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SFB 1047:  Insect Timing: Mechanisms, Plasticity and Interactions

Subject Area Biology
Medicine
Term from 2013 to 2017
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 208233609
 
Final Report Year 2018

Final Report Abstract

In this CRC we aimed to unravel the molecular, neuronal, and ecological mechanisms of insect timing including its benefits at various temporal and organizational scales. To reach this goal, we integrated different biological disciplines and studied timing in solitary insects, eusocial insects, and populations of interacting species. We revealed the importance of endogenous clocks and of plastic responses to the environment for adequate timing in all investigated systems. In fruit flies, we newly identified kinases that determine the speed of the circadian clock, neuropeptides that control daily or developmental timing, photoreceptors that are crucial for adjusting the daily activity patterns in a plastic way to the environmental light conditions, and metabolites that oscillate in a daily manner and are important for longevity and reproductive fitness. We demonstrated that the circadian clock is not only essential for timing development to adequate times of the day under natural conditions, but also for survival under nutritional restraints. When reared in direct competition for 64 generations, both a-rhythmic clock mutants and clock mutants with clocks that were too fast or too slow lost to wild-type flies and virtually disappeared from the population. We also showed that a functional clock enables fruit flies to learn the time of day, which may be useful for finding food. We characterized the circadian clock in the brain of several species and found that its main components are conserved but exhibit prominent adaptations to lifestyle and environment. For example, the circadian clock network in the brain of honeybees systematically grows during development and only reaches its final form in adult foragers, who need the clock for time-compensated sun-compass orientation. High-latitude flies, on the other hand, lack parts of the clock network and show only weak circadian rhythms, which appear to be an adaptation to the almost constant environment during summer in Northern Europe. Social bees and ants have an age-and experience-related division of labor and undergo behavioral transitions from nursing to foraging, the timing of which is critical for optimal colony maintenance. We identified several components that changed in the brain of these animals in parallel to the different tasks. Among these are changes in neuropeptides, changes in opsin expression, and changes in the number of synapses in the mushroom bodies that are important for olfactory and visual memory. These changes were partly age-related and partly experience-dependent showing that age and experience contribute to the optimal timing of nurse-forager transitions. In the "Cataglyphis" desert ants performing long-distance foraging trips at dangerously high temperatures, efficient navigation back to the nest is of essential importance for survival. Before the ants start their foraging trips, naïve ants perform structured learning walks close to the nest entrance. We showed for the first time that these learning walks trigger synaptic plasticity in visual input pathways to the central complex and mushroom bodies. We also found that the learning walks calibrate the sky-compass and visual landmark-guidance systems and, most importantly, that the geomagnetic field serves as initial directional reference system for these calibrations. Optimal seasonal timing strategies are especially important at the level of ecological communities that depend on the interactions between several species. We investigated the effects of day-length and season on the fitness of aphids, their interacting predators, and fungal-plant symbionts. Phenological shifts of aphids into early spring due to global warming induced desynchronization with their food plants and predators and resulted in fitness losses in all partners. Solitary bees exhibit an annual rhythm in adult emergence from their cocoons that must be synchronized with the flowering of relevant host plants. We found that even short temporal mismatches of bee emergence and plant flowering by three days strongly reduced the fitness of the bees (measured as reproductive output) clearly indicating the importance of precise timing. Mathematical simulations based on this data confirmed the importance of environmental temperature and the endogenous clock for emergence timing. The annual life cycle of social insects is characterized by a phase of colony foundation or onset of colony activity in spring, a phase of colony growth with workers, and a phase of sexual reproduction. Choosing the right moment for making the transition from one phase to the next greatly affects species fitness in these systems. For honeybees, we found that delaying colony growth decreased the capability of workers to exploit the abundant spring bloom. Early brood onset, on the other hand, increased the loads of the brood parasite Varroa destructor with negative impact on colony size. This indicates a timing-related trade-off and illustrates the importance of investigating effects of climate change on complex multi-trophic systems. Mathematical models showed that the seasonal time (photoperiod) is a reliable and robust trigger for making this transition, whereas climate chamber experiments indicate that ambient temperature plays a major role in the timing of brood onset in hibernating honeybee colonies. Field experiments on the foraging behavior of honeybees demonstrated the relevance of time memory and reveal that honeybees are capable of interval time-place learning to adapt to the complex and variable temporal patterns of floral resource environments. The disruption of the time memory-based dance communication of honeybee colonies reduced the performance of pollen foragers in landscapes with different resource complexity.

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