Keeping time without a spine: what can the insect clock teach us about seasonal adaptation?

Abstract

Seasonal change in daylength (photoperiod) is widely used by insects to regulate temporal patterns of development and behaviour, including the timing of diapause (dormancy) and migration. Flexibility of the photoperiodic response is critical for rapid shifts to new hosts, survival in the face of global climate change and to reproductive isolation. At the same time, the daily circadian clock is also essential for development, diapause and multiple behaviours, including correct flight orientation during long-distance migration. Although studied for decades, how these two critical biological timing mechanisms are integrated is poorly understood, in part because the core circadian clock genes are all transcription factors or regulators that are able to exert multiple effects throughout the genome. In this chapter, we discuss clocks in the wild from the perspective of diverse insect groups across eco-geographic contexts from the Antarctic to the tropical regions of Earth. Application of the expanding tool box of molecular techniques will lead us to distinguish universal from unique mechanisms underlying the evolution of circadian and photoperiodic timing, and their interaction across taxonomic and ecological contexts represented by insects.This article is part of the themed issue 'Wild clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals'.

Keywords: climate change; clock genes; diapause; insect photoperiodism; migration; seasonal adaptations.

Figure 1.

Timing insect migration: from flight orientation to photoperiod-induced migratory switch. (a) Autumn migratory routes of western and eastern monarch butterflies on each side of the Rocky Mountains (brown lines), from their breeding to their overwintering sites in Mexico and California (light blue circle and dark blue line, respectively); (modified from Reppert et al. [22]). (b) Circadian clock control of monarch migration. Left, Circadian clocks in the antennae allow autumn migrants to time compensate their sun compass orientation to maintain a constant flight bearing to the south. The black arrows denote the southward orientation taken by migrants at any time of the day, and the grey dashed arrows denote the default direction the monarch would take in absence of time compensation. Right, Circadian clocks or clock genes in the brain may be part of a photoperiodic timer sensing a photoperiodic decrease that coincides with the onset of autumn southward movement. The blue dots depict the average latitude of eastern adult monarchs sighted at a given day between 1997 and 2013 (observations from Journey North, http://www.learner.org/jnorth/; sightings include the ‘First monarch butterfly’ and ‘Monarch first migration sighting’ for August–November; sightings from Florida were removed as they may be from a resident population). The orange dots depict the average photoperiod experienced by sighted adult monarchs at a given day.

Figure 2.

Differences in seasonal phenology between the ancestral hawthorn host plant and introduced domestic apples has driven speciation by allochronic reproductive isolation in Rhagoletis fruit flies. Radiation of univoltine Rhagoletis flies onto apples has also created a new temporal niche that allowed sequential speciation of a community of univoltine parasitoid wasps that attack these flies. Arrows radiating from flies to wasps signify that changes in the timing of fly seasonality to match their host fruits have also driven concomitant shifts in the seasonal timing of their parasitoid wasps. In both flies and their wasp parasites, regulation of diapause timing serves to synchronize hosts and consumers across trophic levels, driving genetic divergence by allochronic isolation.

Figure 3.

Alternative models for the relationship between the daily circadian clock and the seasonal photoperiodic timer. (a) Fully integrated mechanism in which the circadian clock (red) is viewed as an integrated unit that also provides the mechanistic basis of the photoperiodic timer (green). (b) Independent mechanisms in which the circadian clock and the photoperiodic timer are distinct physiological mechanisms.