Two sides of a coin: ecological and chronobiological perspectives of timing in the wild

Abstract

Most processes within organisms, and most interactions between organisms and their environment, have distinct time profiles. The temporal coordination of such processes is crucial across levels of biological organization, but disciplines differ widely in their approaches to study timing. Such differences are accentuated between ecologists, who are centrally concerned with a holistic view of an organism in relation to its external environment, and chronobiologists, who emphasize internal timekeeping within an organism and the mechanisms of its adjustment to the environment. We argue that ecological and chronobiological perspectives are complementary, and that studies at the intersection will enable both fields to jointly overcome obstacles that currently hinder progress. However, to achieve this integration, we first have to cross some conceptual barriers, clarifying prohibitively inaccessible terminologies. We critically assess main assumptions and concepts in either field, as well as their common interests. Both approaches intersect in their need to understand the extent and regulation of temporal plasticity, and in the concept of 'chronotype', i.e. the characteristic temporal properties of individuals which are the targets of natural and sexual selection. We then highlight promising developments, point out open questions, acknowledge difficulties and propose directions for further integration of ecological and chronobiological perspectives through Wild Clock research.This article is part of the themed issue 'Wild Clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals'.

Keywords: chronotype; circadian; circannual; phenotypic plasticity; reaction norm; time programme.

Figure 1.

Schematic of the factors that affect an organism's manifest timing. The central, orange circle represents an organism, containing its biological timekeeping system shown in blue. Components of external abiotic cycles (shown in grey) and biotic cycles (shown in green) are perceived by an organism's sensory system. External information is interpreted based on an individual's internal clock time (e.g. whether warm winter temperatures should induce breeding), but at the same time, external time components can also modify internal clock time. Jointly, external time components and internal clock time influence individual timing outcomes, which on average can be used to characterize an individual's chronotype. The organism's behaviour and physiology can, in turn, feed back to affect rhythms of conspecifics (social time) or interspecifics (ecological time).

Figure 2.

Plasticity in the clock system. Multiple environmental factors may act on sensory systems that may or may not contain peripheral clocks (indicated by sine waves). The sensory systems are connected to, and can entrain internal clock time of the central clock (yellow central shape, showing multiple central oscillators with a sine wave). The central clock entrains peripheral oscillators and acts on effector systems via neuronal (circle-ended black lines) or other (e.g. humoral, thermal, black arrow) pathways. Environmental signals that are perceived by the sensory system can also act directly on effector systems (e.g. masking) (circle-ended dashed lines). Effector systems generate rhythms in organismal behaviour and physiology. Individual differences in the biological timekeeping system that integrates this information can arise in multiple ways, for example, through genetic variation, epigenetic variation, ontogeny and network properties.

Figure 3.

Chronotype as subject to selection. Most individuals will show some day-to-day variation in timing of physiology or behaviour, but often the relative timing compared with others in the population is quite consistent. Consistent differences in timing map to different chronotypes (red: early chronotype; blue: late chronotype). Because many environmental opportunities as well as risks to an animal (green arrows) depend on time, different chronotypes will have different fitness under different environmental conditions. When selection is directional this will lead to modification of the mechanisms that determine chronotype (blue arrows), and over time, to shifts in the distribution of chronotypes in the population (i.e. microevolution of chronotype).