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).