Project description:Annual cycles in daylength provide an initial predictive environmental cue that plants and animals use to time seasonal biology. Seasonal changes in photoperiodic information acts to entrain endogenous programs in physiology to optimize an animal’s fitness. Attempts to identify the neural and molecular substrates of photoperiodic time measurement in birds have, to date, focussed on blunt changes in light exposure during a restricted period of photoinducibility. The objectives of these studies were first to characterise a molecular seasonal clock in Japanese quail and second, to identify the key transcripts involved in endogenously generated interval timing that underlies photosensitivity in birds. We hypothesized that the mediobasal hypothalamus (MBH) provides the neuroendocrine control of photoperiod-induced changes in reproductive physiology, and that the pars distalis of the pituitary gland contains an endogenous internal timer for the short photoperiod dependent development of reproductive photosensitivity. Here we report distinct seasonal waveforms of transcript expression in the MBH, and pituitary gland and discovered the patterns were not synchronized across tissues. Follicle-stimulating hormone-β (FSHβ) expression increased during the simulated spring equinox, prior to photoinduced increases in prolactin, thyrotropin-stimulating hormone-β and testicular growth. Diurnal analyses of transcript expression showed sustained elevated levels of FSHβ under conditions of the spring equinox, compared to autumnal equinox, short (<12L) and long (>12L) photoperiods. FSHβ expression increased in quail held in non-stimulatory short photoperiod, indicative of the initiation of an endogenously programmed interval timer. These data identify that FSHβ establishes a state of photosensitivity for the external coincidence timing of seasonal physiology. The independent regulation of FSHβ expression provides an alternative pathway through which other supplementary environmental cues, such as temperature, can fine tune seasonal reproductive maturation and involution.

Project description:Seasonal adaptation to changes in light:dark regimes (i.e., photoperiod) allows organisms living at temperate latitudes to anticipate environmental change and adjust their physiology and behavior accordingly. The circadian system has been implicated in measurement and response to changes in photoperiod in nearly all animals studied so far (Saunders, 2011). The use of both traditional and non-traditional model insects with robust seasonal responses has recently genetically demonstrated the central role that clock genes play in photoperiodic response. Yet, the molecular pathways involved in insect photoperiodic responses remain largely unknown. Here, using the Eastern North American monarch butterfly (Reppert et al, 2016; Denlinger et al, 2017), we identified the vitamin A pathway as a novel pathway downstream of the circadian clock mediating insect photoperiod responsiveness. We found that interrupting clock function by disrupting circadian activation and repression abolishes photoperiodic responses in reproductive output, providing a functional link between clock genes and photoperiodic responsiveness in the monarch. Through transcriptomic approaches, we identified a molecular signature of seasonal-specific rhythmic gene expression in the brain, the organ known to function in photoperiodic reception in both Lepidoptera and some flies (Bowen et al, 1984; Saunders & Cymborowski, 1996). Among genes differentially expressed between both long and short photoperiods and between seasonal forms, several were belonging to the vitamin A pathway. The rhythmic expression of all of these genes was abolished in clock-deficient mutants. We also showed that a CRISPR/Cas9-mediated loss-of-function mutation in the pathway’s rate-limiting enzyme, ninaB1, impaired the monarch ability to respond to the photoperiod independently of visual function in the compound eye and without affecting circadian rhythms. Our finding that the vitamin A pathway is a key mediator of photoperiodic responses in insects could have broad implications for understanding the molecular mechanisms underlying photoperiodism.

Project description:Across evolutionary time, nearly all animal species have harnessed photoperiod to initiate processes that ultimately influence seasonal behavior and life history traits. In the freshwater cladoceran Daphnia magna, the effect of photoperiod on various life history traits has generally been investigated in conjunction with additional environmental stimuli. In the present study, we sought to untangling responses directly attributable to photoperiod in D. magna and identify the molecular processes underlying resultant behavioral and life history responses using functional analysis of global transcriptomic expression. D. magna were exposed to five different photoperiods immediately post-hatch for 21d where a standard long-day photoperiod of 16 hours light and 8 hours dark (16L:8D) served as the control relative to 4L:20D, 8L:16D, 12L:12L, and 20L:4D photoperiods. Entrainment to short-day photo-periods (4L:20D, 8L:16D, and 12L:12L) resulted in significantly increased light-avoidance behaviors relative to the control photoperiod where young Daphnia (7d old) displayed the most pronounced avoidance responses. Correspondingly, functional transcriptomics identified differential transcriptional expression of genes involved in glutamate signaling, which is critical in arthropod light-avoidance responses, as well as period circadian protein and proteins coding F-box/LRR-repeat domains, all of which contribute to establishing circadian rhythms in arthropods. Short-day photoperiods also induced increased metabolic rates which corresponded with broad-scale changes in transcriptional expression across multiple systems-level energy metabolism pathways. The most striking observation was increased male production across short-day photoperiods (4L:20D, 8L:16D, and 12L:12D). Transcriptional expression consistent with multiple putative mechanisms of male production were observed including expression suggestive of increased glutamate signaling; a response observed to induce male production in D. pulex via photo-period sensitive mechanisms. Overall, the results demonstrate the importance of photoperiod on behavior and life history trajectories in D. magna where we have now established multiple putative mechanistic pathways underlying several critical responses.

Dataset Information

FSHβ links photoperiodic signalling in the mediobasal hypothalamus to seasonal reproduction in Japanese quail.

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