Advancing behavioural genomics by considering timescale

Abstract

Animal behavioural traits often covary with gene expression, pointing towards a genomic constraint on organismal responses to environmental cues. This pattern highlights a gap in our understanding of the time course of environmentally responsive gene expression, and moreover, how these dynamics are regulated. Advances in behavioural genomics explore how gene expression dynamics are correlated with behavioural traits that range from stable to highly labile. We consider the idea that certain genomic regulatory mechanisms may predict the timescale of an environmental effect on behaviour. This temporally minded approach could inform both organismal and evolutionary questions ranging from the remediation of early life social trauma to understanding the evolution of trait plasticity.

Fig. 1

Environmental inputs at different time points (Ancestral, Parental, Developmental and Current) have variable timescales of effect (Evolutionary time, Lifetime and Days-minutes-seconds). The ancestral environment (e.g., the ecological context and selection pressures faced by individuals, including resource abundance, competition and predation threat) is transmitted across generations genetically as sequence level variation, and thus is considered as part of a spectrum of environmental circumstances (i.e., abiotic and biotic factors) that impact behavioural expression. In the hypothetical example above, a behavioural phenotype is influenced by (left to right): (1) inherited gene sequence variation that evolved over time (purple vs. blue and red), (2) parental influences (which may include chromatin-based epigenetic effects, or other features under parental control, e.g., egg composition or oviposition site), (3) the environment experienced throughout development (including impacts on tissue structure or other mechanisms), and (4) the current environment experienced in real time. Solid black arrows indicate shifts among levels of a phenotype. We propose that timescales for behavioural effects are likely non-independent due to shared underlying regulatory mechanisms

Fig. 2

The early-life environment, including maternal care behaviours, have broad and sometimes long-lasting health outcomes in mammals including humans. Stress reactivity is one iconic example of the effects of maternal stress on offspring behavioural phenotypes later in life. Rat with pup, photo credit: Eric Isselée/Shutterstock. All rights reserved

Fig. 3

Gene expression and behavioural dynamics are understudied, but may provide insights into other levels of organization that influence behaviour. Changes in phenotype in response to a transient shift in environmental conditions (grey vs. beige) is indicated as an increase in gene expression and behaviour. In this figure, we arbitrarily chose to show the direction of change for both phenotypes as an increase. The direction of any given behavioural change is context-dependent, and for many behaviours, genes show changes in expression in both directions (notably some genes, e.g., immediate early genes, commonly increase in expression). The green arrow indicates the potential interaction between behaviour and gene expression. Hypothetical outcomes of this interaction (blue lines 1–3) are discussed in Box 2

Fig. 4

Honey bee aggression shows a high degree of environmental sensitivity throughout life, as well as heritable variation as a function of genotype. Right: Solid lines indicate the continuous increase in aggressive tendency that occurs as bees age. Dotted lines indicate environmentally induced changes in aggression, which have variable timescales of effect. Green bars indicate short-term changes in aggression as a function of acute exposure to a predator threat. Left: Active honey bees at the colony entrance (Photo by C. Rittschof)