Temporal dynamics, evolution and mechanisms of transgenerational plasticity in a prey-predator context – TEATIME

Global change poses adaptive challenges to organisms, which have to face various forms of stress: habitat loss and fragmentation, invasive species pollutant or yet climate change. The main characteristic of environmental changes caused by human activities is that they occur faster and larger than those that organisms have likely experienced in their evolutionary past. Understanding how species tackle fast evolutionary challenges posed by global change is therefore more than ever crucial. Genetic adaptation, although sometimes surprisingly fast, is not the only way organisms may react to rapid environmental changes. Adaptive phenotypic plasticity is an alternative evolutionary solution adopted by organisms facing natural and human-induced fast-changing environments. Recently, plasticity was found to occur across generations (transgenerational plasticity, TGP) with the phenotype of a generation influenced by the environment experienced by the previous generation(s). TGP is taxonomically widespread and can occur in response to a wide range of biotic and abiotic environmental cues. TGP may be adaptive if offspring’s selective pressures resemble their parents’, as it prepares the offspring phenotype to them, even when they are not able to perceive the conditions by themselves. However, while more and more studies document TGP, we still have limited understanding of its evolutionary dynamics and underlying mechanisms.
The objective of TEATIME is to investigate the dynamics, evolutionary potential and mechanisms of TGP in the context of predator-induced defences. We recently demonstrated TGP of inducible defences in the freshwater snail Physa acuta. This snail is able to detect the predator (crayfish) odours, which induced morphological and behavioural defences in both the exposed snail and their offspring. This system is ideal to study transgenerational plasticity. P. acuta has a relatively short generation time (6 weeks) and is easy to rear in the laboratory. Our approach will be integrative. We will combine experimental approaches on adaptive traits (life-history, morphology, behaviour), ambitious experimental evolution protocols and cutting-edge investigation of molecular mechanisms at the genome scale, based on transcriptomics and epigenetics (chromatin openness).
TEATIME will be organized along three axes: (1) As TGP is a form of memory of past environments, what is the temporal dynamics of this memory? Firstly, we will investigate the sensitive developmental windows at which parents experience the environmental cues and at which the offspring express the response. Secondly, we will determine how much time (in generations) will this memory last; (2) As TGP is expected adaptive when parents and offspring are exposed to similar selection pressures, can it evolve in response to variation of the parent-offspring correlation in selective environments? We will conduct experimental evolution and evaluate local adaptation in transgenerational plasticity in natural populations; (iii) Can we detect the molecular bases of TGP. We will test in parallel whether the environmental experience of parents may change the gene expression patterns of offspring over generations and whether the environmental signal perceived by parents may be imprinted and transmitted via changes in chromatin openness.
Emilien Luquet, a young evolutionary ecologist working on plasticity for several years, has gathered partners with highly complementary skills to propose TEATIME. The project has the potential to shed a new light onto TGP that may position TGP as a process filling the gap between within-generational plasticity and long-term genetic adaptation, usually represented as a binary dichotomy in evolutionary theory, though they may end up being two extremes of a continuum from fast and ephemerous to slow and permanent responses.