Mechanisms underlying phenotypic plasticity in response to environmental change

Understanding how human activity impacts natural systems is crucial for maintaining ecosystem health and the services these provide for societies. Phenotypic plasticity - the regulated expression of different phenotypes by a single genotype - is the most effective response to increase resistance or resilience of phenotypes to rapidly changing environments. Here, we review the mechanisms that underlie phenotypic plasticity in animals. Understanding the regulatory mechanisms is important because these determine the time course of establishment and persistence of alternative phenotypes. We propose that regulation of trans- and intergenerational plasticity, developmental plasticity and reversible acclimation involves (i) environmental information acquisition, (ii) signal integration, and (iii) translation of environmental information to alter phenotypes. We provide a high-level overview of each of these stages with the aim of summarising current knowledge and making it accessible to a broader audience who are not necessarily expert in neuroendocrine and molecular biology. Information acquisition occurs primarily by sensors that transduce environmental information (e.g. temperature, light, chemicals, etc.) to the central nervous system. An exception is AMP-activated protein kinase (AMPK) that senses cellular energy levels and interacts locally and with neuroendocrine systems to adjust anabolic and catabolic metabolism. Signal integration is achieved primarily by neural and endocrine mechanisms. The major players are the autonomic nervous system, the hypothalamus-pituitary-adrenal/interrenal (HPA/I), the hypothalamus-pituitary-thyroid (HPT), and the hypothalamus-pituitary-somatotrophic (HPS) axes, which receive environmental information from the brain and transmit it via hormone signalling. Phenotypic effects of these major axes can be directly to the target tissues, or via epigenetically modified gene expression programs. DNA methylation, histone modifications, and microRNAs are the principal epigenetic processes, of which the first two are regulated by neuroendocrine signalling. Importantly, all of these processes (AMPK, neuroendocrine, epigenetic) interact with each other so that regulation occurs in a network-like manner rather than by individual regulators alone. Nonetheless, an appreciation of individual mechanisms is an essential starting point that can guide future research into more complex interactions to advance understanding of the evolution and ecological importance of plasticity.