The thyroid and photoperiodic control of seasonal reproduction in American tree sparrows (Spizella arborea)

Abstract

To explore the role of the thyroid gland in the control of seasonal reproduction in obligately photoperiodic American tree sparrows (Spizella arborea), the effects of (1) thyroxine administered in drinking water to thyroid-intact photosensitive or photorefractory birds, and (2) radiothyroidectomy before and after photostimulation and during photorefractoriness were examined. Chronic administration of pharmacological doses of thyroxine induced testicular growth and usually regression in initially photosensitive birds held on short or intermediate daylengths. Some thyroxine-treated birds with regressed testes were absolutely photorefractory, but most remained photosensitive. Exogenous thyroxine never induced testicular growth in photorefractory birds moved to short days, though it often impeded, and sometimes even blocked, the recovery of photosensitivity. Although circumstantial, these effects of exogenous thyroxine are consistent with an hypothesis that assigns to thyroid hormones two roles--one stimulatory and the other inhibitory--in the control of seasonal reproduction. Radiothyroidectomy before photostimulation inhibited (but did not prevent) photoinduced testicular growth, blocked spontaneous testicular regression, suppressed molt, and prevented photorefractoriness. Moreover, as demonstrated by testicular growth after thyroxine replacement therapy, radiothyroidectomy during photorefractoriness later restored photosensitivity despite continued photostimulation. Thus, euthyroidism is an essential condition for maximizing (but not for initiating) photoinduced testicular growth and for triggering and maintaining photorefractoriness in photostimulated tree sparrows. However, when performed early during photostimulation, radiothyroidectomy neither immediately induced nor later blocked spontaneous testicular regression. Thus, endogenous thyroid hormones and long days may interact during a critical period to program a sequence of physiological events that plays out as photorefractoriness in chronically photostimulated birds. Such an organizational event cannot be permanent, for seasonal reproduction is episodic and its control mechanism necessarily cyclic. Because thyroidectomy simulated the well-known restorative effect of short days (and exogenous thyroxine impeded it), short days may dissipate photorefractoriness by creating a milieu wherein thyroid hormones are deficient or inactive.

A Thyroid Hormone Antagonist That Inhibits Thyroid Hormone Action in Vivo

“…Beyond anuran metamorphosis, thyroid hormone has been implicated in a wide range of important biological processes in organisms that lack an available genetic approach. These include direct and indirect development of amphibians and fish (28 -31), the control of photoperiodism in seasonally breeding birds (32), and smoltification of salmonids (33,34), all of which can be explored in more mechanistic detail using NH-3. Finally, our results clearly demonstrate the degree of structural and functional relatedness between the mammalian and amphibian TRs and further underscore the usefulness of the amphibian model for identifying biologically active nuclear receptor ligands.…”

Effect of Withdrawing Long Days from Male American Tree Sparrows (Spizella Arborea): Implications for Understanding Thyroid-Dependent Programming of Seasonal Reproduction and Postnuptial Molt1

“…In addition, each of the 18 primary flight feathers was assigned a molt score using Newton's [25] scale of 0 (old) to 5 (new). Because neither testicular growth nor molt occurs in photosensitive tree sparrows held on short days [14,18], testis lengths and molt scores recorded at Week -1 reflect testicular condition and molt status at Week 0, at which time one group of males (short-day controls) was retained on 8L: 16D and seven groups (including long-day controls) were moved to 20L:4D. One day, 4 days, 1 wk, 2 wk, 3 wk, and 4 wk later, a separate group of males was evaluated for testis length, scored for molt, and returned to 8L:16D for 7 -n wk (i.e., for a period ranging from 6.86 wk [after 1 day on 20L:4D] to 3 wk [after 4 wk on 20L:4D]); longday controls remained on 20L:4D for 7 wk.…”

“…Our studies on obligately photoperiodic American tree sparrows (Spizella arborea) lead us to conclude that THs and long days interact to program males for the vernal component of seasonality, as well as the autumnal component [12,[14][15][16][17][18]. By performing thyroidectomy (THX) before, at, or after the onset of photostimulation, we have demonstrated that programming for testicular growth occurs during the first week of photostimulation [16,18] and is independent of programming for photorefractoriness and postnuptial molt, which occurs between Weeks 1 and 3 [15,16,18].…”

“…In previous experiments [14][15][16]18], we tested this model by withdrawing THs by THX before, at, or after the onset of photostimulation. Here we test it by withdrawing long days at times suggested by studies on thyroid-dependent programming in photostimulated male tree sparrows [15,16] and by Wingfield's [22] observation that a single long day stimulates gonadal growth in song sparrows.…”

Clues from wildlife to create an assay for thyroid system disruption.

“…Photorefractoriness, "a reversible state of unresponsiveness to gonado-stimulatory daylengths," initiates and then terminates breeding in photoperiodic species of birds (32). Preventing migrating species from breeding out of season is especially critical for their survival.…”