Developmental arcs of plasticity in whole movement repertoires of a clonal fish

Abstract

Developmental plasticity at the behavioral repertoire level allows animals to incrementally adjust their behavioral phenotypes to match their environments through ontogeny, serving as a lynchpin between ecological factors that cue phenotypic adjustments and evolutionary forces that select upon emergent phenotypic variation. Quantifying the continuous arcs of plasticity throughout animals development, however, has often been prohibitively challenging. Here, we leverage recent advancements in high-resolution behavioral tracking and analysis to (i) track the behavior of 45 genetically identical fish clones (Poecilia formosa) reared in near-identical environments during their first four weeks of life at 0.2 s resolution and (ii) quantify the continuous arcs of plasticity across entire behavioral repertoires through development. Doing so, we are able to test one of the most fundamental theoretical predictions from Bayesian models of development that in stable (but initially unknown) environments, behavioral plasticity should gradually decrease from a maximum at the beginning of life. Using two approaches to measure plasticity across ontogeny, we first quantify plasticity in individual behavioral metrics before also developing a novel whole-repertoire approach that calculates plasticity as the degree of behavioral entropy across a multi-dimensional behavioral phenotype space. We robustly find - despite experimentally matching as best as possible the assumptions of models that predict decreasing plasticity - a [~]two-week initial increase in plasticity in movement behaviors before plasticity subsequently decreased. Our results challenge a common intuition about the optimal developmental course of plasticity through early ontogeny, thereby also demonstrating the value of long-term behavioral tracking approaches for testing fundamental predictions on phenotypic development. Significance statementBehavioral plasticity across development may help animals adjust to uncertainty in moderately unpredictable environments. In stable environments, developing animals should gradually decrease this uncertainty through ontogeny, becoming less sensitive to incoming information (and thus less behaviorally plastic) as they age. This intuitive expectation of old dog inflexibility to new tricks, however, has not been adequately tested with the long-term, highresolution datasets that would be ideal. Here, we achieve such a test and emphasize the significance of this study in (1) providing a novel method for quantifying multi-dimensional behavioral plasticity continuously across long-term, high-resolution behavioral timeseries and in (2) testing fundamental theory that links the temporal patterning of environmental conditions to evolved patterns of behavioral plasticity across development.