Introduction
Organisms living in the temperate zone are exposed to seasonal
fluctuations in temperature that provide contrasting physiological
environments during summer and winter. Many species inhabiting such
environments have adapted to temperature variation by specializing and
evolving thermal preference to either high or low temperature (Huey and
Kingsolver, 1989) or scheduling their major life events to different
parts of the year (McNamara and Houston, 2008). For instance, among
invertebrates that combine sexual with asexual reproduction in a complex
life cycle (i.e., facultatively sexual organisms, such as aphids,
flatworms, crustaceans, rotifers, sponges or cnidarians), sexual and
asexual reproduction events are often performed in different parts of
the year (Acker and Muscat, 1976; Fuchs et al., 2014; Green, 1966;
Reisa, 1973; Shaffer et al., 2020; Simon et al., 2002). Increasing or
decreasing temperatures in these species can induce a switch from
asexual to sexual reproduction (Acker and Muscat, 1976; Fuchs et al.,
2014; Reisa, 1973; Schröder, 2005; Shaffer et al., 2020; Simon et al.,
2002; Vowinckel, 1970), initiate the growth and development of embryos
inside resting eggs (Cáceres and Schwalbach, 2001; Cooley, 1971;
Gilbert, 2017; Gulbrandsen and Johnsen, 1990; Hairston and Kearns, 1995;
Vandekerkhove et al., 2005), and act as a modulator of other cues, such
as photoperiod and crowding (Decaestecker et al., 2009; Gyllström and
Hansson, 2004; Innes, 1997; Reisa, 1973; Schröder, 2005).
Temperature is a key regulator of the dynamics of populations because it
determines locomotor activity and food intake rates (Angilletta et al.,
2002) and acts as a physical factor regulating cellular processes, such
as metabolism or energy budgets (Brown et al., 2004; Huey and
Kingsolver, 2019), ultimately determining growth, reproduction and
survival (Angilletta, 2009). In facultatively sexual organisms both
sexual and asexual modes of reproduction critically depend on
temperature and switches in the mode of reproduction are expected to
have a major influence of population dynamics. Both modes of
reproduction contribute to population persistence and/or growth, albeit
in different ways. Asexual reproduction results in quick population
growth, allowing genotypes to increase in frequency when conditions are
favourable (Scheuerl and Stelzer, 2019). Sexual reproduction, by
contrast, often results in the production of resting eggs that are able
to survive adverse conditions. These resting eggs are able to persist
for years or even decades and replenish populations after stochastic
extinction events (Franch-Gras et al., 2017), provide sources of novel
genetic combinations with higher fitness (McLean et al., 2022), and
enable dispersal of propagules to novel habitats (Panov et al., 2004).
Recent climate change, however, is affecting temperatures worldwide and
rapidly rising temperatures have negative effects on organisms that
evolved under a different thermal regime (McCarty, 2001; Walther et al.,
2002). Documented effects of global warming include changes in phenology
(i.e. timing of major life history events such as migration in birds or
flowering in plants; (Jenni and Kéry, 2003; Molnár V et al., 2012)),
shifts in geographical range size (Thomas, 2010) and a widely detected
decline in animal body size (Sheridan and Bickford, 2011). Facultatively
sexual organisms, due to their adaptation to seasonally varying
temperature regimes, should be strongly impacted by warming
temperatures, although the complexity of facultatively sexual life
cycles makes prediction of the expected consequences of global warming
difficult. In aphids, for instance, documented population responses to
warming can be either positive, neutral or negative (Blanchard et al.,
2019; van Baaren et al., 2010). Since aphids are reproducing
parthenogenetically during summer and switch to sexual reproduction
during summer, rising temperatures are expected to yield short-term
increases in population sizes (until temperature becomes stressful) and
the disappearance of sexually produced offspring (Blanchard et al.,
2019). Warming temperatures have been shown in mesocosm experiments to
boost spring population growth of zooplankton, with a higher effect in
parthenogenetically reproducing cladocerans than non-parthenogenetic
copepods (Ekvall and Hansson, 2012). Due to the altered population
growth and differential thermal sensitivity, zooplankton communities
experience changes in dominance patterns (Ekvall and Hansson, 2012), but
also experience trophic mismatches that can result in population
declines (Winder and Schindler, 2004). However, despite these examples,
the number of studies examining the expected consequence of temperature
warming on facultatively sexual organisms is still very low. This is
unfortunate, since facultatively sexual organisms – through their
ability to achieve quick population growth through asexually
reproduction and long-term persistance and dispersal through the
production of dormant stages – are key components of the ecosystems
they inhabit, both as prey and as predators. Therefore, changes in their
population dynamics due to climate warming is likely to have wide-range
consequences at the level of the whole ecosystem.
The freshwater cnidarian Hydra oligactis Pallas 1766 is a small,
sessile predator inhabiting the temperate zone. It is a cold-adapted
species that prefers low temperatures, and even short-term exposures to
temperatures above 30 ºC are lethal (Bosch et al., 1988). They reproduce
asexually throughout much of the year through budding, however, they
rapidly switch to a sexual mode of reproduction upon exposure to cold
temperatures (Reisa, 1973). Males produce testes, and females produce
ovaries, and upon fertilization the egg develops a into a resting embryo
surrounded by a thick shell that is extremely resistant to adverse
conditions (Reisa, 1973). Hence, the production of resting eggs appears
to be an adaptation to survive freezing water through dormancy, and
indeed, sexually reproducing individuals are found in nature during
autumn, before the freezing of water surface occurs (Miklós et al.,
2021; Sebestyén et al., 2018). Following sexual reproduction, hydra
polyps experience a senescence-like process and increased mortality
risk, although some of them survive and revert to asexual reproduction
(Tökölyi et al., 2017; Yoshida et al., 2006), depending on their age,
size, and genotype (Miklós et al., 2022; Ngo et al., 2021; Sebestyén et
al., 2020). Because of the presence of these asexual individuals,H. oligactis can reach huge population densities during late
winter and early summer ((Bryden, 1952); J.T. personal observation)
which could influence the population dynamics of their prey (mainly
cladocerans and copepods) in a manner that amplifies with climate
change. However, whether warming temperatures affect sexual or asexual
fitness, and thereby population dynamics in hydra is still unclear.
Here, I set out to address this question by exposing H. oligactispolyps belonging to six strains (three male and three female) to
elevated temperature. Since climate warming is predicted to be unequal
across seasons (Meehl et al., 2007), I considered two scenarios: an
increased frequency of summer heatwaves and an increased average winter
temperature, both of these predicted based on current climate
projections for the temperate and boreal zone (Meehl et al., 2007). To
this end, hydra polyps were exposed either to a short (1-week long)
period of high summer temperature (23 ºC, compared to 18 ºC for
controls), which was followed by a winter treatment consisting either of
low (8 ºC) or high winter temperature (12 ºC) maintained for five
months. Throughout the experiment sexual and asexual fitness components
were recorded. Because of the sensitivity of H. oligactis to high
temperature I predicted reduced performance (both sexual and asexual) of
polyps exposed to short heatwaves. Furthermore, because of the
dependence of sexual reproduction on cold temperatures in H.
oligactis I predicted a reduced sexual fitness in groups exposed to
warm winter temperatures. Conversely, a higher asexual fitness and
survival might be predicted due to the negative relationship between
sexual reproduction and other fitness components (Ngo et al., 2021;
Roff, 1993; Stearns, 1989).