Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds

Yoshimura, Takashi; Yasuo, Shinobu; Watanabe, Miwa; Iigo, Masayuki; Yamamura, Takashi; Hirunagi, Kanjun; Ebihara, Shizufumi

doi:10.1038/nature02117

Cited by 463 publications

(387 citation statements)

References 23 publications

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“…Gwinner & Dittami 1980;Gwinner 1981;Ubuka et al 2005). Other hormones, such as leptin, orexin, ghrelin and thyroxines could influence circannual rhythmicity, but so far the evidence for a causal involvement in the generation of these long-term clocks is missing (Yoshimura et al 2003;Mustonen et al 2005;Kondo et al 2006).…”

Section: Discussionmentioning

confidence: 99%

Avian circannual clocks: adaptive significance and possible involvement of energy turnover in their proximate control

Wikelski

Martin

Scheuerlein

et al. 2007

Phil. Trans. R. Soc. B

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Endogenous circannual clocks are found in many long-lived organisms, but are best studied in mammal and bird species. Circannual clocks are synchronized with the environment by changes in photoperiod, light intensity and possibly temperature and seasonal rainfall patterns. Annual timing mechanisms are presumed to have important ultimate functions in seasonally regulating reproduction, moult, hibernation, migration, body weight and fat deposition/stores. Birds that live in habitats where environmental cues such as photoperiod are poor predictors of seasons (e.g. equatorial residents, migrants to equatorial/tropical latitudes) rely more on their endogenous clocks than birds living in environments that show a tight correlation between photoperiod and seasonal events. Such population-specific/interspecific variation in reliance on endogenous clocks may indicate that annual timing mechanisms are adaptive. However, despite the apparent adaptive importance of circannual clocks, (i) what specific adaptive value they have in the wild and (ii) how they function are still largely untested. Whereas circadian clocks are hypothesized to be generated by molecular feedback loops, it has been suggested that circannual clocks are either based upon (i) a de-multiplication ('counting') of circadian days, (ii) a sequence of interdependent physiological states, or (iii) one or more endogenous oscillators, similar to circadian rhythms. We tested the de-multiplication of days (i) versus endogenous regulation hypotheses (ii) and (iii) in captive male and female house sparrows (Passer domesticus). We assessed the period of reproductive (testicular and follicular) cycles in four groups of birds kept either under photoperiods of LD 12 L : 12 D (period length: 24 h), 13.5 L : 13.5 D (27 h), 10.5 L : 10.5 D (23 h) or 12 D : 8 L : 3 D : 1 L (24-h skeleton photoperiod), respectively, for 15 months. Contrary to predictions from the de-multiplication hypothesis, individuals experiencing 27-h days did not differ (i.e. did not have longer) annual reproductive rhythms than individuals from the 21-or 24-h day groups. However, in line with predictions from endogenous regulation, birds in the skeleton group had significantly longer circannual period lengths than all other groups. Birds exposed to skeleton photoperiods experienced fewer light hours per year than all other groups (3285 versus 4380) and had a lower daily energy expenditure, as tested during one point of the annual cycle using respirometry. Although our results are tantalizing, they are still preliminary as birds were only studied over a period of 15 months. Nevertheless, the present data fail to support a 'counting of circadian days' and instead support hypotheses proposing whole-organism processes as the mechanistic basis for circannual rhythms. We propose a novel energy turnover hypothesis which predicts a dependence of the speed of the circannual clock on the overall energy expenditure of an organism.

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Section: Discussionmentioning

confidence: 99%

Avian circannual clocks: adaptive significance and possible involvement of energy turnover in their proximate control

Wikelski

Martin

Scheuerlein

et al. 2007

Phil. Trans. R. Soc. B

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“…This enzyme, which converts thyroxine (T 4 ) to 3,5,3 0 -triiodothyronine (T 3 ), implicates local changes in thyroid hormone concentrations in the photoperiodic stimulation of the testes. Lending support to this idea, intracerebroventricular (ICV) infusions of T 3 induce gonadal growth in quail housed in a short day length, whereas infusions of iopanoic acid, a type 2 iodothyronine deiodinase inhibitor, attenuate gonadal growth in long day lengths (Yoshimura et al 2003). Interestingly, MBH mRNA levels of type 3 iodothyronine deiodinase, an enzyme that degrades both T 3 and T 4 , are decreased under long compared with short day lengths, a photoperiodic pattern opposite to that of type 2 iodothyronine deiodinase (Yasuo et al 2005).…”

Section: Photoperiodic Time Measurement (A) Modelsmentioning

confidence: 99%

“…Selective daily illumination of the MBH for 16 h per day stimulates gonadal growth in quail housed under 10L conditions (Ohta et al 1984). Type 2 iodothyronine deiodinase gene expression in the MBH is elevated under long compared to short day lengths (Yoshimura et al 2003). This enzyme, which converts thyroxine (T 4 ) to 3,5,3 0 -triiodothyronine (T 3 ), implicates local changes in thyroid hormone concentrations in the photoperiodic stimulation of the testes.…”

Section: Photoperiodic Time Measurement (A) Modelsmentioning

confidence: 99%

Tracking the seasons: the internal calendars of vertebrates

Paul

Zucker

Schwartz

2007

Phil. Trans. R. Soc. B

175

152

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Animals have evolved many season-specific behavioural and physiological adaptations that allow them to both cope with and exploit the cyclic annual environment. Two classes of endogenous annual timekeeping mechanisms enable animals to track, anticipate and prepare for the seasons: a timer that measures an interval of several months and a clock that oscillates with a period of approximately a year. Here, we discuss the basic properties and biological substrates of these timekeeping mechanisms, as well as their reliance on, and encoding of environmental cues to accurately time seasonal events. While the separate classification of interval timers and circannual clocks has elucidated important differences in their underlying properties, comparative physiological investigations, especially those regarding seasonal prolactin secretions, hint at the possibility of common substrates.Keywords: seasonality; photoperiodism; circannual; interval timers While the Earth remaineth, seedtime and harvest, and cold and heat, and summer and winter, and day and night shall not cease.Genesis 8: 22, King James Version (1611) As the Earth makes its yearly orbit around the Sun, the planet's 23.58 axial tilt leads to the cyclical environmental changes that we call the seasons. Recurrent challenges to the survival of organisms and their offspring arise with the dawning of each new season, and animals have evolved seasonally induced changes in phenotype that adapt them to these predictable events. For example, in many temperate environments, winter is generally characterized by severe decreases in ambient temperature and food availability, leading to increased energetic demands at a time when resources are diminished. Because energy requirements of female mammals typically increase markedly during lactation (Bronson 1989) and newly weaned offspring are particularly vulnerable to environmental perturbations (Hill 1992), raising offspring during this time of year is often futile. Thus, many temperate species have evolved winter-specific behaviours and physiology to conserve energy (e.g. hibernation, a more insulative pelage, huddling) or provide for escape (e.g. migration). Many species also increase the chances of offspring survival by timing their mating behaviours so that parturition occurs during energetically favourable times of year.

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“…Birds have extra-retinal photoreceptors which they use, in conjunction with a circadian clock, to measure photoperiod (Dawson et al 2001). Experimental transfer of birds from a short to a long photoperiod induces neuroendocrine changes within hours (Meddle & Follett 1997;Yoshimura et al 2003) and these lead to gonadal maturation during subsequent days and weeks. The longer the photoperiod is, the greater the rate of gonadal maturation (Farner & Wilson 1957;Dawson & Goldsmith 1983).…”

Section: Introductionmentioning

confidence: 99%

Seasonality in a temperate zone bird can be entrained by near equatorial photoperiods

Dawson

2006

Proc. R. Soc. B.

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Birds use photoperiod to control the time of breeding and moult. However, it is unclear whether responses are dependent on absolute photoperiod, the direction and rate of change in photoperiod, or if photoperiod entrains a circannual clock. If starlings (Sturnus vulgaris) are kept on a constant photoperiod of 12 h light : 12 h darkness per day (12 L : 12 D), then they can show repeated cycles of gonadal maturation, regression and moult, which is evidence for a circannual clock. In this study, starlings kept on constant 11.5 L : 12.5 D for 4 years or 12.5 L : 11.5 D for 3 years showed no circannual cycles in gonadal maturation or moult. So, if there is a circannual clock, it is overridden by a modest deviation in photoperiod from 12 L : 12 D. The responses to 11.5 L : 12.5 D and 12.5 L : 11.5 D were very different, the former perceived as a short photoperiod (birds were photosensitive for most of the time) and the latter as a long photoperiod (birds remained permanently photorefractory). Starlings were then kept on a schedule which ranged from 11.5 L : 12.5 D in mid-winter to 12.5 L : 11.5 D in mid-summer (simulating the annual cycle at 9 8N) for 3 years. These birds entrained precisely to calendar time and changes in testicular size and moult were similar to those of birds under a simulated cycle at 52 8N. These data show that birds are very sensitive to changes in photoperiod but that they do not simply respond to absolute photoperiod nor can they rely on a circannual clock. Instead, birds appear to respond to the shape of the annual change in photoperiod. This proximate control could operate from near equatorial latitudes and would account for similar seasonal timing in individuals of a species over a wide range of latitudes.

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Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds

Cited by 463 publications

References 23 publications

Avian circannual clocks: adaptive significance and possible involvement of energy turnover in their proximate control

Avian circannual clocks: adaptive significance and possible involvement of energy turnover in their proximate control

Tracking the seasons: the internal calendars of vertebrates

Seasonality in a temperate zone bird can be entrained by near equatorial photoperiods

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