation, reduced fecundity, but a higher post-reproductive survival (Ngo et al., 2021). In accordance, I found that polyps in the “Warm Summer” groups, exposed to simulated summer heat wave, required more time to produce the first gonads, had reduced sexual fitness and at least in males, they had a higher post-reproductive survival rate and higher asexual fitness.
The effects of the summer heat wave, however, were modulated by the winter treatment in a complex way. In H. oligactis , temperatures below 12 ºC degrees are required for gamete differentiation to occur (Littlefield, 1991; Littlefield et al., 1991), and researchers previously used temperatures from 4 to 10 ºC to induce sex in this species (Boutry et al., 2022; Kaliszewicz, 2015; Tomczyk et al., 2020). Higher simulated winter temperatures advanced sexual maturation in both males and females, which is consistent with a hypothesis that higher temperatures are more permissive for cell proliferation and the differentiation of gametes and reproductive tissue (Álvarez and Nicieza, 2002). These results suggest that, while all temperatures below or equal to 12 ºC promote sexual development in H. oligactis , the exact temperature can affect fine details of sexual development. The strongest effects on sexual development and fecundity were, however, observed in the WS-CW group, where simulated summer heatwaves were followed by a sudden drop in temperature. Animals in this group needed the most time to produce the first gonads and, at least in males, they had the lowest number of reproductive organs. This suggests that sudden drops in temperature are stressful for Hydra, and this stress could contribute to sex induction in this species. While temperature fluctuations as large as this (from 23 to 8 ºC within one day) are unlikely to occur under natural conditions in a freshwater habitat, both heat waves and cold spells, i.e. temperature variability are predicted to be more common in the future (Meehl et al., 2007) and these are likely to have negative physiological consequences in Hydra. Remarkably, I detected an unexpected consequence of simulated winter warming: polyps cultured under 12 ºC underwent a second round of gonadogenesis and continued to show signs of sexual reproduction five months after cooling, while all surviving polyps cultured on 8 ºC were asexual. Hence, while warming might have immediate negative effects on sexual reproduction in general in this species (especially if it demonstrates in increased temperature fluctuations), these negative effects could be counterbalanced on the longer term by the positive effects of warm winters on the number of reproductive cycles.
Compared to sexual reproduction, the effects of elevated temperatures on asexual fitness were much more clearcut (although sex-dependent). Polyps exposed to simulated heatwaves produced a higher number of asexual buds in male strains, and males exposed to elevated winter temperatures produced a higher number of asexual buds. The increased asexual fitness might be explained on one hand by a shift from sexual to asexual reproduction (possibly mediated by the reduced size of polyps exposed to simulated heat waves) and by the higher survival rate of polyps exposed to higher temperatures. Since asexual reproduction allows very quick population growth, these results suggest that increased temperatures will result in higher hydra population sizes in late winter due to climate warming. Hence, temperate freshwater bodies might experience “hydra blooms” similar to the warming-induced jellyfish blooms observed in marine environments (Goldstein and Steiner, 2020; Holst, 2012; Purcell et al., 2007), with potential up- and down-stream consequences on the whole aquatic food web. Unfortunately, little is known about hydra population dynamics under natural settings. Based on the phenology of resting egg production in H. oligactis, which peaks before the onset of the winter, one could assume that population size collapses during winter either due to freezing, low food availability, or increased mortality due to reduced somatic maintenance of sexually reproducing polyps (Sebestyén et al., 2018). The limited number of field observations, however, seem to contradict this assumption, since all observations point to the fact that H. oligactis thrives during the winter and reaches very large population densities (Bryden, 1952; Ribi et al., 1985; Welch and Loomis, 1924). The experiment presented here suggests that Hydra population sizes could become even higher in the future due to climate warming. Future studies should aim to test these predictions in a more natural setting, e.g., in mesocosms simulating the complexity of an aquatic food web to gain more insight into this problem.
In parallel with the higher asexual fitness of polyps exposed to simulated warming, I also found a positive effect of summer heatwaves and warmer winters on post-reproductive survival. Indeed, the higher asexual fitness of polyps exposed to higher temperature might be at least partly the consequence of their increased survival rate, although this effect was clearly observed only in males, while in females it was much more subtle. Hence, temperature appears in a growing list of intrinsic and extrinsic factors that affect post-reproductive survival in this species (age, size, genotype; Miklós et al., 2022; Ngo et al., 2021; Sebestyén et al., 2020). Exposure to high temperature could have resulted in higher survival for at least two different reasons. First, simulated summer heatwaves caused a reduction in body size, which is known to directly influence survival rate in this species (Ngo et al., 2021), most likely through a shift of resources from reproduction to survival. However, even male polyps that were not exposed to simulated summer heatwaves experienced improved survival rate if they were cultured at 12 ºC simulated winter temperatures, which points at a second, independent mechanism. The higher temperature could have caused improved survival by altering the metabolic cost of tissue maintenance in these polyps (Gillooly et al., 2001). Alternatively, it could also be the consequence of a shift from reproduction to survival functions in polyps experiencing warmer winters, although no clear evidence of that was observed, since polyps in the “Warm Winter” groups did not show evidence of reduced testes number compared to the “Cold Winter” groups. Further studies should explore the effect of temperature on post-reproductive survival in more detail.