Trans‐generational plasticity in response to immune challenge is constrained by heat stress

Abstract

Trans‐generational plasticity (TGP) is the adjustment of phenotypes to changing habitat conditions that persist longer than the individual lifetime. Fitness benefits (adaptive TGP) are expected upon matching parent–offspring environments. In a global change scenario, several performance‐related environmental factors are changing simultaneously. This lowers the predictability of offspring environmental conditions, potentially hampering the benefits of TGP. For the first time, we here explore how the combination of an abiotic and a biotic environmental factor in the parental generation plays out as trans‐generational effect in the offspring. We fully reciprocally exposed the parental generation of the pipefish Syngnathus typhle to an immune challenge and elevated temperatures simulating a naturally occurring heatwave. Upon mating and male pregnancy, offspring were kept in ambient or elevated temperature regimes combined with a heat‐killed bacterial epitope treatment. Differential gene expression (immune genes and DNA‐ and histone‐modification genes) suggests that the combined change of an abiotic and a biotic factor in the parental generation had interactive effects on offspring performance, the temperature effect dominated over the immune challenge impact. The benefits of certain parental environmental conditions on offspring performance did not sum up when abiotic and biotic factors were changed simultaneously supporting that available resources that can be allocated to phenotypic trans‐generational effects are limited. Temperature is the master regulator of trans‐generational phenotypic plasticity, which potentially implies a conflict in the allocation of resources towards several environmental factors. This asks for a reassessment of TGP as a short‐term option to buffer environmental variation in the light of climate change.

Recent advances in vertebrate and invertebrate transgenerational immunity in the light of ecology and evolution

“…Parental effects are responsible for a broad range of plastic responses across generations, e.g. predator defenses (Agrawal et al 1999), acclimation to abiotic environmental changes (Donelson et al 2012;Sunday et al 2012;Shama and Wegner 2014;Roth and Landis 2017), and disease resistance (Mitchell and Read 2005;Goellner and Conrath 2008). Transgenerational immune priming (TGIP), where parents enhance offspring immune defense based on their own immunological experience, can thus be viewed as a case of phenotypic plasticity achieved through parental effects (Grindstaff et al 2003;Moret 2006;Hasselquist and Nilsson 2009;Moreau et al 2012;Roth et al 2012).…”

“…However, these limitations may not hold in animals with extreme paternal care. For instance, the sex-role reversed pipefish Syngnathus typhle has biparental TGIP (Roth et al 2012;Roth 2016a, b, 2017;Roth and Landis 2017). In S. typhle, males have evolved a unique placenta-like structure in the male brood pouch for nutrient and oxygen transfer (Wilson et al 2001;Dzyuba et al 2006;Harlin-Cognato et al 2006;Stölting and Wilson 2007;Ripley and Foran 2009), but it may also facilitate TGIP.…”

“…To substantially add to our understanding of TGIP, studies need to step away from only measuring classical routes and immune parameters. For example, it is now apparent that TGIP in vertebrates is much more than maternal antibody transfer, and endogenous immune-related gene expression of offspring can be significantly altered (Roth et al 2012;Roth 2016a, b, 2017;Roth and Landis 2017). Rapid advancements in sequencing technologies now allow for the TGIP phenotype to be tied to genome-wide transcriptomic patterns, and this has been informative in invertebrate systems (Trauer-Kizilelma and Hilker 2015; Barribeau et al 2016;Tate et al 2017).…”

Phloroglucinol Treatment Induces Transgenerational Epigenetic Inherited Resistance Against Vibrio Infections and Thermal Stress in a Brine Shrimp (Artemia franciscana) Model

“…Epigenetic changes involve chromatin remodeling, e.g., DNA methylation, histone modifications, and RNA-based epigenetic regulatory control, i.e., non-coding RNAs (ncRNA) such as microRNAs, small RNAs, and long RNAs (lncRNAs) and RNA methylation (9, 10). Currently, it is well-known that epigenetic programming during the early life stage not only can affect the organism directly in subsequent life stages but also can transmit traits via the germline to subsequent generations in a non-mendelian fashion (11, 12). Additionally, epigenetics reprogramming can be used to train the immune system by pre-exposing them to various stimuli, and it could serve as a promising approach ensuring enhanced immune response and disease resistance in cultured animals.…”

Phenotypic and molecular consequences of stepwise temperature increase across generations in a coral reef fish

“…Parents can potentially influence the performance of their offspring in stressful environmental conditions, through mechanisms such as transmission of beneficial epigenetic marks, nutrients, proteins, hormones or even through differences in parental care (Bonduriansky, Crean, & Day, ; Hofmann, ; Torda et al., ). Indeed, improvements in performance as a result of adaptive parental effects or transgenerational plasticity have been observed in a number of fish species, including pipefishes (Roth & Landis, ), sheepshead minnows (Salinas & Munch, ), skates (Lighten et al., ), three‐spine sticklebacks (Shama et al., , ) and tropical damselfish (Donelson et al., ). However, in the majority of multigenerational studies that evaluate the effects of climate change, end‐of‐the‐century temperature projections are immediately applied in one generation and kept stable across generations, even though most species will experience ocean warming across multiple generations.…”