SFB 1047: Insect Timing: Mechanisms, Plasticity and Interactions
Medicine
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.
Publications
- (2014) Channelrhodopsin-2-XXL, a powerful optogenetic tool for low light applications. Proc Natl Acad Sci USA 111:13972–13977
Dawydow A, Gueta R, Ljaschenko D, Ullrich S, Hermann M, Ehmann N, Gao S, Fiala A, Langenhan T, Nagel G, Kittel RJ
(See online at https://doi.org/10.1073/pnas.1408269111) - (2014) Light exposure leads to reorganization of microglomeruli in the mushroom bodies and influences juvenile hormone levels in the honeybee. Dev Neurobiol 74:1141-1153
Scholl C, Wang Y, Krischke M, Mueller MJ, Amdam GV, Rössler W
(See online at https://doi.org/10.1002/dneu.22195) - (2014) Specialization and phenological synchrony of plant-pollinator interactions along an altitudinal gradient. J Animal Ecol 83:639–650
Benadi G, Hovestadt T, Poethke H-J, Blüthgen N
(See online at https://doi.org/10.1111/1365-2656.12158) - (2014) The Ion Transport Peptide is a new functional clock neuropeptide in the fruit fly Drosophila melanogaster. J Neurosci 34:9522-9536
Hermann-Luibl C, Yoshii T, Senthilan PR, Dircksen H, Helfrich-Förster C
(See online at https://doi.org/10.1523/jneurosci.0111-14.2014) - (2014) The MAP kinase p38 is part of Drosophila melanogaster's circadian clock. PLoS Genet 10:e1004565
Dusik V, Senthilan PR, Mentzel B, Hartlieb H, Wülbeck C, Yoshii T, Raabe T, Helfrich-Förster C
(See online at https://doi.org/10.1371/journal.pgen.1004565) - (2015) Annual dynamics of wild bee densities: attractiveness and productivity effects of oilseed rape. Ecology 96:1351-1360
Riedinger V, Mitesser O, Hovestadt T, Steffan-Dewenter I, Holzschuh A
(See online at https://doi.org/10.1890/14-1124.1) - (2015) Biological pest control and yields depend on spatial and temporal crop cover dynamics. J Appl Ecol 52:1283-1292
Schneider G, Krauss J, Riedinger V, Holzschuh A, Steffan-Dewenter I
(See online at https://doi.org/10.1111/1365-2664.12471) - (2015) Coping with shorter days: Do phenology shifts constrain aphid fitness? PeerJ 3:e1103
Joschinski J, Hovestadt T, Krauss J
(See online at https://doi.org/10.7717/peerj.1103) - (2015) Dispersal timing: Emigration of insects living in patchy environments. PLoS ONE 10:e0128672
Lakovic M, Poethke H-J, Hovestadt T
(See online at https://doi.org/10.1371/journal.pone.0128672) - (2015) Flies remember the time of day. Curr Biol 25 (12):1619-1624
Chouhan NS, Wolf R, Helfrich-Förster C, Heisenberg M
(See online at https://doi.org/10.1016/j.cub.2015.04.032) - (2015) Normal vision can compensate for the loss of the circadian clock. Proc Roy Acad Sci B 282:20151846
Schlichting M, Menegazzi P, Helfrich-Förster C
(See online at https://doi.org/10.1098/rspb.2015.1846) - (2016) A neuronal network underlying circadian entrainment and photoperiodic adjustment of sleep and activity. J Neurosci 36:9084-9096
Schlichting M, Menegazzi P, Lelito K, Yao Z, Buhl E, Dalla Benetta E, Bahle A, Denike J, Hodge JJL, Helfrich-Förster C, Shafer OT
(See online at https://doi.org/10.1523/jneurosci.0992-16.2016) - (2016) A new device for monitoring individual activity rhythms of a honey bee (Apis mellifera) reveals critical effects of the social environment on behavior. J Comp Physiol A 202:555-565
Beer K, Steffan-Dewenter I, Härtel S, Helfrich-Förster C
(See online at https://doi.org/10.1007/s00359-016-1103-2) - (2016) Age-related and light-induced plasticity in opsin gene expression and in primary and secondary visual centers of the nectar-feeding ant Camponotus rufipes. Dev Neurobiol 76:1041-1057
Yilmaz A, Lindenberg A, Albert S, Grübel K, Spaethe J, Rössler W, Groh C
(See online at https://doi.org/10.1002/dneu.22374) - (2016) Allatostatin A signalling regulates feeding and sleep and is downstream of PDF-signaling in Drosophila. PLOS Genetics 12:e1006346
Chen J, Reiher W, Hermann-Luibl C, Sellami A, Cognigni P, Kondo S, Helfrich-Förster C, Veenstra JA, Wegener C
(See online at https://doi.org/10.1371/journal.pgen.1006346) - (2016) Daily thermal fluctuations experienced by pupae via rhythmic nursing behavior increase numbers of mushroom body microglomeruli in the adult ant brain. Front Behav Neurosci 10:73
Falibene A, Roces F, Rössler W, Groh C
(See online at https://doi.org/10.3389/fnbeh.2016.00073) - (2016) Learning walks and the acquisition of landmark information in desert ants, Cataglyphis fortis. J Exp Biol 219:3137-3145
Fleischmann PN, Christian M, Müller VL, Rössler W, Wehner R
(See online at https://doi.org/10.1242/jeb.140459) - (2016) Pea aphids have diurnal rhythms when raised independently of a host plant. J Insect Sci 31:1-5
Joschinski J, Beer K, Helfrich-Förster C, Krauss J
(See online at https://doi.org/10.1093/jisesa/iew013) - (2016) The evolution of optimal emergence times: bet hedging and the quest for an ideal free temporal distribution of individuals. Oikos 125:1647–1656
Poethke HJ, Hovestadt T, Mitesser O
(See online at https://doi.org/10.1111/oik.03213) - (2016) The timed depolarization of morning and evening oscillators phase shifts the circadian clock of Drosophila. J Biol Rhythms 31:428-442
Eck S, Helfrich-Förster C, Rieger D
(See online at https://doi.org/10.1177/0748730416651363) - (2017) A damping circadian clock drives weak oscillations in metabolism and locomotor activity of aphids (Acyrthosiphon pisum). Sci Reports 7:14906
Beer K, Joschinski J, Alazne AS, Krauss J, Helfrich-Förster C
(See online at https://doi.org/10.1038/s41598-017-15014-3) - (2017) A new Rhodopsin influences light-dependent daily activity patterns of fruit flies. J Biol Rhythms 32:406-422
Kistenpfennig C, Grebler R, Ogueta M, Hermann-Luibl C, Schlichting M, Stanewsky R, Senthilan PR, Helfrich-Förster C
(See online at https://doi.org/10.1177/0748730417721826) - (2017) Adaptation of circadian neuronal network to photoperiod in high-latitude European Drosophilids. Curr Biol 27:833-839
Menegazzi P, Dalla Benetta E, Beauchamp M, Schlichting M, Steffan-Dewenter I, Helfrich-Förster C
(See online at https://doi.org/10.1016/j.cub.2017.01.036) - (2017) Combined effects of waggle dance communication and landscape heterogeneity on nectar and pollen uptake in honey bee colonies. PeerJ 5:e3441
Nürnberger F, Steffan-Dewenter I, Härtel S
(See online at https://doi.org/10.7717/peerj.3441) - (2017) Enhanced aphid abundance in spring desynchronizes predator-prey and plant-microorganism interactions. Oecologia 183:469–478
Fuchs B, Breuer T, Krischke M, Mueller MJ, Findling S, Holzschuh A, Krauss J
(See online at https://doi.org/10.1007/s00442-016-3768-1) - (2017) Mating timing, dispersal and local adaptation in patchy environments. Oikos 12:1804-1814
Lakovic M, Mitesser O, Hovestadt T
(See online at https://doi.org/10.1111/oik.04369) - (2017) Neuropeptides in the desert ant Cataglyphis fortis: Mass spectrometric analysis, localization, and age-related changes. J Comp Neurol 525:901-918
Schmitt F, Vanselow JT, Schlosser A, Wegener C, Rössler W
(See online at https://doi.org/10.1002/cne.24109) - (2017) Plant age and seasonal timing determine endophyte growth and alkaloid biosynthesis. Fungal Ecol 29:52-58
Fuchs B, Krischke M, Mueller MJ, Krauss J
(See online at https://doi.org/10.1016/j.funeco.2017.06.003) - (2017) Plasticity of daily behavioral rhythms in foragers and nurses of the ant Camponotus rufipes: influence of social context and feeding times. PLoS ONE 12:e0169244
Mildner S, Roces F
(See online at https://doi.org/10.1371/journal.pone.0169244) - (2017) Species-specific differences in the fine structure of learning-walk elements in Cataglyphis ants. J Exp Biol 220:2426-2435
Fleischmann PN, Grob R, Wehner R, Rössler W
(See online at https://doi.org/10.1242/jeb.158147) - (2017) The PTTH neuropeptide couples central and peripheral clocks in Drosophila. Nature Comm 8:15563
Selcho M, Millán C, Palacios-Muñoz A, Ruf F, Ubillo L, Chen J, Bergmann G, Ito C, Silva V, Wegener C, Ewer J
(See online at https://doi.org/10.1038/ncomms15563) - (2017) The role of celestial compass information in Cataglyphis ants during learning walks and for neuroplasticity in the central complex and mushroom bodies. Front Behav Neurosci 11:226
Grob R, Fleischmann PN, Grübel K, Wehner R, Rössler W
(See online at https://doi.org/10.3389/fnbeh.2017.00226) - (2018) Desynchronizations in bee-plant interactions cause severe fitness losses in solitary bees. J Animal Ecol 87:139-149
Schenk M, Krauss J, Holzschuh A
(See online at https://doi.org/10.1111/1365-2656.12694) - (2018) Drosophila RSK influences the pace of the circadian clock by negative regulation of protein kinase Shaggy activity. Front Mol Neurosci 11:122
Beck K, Hovhanyan A, Menegazzi P, Helfrich-Förster C, Raabe T
(See online at https://doi.org/10.3389/fnmol.2018.00122) - (2018) Neuroanatomical details of Drosophila lateral neurons support their functional role in the circadian system. J Comp Neurol 526:1209-1231
Schubert FK, Hagedorn N, Yoshii T, Helfrich-Förster C, Rieger D
(See online at https://doi.org/10.1002/cne.24406) - (2018) Opsin expression patterns coincide with photoreceptor development during pupal development in the honey bee, Apis mellifera. BMC Dev Biol 18:1
Lichtenstein L, Grübel K, Spaethe J
(See online at https://doi.org/10.1186/s12861-018-0162-8) - (2018) Pigment-Dispersing Factor expressing neurons provide an infrastructure for conveying circadian information in the honey bee brain. Open Biol 8:170224
Beer K, Kolbe E, Kahana N, Yayon N, Weiss R, Menegazzi P, Bloch G, Helfrich-Förster C
(See online at https://doi.org/10.1098/rsob.170224) - (2018) The circadian clock of the ant Camponotus floridanus is localized in dorsal and lateral neurons of the brain. J Biol Rhythms
Kay J, Menegazzi P, Mildner S, Roces F, Helfrich-Förster C
(See online at https://doi.org/10.1177/0748730418764738) - (2018) The geomagnetic field is a compass cue in Cataglyphis ant navigation. Curr Biol, Volume 28, Issue 9, 7 May 2018, Pages 1440-1444.e2.
Fleischmann PN, Grob R, Müller VL, Wehner R, Rössler W
(See online at https://doi.org/10.1016/j.cub.2018.03.043) - (2018) Day length constrains the time budget of aphid predators. Insect Sci., Volume 26, Issue1, February 2019, Pages 164-170.
Joschinski J, Kiess T, Krauss J
(See online at https://doi.org/10.1111/1744-7917.12507)
