Thermal plasticity of a freshwater cnidarian holobiont: detection of trans-generational effects in asexually reproducing hosts and symbionts

Abstract

Understanding factors affecting the susceptibility of organisms to thermal stress is of enormous interest in light of our rapidly changing climate. When adaptation is limited, thermal acclimation and deacclimation abilities of organisms are critical for population persistence through a period of thermal stress. Holobionts (hosts plus associated symbionts) are key components of various ecosystems, such as coral reefs, yet the contributions of their two partners to holobiont thermal plasticity are poorly understood. Here, we tested thermal plasticity of the freshwater cnidarian Hydra viridissima (green hydra) using individual behavior and population responses. We found that algal presence initially reduced hydra thermal tolerance. Hydra with algae (symbiotic hydra) had comparable acclimation rates, deacclimation rates, and thermal tolerance after acclimation to those without algae (aposymbiotic hydra) but they had higher acclimation capacity. Acclimation of the host (hydra) and/or symbiont (algae) to elevated temperatures increased holobiont thermal tolerance and these effects persisted for multiple asexual generations. In addition, acclimated algae presence enhanced hydra fitness under prolonged sublethal thermal stress, especially when food was limited. Our study indicates while less intense but sublethal stress may favor symbiotic organisms by allowing them to acclimate, sudden large, potentially lethal fluctuations in climate stress likely favor aposymbiotic organisms. It also suggests that thermally stressed colonies of holobionts could disperse acclimated hosts and/or symbionts to other colonies, thereby reducing their vulnerability to climate change.

Bacterial Symbionts Confer Thermal Tolerance to Cereal Aphids Rhopalosiphum padi and Sitobion avenae

“…The findings of this study corroborated the fact that the R. padi species is more heat tolerant and exhibits higher evolutionary potential to high temperature events as compared to S. avenae [ 10 , 13 , 30 ]. Moreover, the acclimation-induced enhanced thermal threshold observed in both aphid species is in line with previous studies demonstrating the greater thermal plasticity induced by the acclimation to elevated temperatures and by heat-hardening in Trichogramma wasps [ 31 ], mites [ 32 ] and in other organisms, such as in the aquatic hydra/algae holobiont system [ 33 ].…”

Extreme climate shifts pest dominance hierarchy through thermal evolution and transgenerational plasticity

“…This plasticity in heat tolerance may be driven by a multi‐generational mechanism. For example, epigenetic inheritance (Heard & Martienssen, 2014) of thermal tolerance or related high production of Hsp can be transferred for over three generations after thermal extremes in Artemia (Norouzitallab et al., 2014) and Hydra viridissima (Ye et al., 2019). In addition, obligate symbionts like Buchnera aphidicola could supply micro‐ Hsps to help its aphid host buffer heat stress (Dunbar et al., 2009).…”

“…However, mild temperature intermitted with thermal stress in nature may release intergenerational plasticity driven by stress. Even so, there is evidence for both epigenetic mechanisms and symbionts mediating a ‘true’ transgenerational response to thermal stress stably in offspring for more than three generations in the mild context, especially for asexually reproducing animals (Norouzitallab et al., 2014; Ye et al., 2019). Like genetic evolution, transgenerational plasticity varies among species, improving (Donelson et al., 2012) or deteriorating (Mousseau & Fox, 1998; Shama & Wegner, 2014) thermal tolerance.…”

“…In addition, interspecific variation in transgenerational (or intergenerational) responses, which often occur together with genetic evolution (Bonduriansky et al., 2012; Guillaume et al., 2016), may be involved in dominance shifts following extreme conditions. As long as transgenerational (or intergenerational) effects do not fade quickly (Klosin et al., 2017; Ye et al., 2019), they may change performance during subsequent periods of thermal selection in both positive and negative directions. For instance, short‐term selection can increase cold tolerance in Drosophila but ongoing selection decreases cold tolerance through detrimental intergenerational effects that accumulate to weaken adaptation and even cause maladaptation (Watson & Hoffmann, 1996).…”

“…Like genetic evolution, transgenerational plasticity varies among species, improving (Donelson et al., 2012) or deteriorating (Mousseau & Fox, 1998; Shama & Wegner, 2014) thermal tolerance. Furthermore, species‐specific transgenerational responses to thermal extremes affect population growth rates (see Hydra example in Ye et al., 2019) and could thereby influence the relative dominance of species in a community.…”