Harbingers of change: towards a mechanistic understanding of anticipatory plasticity

1. Phenotypic plasticity is a central avenue through which organisms cope with environmental heterogeneity by responding to cues of current environmental change to maximize fitness. If environmental change is impending and cues can reliably predict future conditions, organisms can also mount adaptive responses in anticipation of these changes if they possess the mechanistic architecture to do so (i.e., anticipatory plasticity). 2. Anticipatory plasticity has been documented across the tree of life, but how organisms detect and integrate cues of future conditions and mount anticipatory responses remains ambiguous. We synthesize theoretical principles from sensory biology and animal communication with recent advances in physiological ecology and extrapolate these insights to identify candidate mechanisms that may underpin anticipatory plasticity. 3. We discuss how ecological rhythms, cue detection and perception, and three major physiological mechanisms–the epigenome, neuroendocrine system, and the commensal gut microbiota–can contribute to the evolution and maintenance of anticipatory plasticity. We then integrate across these components by focusing on anticipatory plasticity in reproductive phenotypes (i.e., anticipatory reproduction). 4. We close by detailing a series of open questions related to both the proximate causes and evolutionary consequences of anticipatory plasticity. We hope to shed light on the potential mechanisms that facilitate anticipatory plasticity in the face of environmental variation, and how these mechanisms may influence how organisms and populations respond to anthropogenic change.