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.