Predictable seasonal change in photoperiod triggers a sequential change in the daily activity-rest pattern, adaptive for migration in several bird species. The night-migratory black-headed bunting (Emberiza melanocephala) is day active under short photoperiods (8 h light:16 h dark, short day sensitive). Under long photoperiods (16 h light:8 h dark), the buntings are initially day active (long day premigratory) but subsequently become intensely night active (long day migratory) and after few weeks again return to a day active pattern (long day refractory). However, it is unclear how the daily expression of circadian genes changes during photoperiod-induced seasonal life-history states (LHSs). We measured period 2 (Per2), cryptochrome 1 (Cry1), brain and muscle arnt-like protein 1 (Bmal1), and circadian locomotor output cycles kaput (Clock) mRNA expressions in various neural and peripheral tissues of buntings in different LHSs and discovered differences of ∼2 to 6 h in the phase and 2- to 4-fold in amplitude of circadian oscillations of Per2, Cry1, and Bmal1 between photoperiod-induced LHSs. Phase relationship in mRNA oscillations was altered between oscillator components in the circadian pacemaker system (retina, pineal, hypothalamus) as well as in the peripheral (liver, muscle) tissues. These results show for the first time altered waveforms of clock gene expressions in all tissues in parallel with behavioral shifts and suggest the involvement of circadian system in photoperiod induction of seasonal LHSs in a migratory species.
Birds seasonally switch from one life history state (LHS) to another to maximize their fitness. Accordingly, they exhibit distinct differences in their physiological and behavioral phenotypes between seasons. Possible molecular mechanisms underlying changes through the seasons have scarcely been examined in migratory birds. The present study measured key genes suggested to be involved in the metabolic regulation of 4 photoperiodically induced seasonal LHSs in a long-distance migratory songbird, the blackheaded bunting (Emberiza melanocephala). Buntings were held under short days (8 h light:16 h darkness, 8L:16D), during which they maintained the winter nonmigratory phenotype. Then they were exposed for several weeks to long days (13L:11D). Differences in the activity-rest pattern, body fattening and weight gain, testis size, organ (heart, intestine) weights, and blood glucose and triglyceride levels confirmed that buntings sequentially exhibited spring migration-linked premigratory, migratory, and postmigratory LHSs under long days. The mRNA levels of circadian genes involved in metabolism (Bmal1, Clock, Npas2, Rorα, and Rev-erbα) and of genes that encode for proteins/enzymes involved in the regulation of glucose (Sirt1, FoxO1, Glut1, and Pygl) and lipids (Hmg-CoA; Pparα, Pparγ; Fasn and Acaca) showed LHS-dependent changes in their light-dark expression patterns in the hypothalamus and liver. These initial results on genetic regulation of metabolism in a migratory species extend the idea that the transitions between LHSs in a seasonal species are accomplished by changes at multiple regulatory levels. Thus, these findings promise new insights into the mechanism(s) of adaptation to seasons in higher vertebrates.
As both a photoreceptor and pacemaker in the avian circadian clock system, the pineal gland is crucial for maintaining and synchronizing overt circadian rhythms in processes such as locomotor activity and body temperature through its circadian secretion of the pineal hormone melatonin. In addition to receptor presence in circadian and visual system structures, high-affinity melatonin binding and receptor mRNA are present in the song control system of male oscine passeriform birds. The present study explores the role of pineal melatonin in circadian organization of singing and calling behavior in comparison to locomotor activity under different lighting conditions. Similar to locomotor activity, both singing and calling behavior were regulated on a circadian basis by the central clock system through pineal melatonin, since these behaviors free-ran with a circadian period and since pinealectomy abolished them in constant environmental conditions. Further, rhythmic melatonin administration restored their rhythmicity. However, the rates by which these behaviors became arrhythmic and the rates of their entrainment to rhythmic melatonin administration differed among locomotor activity, singing and calling under constant dim light and constant bright light. Overall, the study demonstrates a role for pineal melatonin in regulating circadian oscillations of avian vocalizations in addition to locomotor activity. It is suggested that these behaviors might be controlled by separable circadian clockworks and that pineal melatonin entrains them all through a circadian clock.
Daytime light intensity can affect the photoperiodic regulation of the reproductive cycle in birds. The actual way by which light intensity information is transduced is, however, unknown. We postulate that transduction of the light intensity information is mediated by changes in the pattern of melatonin secretion. This study, therefore, investigated the effects of high and low daytime light intensities on the daily melatonin rhythm of Afro-tropical stonechats (Saxicola torquata axillaris) in which seasonal changes in daytime light intensity act as a zeitgeber of the circannual rhythms controlling annual reproduction and molt. Stonechats were subjected to light conditions simulated as closely as possible to native conditions near the equator. Photoperiod was held constant at 12.25 h of light and 11.75 h of darkness per day. At intervals of 2.5 to 3.5 weeks, daytime light intensity was changed from bright (12,000 lux at one and 2,000 lux at the other perch) to dim (1,600 lux at one and 250 lux at the other perch) and back to the original bright light. Daily plasma melatonin profiles showed that they were linked with changes in daytime light intensity: Nighttime peak and total nocturnal levels were altered when transitions between light conditions were made, and these changes were significant when light intensity was changed from dim to bright. We suggest that daytime light intensity could affect seasonal timing via changes in melatonin profiles.
BackgroundIn many birds, day length (=photoperiod) regulates reproductive cycle. The photoperiodic environment varies between different seasons and latitudes. As a consequence, species at different latitudes may have evolved separate photoperiodic strategies or modified them as per their adaptive need. We studied this using house sparrow as a model since it is found worldwide and is widely investigated. In particular, we examined whether photoperiodism in house sparrows (Passer domesticus) at 27°N, 81°E shared features with those exhibited by its conspecifics at high latitudes.ResultsInitial experiment described in the wild and captive conditions the gonad development and molt (only in captives) cycles over a 12-month period. Both male and female sparrows had similar seasonal cycles, linked with annual variations in day length; this suggested that seasonal reproduction in house sparrows was under the photoperiodic control. However, a slower testis and attenuated follicular growth among captives indicated that other (supplementary) factors are also involved in controlling the reproductive cycle. Next experiment examined if sparrows underwent seasonal variations in their response to stimulatory effects of long day lengths. When birds were transferred every month over a period of 1 year to 16 hours light:8 hours darkness (16L:8D) for 17–26 weeks, there was indeed a time-of-year effect on the growth-regression cycle of gonads. The final experiment investigated response of house sparrows to a variety of light-dark (LD) cycles. In the first set, sparrows were exposed for 31 weeks to photoperiods that were close to what they receive in between the period from sunrise to sunset at this latitude: 9L:15D (close to shortest day length in December), 12L:12D (equinox, in March and September) 15L:9D (close to longest day length in June). They underwent testicular growth and regression and molt in 12L and 15L photoperiods, but not in 9L photoperiod. In the second set, sparrows were exposed for 17 weeks to photoperiods with light periods extending to different duration of the daily photosensitivity rhythm (e.g. 2L:22D, 6L:18D, 10L:14D, 14L:10D, 18L:6D and 22L:2D). Interestingly, a slow and small testicular response occurred under 2L and 10L photoperiods; 6L:18D was non-inductive. On the other hand, 14L, 18L and 22L photoperiods produced testicular growth and subsequent regression response as is typical of a long day photostimulation.ConclusionSubtropical house sparrows exhibit photoperiodic responses similar to that is reported for its population living at high latitudes. This may suggest the conservation of the photoperiodic control mechanisms in birds evolved over a long period of time, as a physiological strategy in a temporally changing environment ensuring reproduction at the best suited time of the year.
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