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Avian EndocrinologyA Dawson & C M Chaturvedi (Eds)

Copyright 2001 Narosa Publishing House, New Delhi, India

Photoperiodic control of seasonal reproduction: neuroendocrine mechanisms and adaptations

P Deviche and T Small

Department of Biology, Arizona State University, Tempe, AZ 85287-1501, USA

Introduction

Over 75 years ago, Rowan (51) used dark-eyed juncos, Junco hyemalis, to demonstrate that changes in ambient photoperiod can profoundly affect the activity of the reproductive system. Many subsequent investigations have confirmed and extended this original finding. It is now established that, in many birds living at middle and high latitudes, exposure to long days (LD, approximately 12 or more hours of light) stimulates the hypothalamo-pituitary-gonadal axis, increasing the secretion of gonadotropins (luteinizing hormone, LH; follicle-stimulating hormone, FSH), and induces gonadal growth (54, 56, 62). It is also known that in most species, prolonged exposure to LD does not maintain the activity of the reproductive system indefinitely: The system eventually ceases to respond to LD and regresses. This phenomenon is called photorefractoriness.

The hypothalamic peptide, gonadotropin-releasing hormone (GnRH-I, hereafter referred to as GnRH; review, 11), plays a pivotal role in mediating photoinduced reproductive development and in inducing the ensuing gonadal regression that results from photorefractoriness. The amount of GnRH in the hypothalamus, as assessed by semi-quantitative immunocytochemistry or radioimmunoassay, is high in photosensitive birds exposed to short days (SD) or LD, is greatly depressed in chronically photorefractory birds when compared to photosensitive birds, and is increased following subsequent exposure to SD and re-establishment of photosensitivity (12, 13, 14). The mechanism that mediates alterations in GnRH-secreting cell function when birds become photorefractory is poorly understood. Little is known also on the contribution of changes in GnRH production versus release to the regression of the reproductive system observed in photorefractory birds. Not all species show similar responses to day length with respect to the

114 Avian Endocrinology

timing and extent of photorefractoriness, and in fact pioneering investigations by Farner and colleagues (21) suggested that photorefractoriness evolved more than once in birds.

In this article, we compare some well-studied experimental models in terms of events occurring at the time of photorefractoriness with particular emphasis on changes in GnRH activity. We use this information to discuss how photorefractoriness may affect GnRH production and release differently across species.

Photoinduced reproductive development and regressionIn most avian species, the elevated activity of the reproductive system that characterizes the breeding period is influenced by multiple environmental factors such as day length, temperature, food availability, mates in appropriate physiological condition, and a suitable breeding habitat (63). Of these factors, day length has been shown in many cases to be of paramount importance. Even desert species, such as zebra finches, Taeniopygia guttata, that are thought to time breeding as a function of rainfall and have traditionally been considered non-photoperiodic, increase their reproductive system activity when exposed to very long day length in captivity (2). Day length also influences the reproductive physiology of spotted antbirds, Hylophylax naevioides, a sedentary tropical species that is naturally exposed to relatively small annual changes in photoperiod (32). Thus, the reproductive system of most, and perhaps all, birds living over a wide range of latitudes from arctic regions to the tropics (59) can presumably respond to changes in day length.

Photic information affecting the avian hypothalamo-pituitary axis is conveyed to this axis by extra-ocular and extra-pineal brain receptors (60, reviews, 34, 44) that are generally referred to as deep encephalic receptors. These receptors are believed to be located in or close to the lateral septum and the tuberal hypothalamus regions of the brain (39, 64). In pigeons, Columba livia, encephalic photoreceptors have biochemical characteristics resembling those of retinal rod/cones (58). Neither the exact identity of these receptors nor their anatomical or functional relationship with GnRH cells is known.

In typically photoperiodic species, photorefractoriness develops during the summer, when day length is still well in excess of that necessary to stimulate vernal gonadal development. Thus, a characteristic of these species is that photoinduced cycles of gonadal recrudescence followed with regression are asymmetrical with respect to the summer solstice. Photoinduced gonadal regression in summer is considered adaptive for at least two reasons. First, it curtails reproduction in anticipation of a seasonal deterioration of ambient

Photoperiodic control of reproduction Deviche and Small 115

conditions. Second, it permits the expression of other aspects of the annual cycle including postnuptial molt, fattening, and migration, which are energetically or otherwise incompatible with reproductive activities (15, 35, 45). Photorefractoriness is mediated centrally and is not consequent to an increased negative feedback of gonadal steroids on the hypothalamo-pituitary axis or to an inability of the anterior pituitary to respond to GnRH (38, 44). As discussed below, species may differ with respect to the neuroendocrine events occurring at the end of the breeding period, raising the question of whether there are fundamental species differences in the processes that cause and possibly maintain photorefractoriness.

Absolutely photorefractory speciesAt the end of a photoinduced gonadal cycle, species, such as the European starling, Sturnus vulgaris, the house finch, Carpodacus mexicanus, the dark-eyed junco, the white-crowned sparrow, Zonotrichia leucophrys, and the male American tree sparrow, Spizella arborea, become absolutely photorefractory. The photorefractory condition in these species persists as long as birds remain exposed to LD. Dissipation of photorefractoriness, i.e. restoration of photosensitivity as determined by the ability to respond to LD with increased GnRH release, requires exposure to SD. The neuroendocrine changes that result from photorefractoriness have been examined in greatest detail in European starlings. Photorefractoriness in starlings is associated with decreased size and immunostaining intensity of hypothalamic GnRH perikarya, but fiber staining in the median eminence does not decline until gonadal regression is nearly complete (26). Reduced GnRH production in starlings, therefore, constitutes an early indication that birds have become photorefractory. At this time some GnRH may still be released into the anterior pituitary, but not in amounts sufficient to sustain elevated gonadotropin secretion and gonadal function. Consistent with the idea that photorefractoriness in starlings inhibits GnRH production prior to necessarily inhibiting the GnRH release mechanism, males sampled during gonadal regression had reduced hypothalamic, but not median eminence, expression of the precursor molecule for GnRH (proGnRH-GAP) and of GnRH itself, compared to photostimulated males (47). Median eminence staining for both peptides was reduced only after regression was complete. The mechanism mediating the decrease in GnRH production when birds become photorefractory is not known. Parry and Goldsmith (46) found that GnRH cells of photoregressed starlings receive increased synaptic input compared to cells of birds that were undergoing photoinduced gonadal maturation. However, no such increase occurred until gonadal regression was complete. Thus, changes in synaptic input to GnRH cells may contribute


to maintaining starlings in the photorefractory state, although they are probably not responsible for inhibiting the production of GnRH that is an early consequence of photorefractoriness.

Less is known about the neuroendocrine changes associated with the onset of photorefractoriness in other species. We recently investigated this question in adult male dark-eyed juncos obtained from a subarctic population. Juncos become photorefractory at the end of June, after exposure to photoperiod exceeding 12 h (12 L) for approximately four months. At this time LH concentrations and testis mass decline rapidly (20), but this decline is not coupled to changes in the numbers of hypothalamic proGnRH-GAP or GnRH cells, which do not differ from those of fully photostimulated and photosensitive juncos (41). Similar observations have been made in white-crowned sparrows (Meddle, personal communication). They suggest that in these species, and contrary to the situation in starlings, the decrease release of GnRH that is observed in photorefractory birds does not result from decreased hypothalamic production of the peptide. A recent investigation on white-crowned sparrows extended this conclusion by investigating whether photorefractory birds can acutely release physiologically effective amounts of GnRH in response to pharmacological stimulation by the excitatory glutamate agonist, N-methyl-D-aspartate (NMDA; (40)). NMDA is thought to stimulate LH release by acting on GnRH-secreting neurons (33). An injection of NMDA to photorefractory sparrows with partially regressed testes rapidly increased plasma LH. This treatment had a similar effect on LH when given to photostimulated sparrows, suggesting that photorefractoriness in these birds (and in juncos) does not deplete hypothalamic GnRH stores.

If photorefractoriness in juncos and sparrows caused an inhibition of the GnRH release mechanism without concurrently depressing the peptide production, GnRH would presumably accumulate in hypothalamic cells. GnRH would then be found in higher amounts in photorefractory birds than in photostimulated birds. That this has not been observed using immunocytochemical methods suggests that decreased GnRH release must somehow be coupled to declining GnRH production, as is the case in starlings. Further experimentation, perhaps using methods other than immunocytochemistry, is warranted to test this hypothesis and to evaluate the extent to which changes in GnRH production and release are temporally related as birds of various species become photorefractory or regain photosensitivity. Research into the above questions will also benefit from investigations on the extent to which changes in hypothalamic GnRH expression follow changes in the synthesis of proGnRH-GAP or the conversion of this peptide to GnRH.


Photorefractoriness in absolutely photorefractory birds kept on LD for a prolonged period is generally associated with low hypothalamic GnRH stores as measured by immunoreactive GnRH cell numbers or sizes, intensity of immunostaining in these cells, or numbers or densities of immunoreactive fibers (19, 52). The time course of this decrease has not been determined, and we do not know to what extent it results from intracellular degradation of GnRH or release of the peptide in small amounts that do not induce a significant secretion of gonadotropins.

Relatively photorefractory speciesThe Japanese quail, Coturnix c. japonica, has proved to be an exceptional model for many elegant studies on photoperiodic responses (reviews, 22, 24). As is the case for absolutely photorefractory birds that have regained photosensitivity, transfer of Japanese quail from SD to LD rapidly activates the hypothalamo-pituitary-gonadal axis (23). Similarly, the reproductive system of European quail, Coturnix coturnix, exposed to natural photoperiod recrudesces when day length exceeds approximately 12L (3). In contrast to the situation in absolutely photorefractory species, Japanese quail that are chronically exposed to fixed artificial LD do not undergo spontaneous gonadal regression, which in this species requires some decrease in day length. In European quail exposed to a natural photocycle, gonadal regression likewise occurs in late summer, when photoperiod has declined from 18L: 6D to about 14L: 10 D (3). Further, gonadal recrudescence in SD-regressed quail starts immediately after transfer back to LD and is not preceded by a period of unresponsiveness to LD (50). Quail are for this reason said to be relatively photorefractory. Note that the definition of relative photorefractoriness in quail differs from that in another species, the house finch (31). Male house finches exposed to summer photoperiod become absolutely photorefractory. The period of absolute photorefractoriness in this species last for about 45 days and naturally ends in September, when finches start to regain photosensitivity as measured by their capacity to recrudesce testes in response to LD. During this period birds are said to be relatively photorefractory because exposure to day length exceeding, but neither equal to nor shorter than that to which they were previously exposed, is necessary to stimulate gonadal development. Male finches exposed to natural photoperiod and sampled at the end of October, when they had presumably regained photosensitivity to very long days and were relatively photorefractory, had reduced brain GnRH expression compared to breeding birds (6).

The neuroendocrine events associated with photostimulation in quail have been studied in considerable detail (7, 39, 48), but the changes in GnRH function taking place during relative photorefractoriness are


not well known. Foster et al. (25) found GnRH expression in brain regions including the preoptic area of quail exposed to SD for 25 days and with regressed gonads to be higher than in chronically LD-exposed birds. GnRH release in these birds may cease following transfer to SD, allowing the peptide to accumulate within brain cells.

The question of whether absolute and relative photorefractoriness, as defined in the quail, represent extremes of a continuum or two fundamentally different mechanisms has been debated by several authors (10, 29, 44) and remains unsolved. This issue has been addressed by investigating species, such as the house sparrow, Passer domesticus, that may not strictly follow the above-described pattern of absolute or relative photorefractoriness. Male house sparrows exposed to LD for a sufficiently long time become photorefractory, as shown by the fact that their GnRH expression declines and their gonads regress (10, 29). Further, males exposed to LD (17L: 7D) in September do not respond to these LD (49), indicating that they are absolutely photorefractory. However, males that are exposed to LD until around the summer solstice, and then to artificially declining day length, can exhibit gonadal regression earlier, and changes in brain expression of GnRH that are intermediate, compared to birds not exposed to declining photoperiod (8, 29). Changes in gonad size in sparrows transferred from LD to shorter day length thus resemble those seen in quail and superficially consistent with the idea that sparrows become relatively, and then absolutely photorefractory. To test this hypothesis, sparrows were photostimulated by exposure to 18L: 6D and then transferred to shorter photoperiod (16L: 8D or 13: 11D) either after or before the onset of testicular regression (10). Testicular regression rate in birds transferred to shorter photoperiod after regression had begun was accelerated compared to that of males that became absolutely photorefractory as a result of continued exposure to 18L: 6D. In contrast, transfer from 18L: 6D to a shorter photoperiod before the onset of gonadal regression did not affect regression. The data suggest that photorefractoriness is programmed well in advance of testicular regression, as is the case in white-crowned sparrows (42). The results also argue against a period of relative photorefractoriness preceding absolute photorefractoriness, supporting the view that absolute and relative photorefractoriness represent two distinct mechanisms and not extremes of a continuum.

Temporally flexible speciesPhotoperiod does not play an equally important role in the control of breeding cycles in all species, some of which in fact exhibit considerable reproductive flexibility and have extended or irregular breeding cycles (30, 36). Flexibility is, for example, observed in species that live at low


latitudes and are normally exposed to small annual changes in photoperiod compared to those residing at middle or at high latitudes. Also, species, such as zebra finches, that inhabit xeric environments where rainfall is rare and sporadic, may retain the capacity to respond to changes in day length (2), but use primarily non-photic stimuli such as precipitation and/or environmental changes associated with rainfall to time their breeding activities.

The neuroendocrine bases of reproduction in temporally flexible species have been best studied in crossbills (red crossbill, Loxia curvirostra; white-winged crossbill, L. leucoptera). Crossbills feed primarily on conifer seeds (1, 43), the production and availability of which undergo large and irregular fluctuations from one year and one region to another. The birds have adapted to this temporal and geographical unpredictability by adjusting their breeding period to the food supply. As a result, crossbills can breed throughout a large portion of the year, starting at the end of winter and ending in late summer (16-18, 28). It should be noted that even though crossbills have a longer reproductive period than most middle and high latitude passerines, they exhibit a well-defined seasonal reproductive pattern. They rarely breed during autumn, when they are molting and their gonads are regressed, even if their preferred food is locally abundant (16, 18, 28).

Seasonal changes in reproductive physiology in crossbills do not result only from changes in food supply, because captive birds exposed to a natural photocycle simulating natural conditions and receiving food ad libitum exhibit seasonal cycles of plasma LH, gonadal size, and molt (27). In these birds, testes recrudesce and circulating plasma LH increases in the spring, concurrent with increasing day length. LH levels decrease and gonadal regression occurs at the end of the summer and early autumn (July-August), when molt begins. These results on captive crossbills are consistent with data on free-living conspecific birds (17, 28), generally resemble those obtained in other passerines, and suggest use of photoperiod to time reproductive recrudescence and regression. Indeed, male red crossbills that were transferred from SD to LD had higher circulating LH levels and enlarged testes compared to males held on SD (27, 57). These studies also revealed two important aspects of the crossbill reproductive physiology.

First, photoinduced LH secretion and testis mass development were attenuated, although not eliminated, in chronically food-restricted compared to ad libitum-fed and LD-exposed males, indicating an important stimulatory effect of a non-photic cue – food availability – on the reproductive system. Consistent with this observation, free-living white-winged crossbills started to breed at the end of the winter, i.e. when photoperiod was considerably less than 12L: 12D, following a


summer of high conifer seed production (18). In contrast, after a summer of poor seed production, few or no birds bred locally until the following summer, when a new crop of seeds became available.

Second, male red crossbills exposed to constant LD for over four (57) or five (27) months did not become photorefractory, retaining large gonads and elevated LH. In contrast, the gonads of captive birds held at constant thermoneutral temperature, receiving food ad libitum, and exposed to photoperiod simulating the natural cycle regressed after exposure to day length exceeding 12L for approximately four months (27). The failure of gonads to spontaneously regress despite continued exposure to LD suggests that crossbills are relatively photorefractory: Gonadal regression in the fall may require a decrease in day length, as is the case in quail. Thus, crossbills apparently differ from other temperate region passerines studied so far, which terminate breeding as a result of absolute photorefractoriness.

Only one study has investigated the GnRH system of crossbills (37). Here, captive male white-winged crossbills were held on a naturally changing photoperiod and sacrificed in May, when they had large testes, and then in October and January, when testes were small. It was found that brain expression of GnRH underwent relatively small temporal changes; the intensity of cellular immunostaining for GnRH was lower in October than at other times, but neither the number of GnRH cells nor the brain area containing GnRH fibers changed seasonally. Thus, crossbills in the fall presumably retain relatively high brain GnRH levels, but also have regressed gonads and low circulating testosterone concentrations (18), suggesting that GnRH is not released. At this time they rarely breed even in the presence of an abundant food supply (16, 18, 28). In contrast, breeding can occur at the end of the winter, when the food supply is not greater and day length is equal to or shorter than in the fall, but brain GnRH content is presumably about the same. What mechanism then prevents regular fall breeding by these birds?

One hypothesis is that non-photic stimuli such as food and possibly social factors must be present to induce release of GnRH at concentration sufficient to fully activate the reproductive system, and the sensitivity of the GnRH system to these stimuli varies seasonally. Accordingly, birds have a low sensitivity to non-photic stimuli at the end of the summer and during early fall, shortly after they have completed a breeding cycle. At this time GnRH is present in hypothalamic cells, but is not released in amounts sufficient to stimulate substantial LH and FSH secretion. Thus, the reproductive system remains quiescent. With time spent on SD during fall and early winter, birds become increasingly sensitive to non-photic cues. If an adequate food supply remains


available, reproductive development starts and a breeding cycle is initiated although day length may be shorter than in autumn and not yet increasing. Consistent with this idea, free-living male white-winged crossbills sampled during a fall and winter when spruce seeds were abundant had elevated circulating LH and testosterone in November and December, respectively, when day length was less than 8L and decreasing (18). Crossbills that breed at the end of winter and early spring can perhaps continue to do so during summer, when they are photostimulated by LD, and pending the availability of sufficient food (18). At this time and with the occurrence of shorter days, gonads finally regress and molt begins. Prolactin is a likely candidate in the mediation of autumnal gonadal regression. Secretion of prolactin in free-living male white-winged crossbills gradually increases during summer and early fall (18). The increase is presumably photoinduced, as has been found in other species that terminate breeding by developing relative (4) or absolute (9, 53, 55) photorefractoriness. Prolactin is not considered to cause photorefractoriness (review, 34), but it exerts antigonadal effects (5, review, 53) and in European starlings has been implicated in the control of postnuptial molt (13).

Fig. 1 presents a generalized model of the relative roles of photoperiodic and non-photoperiodic factors in the development of the reproductive system in temporally flexible breeders. It is assumed that GnRH is present in the brain year-round, but its release in amounts sufficient to effectively stimulate the pituitary-gonadal axis above a minimum threshold depends on the additive effects of photoperiodic and non-photoperiodic (food quality and availability, precipitation or factors associated with rainfall, etc, depending on the species) factors. When gonads are regressed at the end of a breeding cycle (e.g. autumn), the GnRH system is resistant to stimulation, and GnRH is normally not released in significant amounts. The sensitivity of the GnRH system to stimulation by these factors then gradually increases (e.g. late winter) and reproductive development can occur if non-photoperiodic factors provide sufficient stimulation, even though photoperiod is short and by itself ineffective. Finally, the stimulatory influence of photoperiod becomes sufficiently strong (e.g. summer) to induce reproductive development despite weak, but still necessary stimulation by non-photoperiodic factors.

It should be noted that the proposed role of non-photic factors on the GnRH system may not differ fundamentally from that used by typically photoperiodic and less flexible species which time reproductive development based primarily on day length. In these species, restoration of photosensitivity after absolute photorefractoriness is gradual, a function of the time spent on SD (61), and associated with a build up of


hypothalamic GnRH stores (12). Once photosensitivity has been partially or completely regained, release of these stores is induced most easily by exposure to sufficiently long days. Species that breed on a flexible schedule have retained sensitivity to photoperiod in that LD activates their reproductive system, but in addition they have evolved an unusually high sensitivity to specific non-photoperiodic factors. By responding reproductively to these factors even when photoperiod is very short, such as at the end of the winter, crossbills, for example, can take advantage of a specialized resource, conifer seeds, which is frequently available in sufficient amount on an irregular temporal and spatial basis.

Fig. 1 Schematic representation of the relative contributions of photoperiod (lower part of columns) and of non-photic cues (upper part of columns) to the development of the reproductive system in temporally flexible species. The figure shows the minimum threshold that need to be reached for stimulation of the hypothalamo-pituitary-gonadal axis in response to day length and to two levels (low, high) of non-photic stimulation. See text for further information.

ConclusionsA lot of our current knowledge on the neuroendocrine bases of avian photoperiodism is derived from investigations on a few well characterized and absolutely photorefractory species. Investigations on species such as quail, as well as examination of the natural diversity of avian reproductive patterns (36), suggest that photoperiod is critical to


the activity of the hypothalamo-pituitary-gonadal axis. However, strict reliance on photoperiodic information to regulate seasonal reproductive cycles, although probably widespread, is not the only, and perhaps not the most common, mechanism used by birds. Recent and limited work on species, such as crossbills, that reproduce on a flexible and variable seasonal schedule, has revealed that environmental stimuli other than photoperiod can profoundly affect the reproductive system. Much remains to be discovered about the very nature of these stimuli, their interaction with photoperiod in the control of the activity of the hypothalamo-pituitary-gonadal axis, and the neural pathways by which they affect neuroendocrine functions, in particular the GnRH system.

It has long been known in photosensitive birds that the threshold for physiological responses to photic information, and the magnitude of these responses, is not constant, but rather variable. This threshold is higher in birds that have just regained photosensitivity than in birds that are fully photosensitive as a result of prolonged exposure to SD. Recent data on crossbills, which can also respond to photoperiod, suggest that the same applies to non-photic cues. Accordingly, gonadal cycles in species exhibiting reproductive plasticity must be considered to result from complex interactions between photoperiod and non-photoperiodic factors to which these species are sensitive, but also from the temporally variable impact of these factors, itself a function of the physiological condition of the individual.

AcknowledgmentsThe authors thank Dany Pierard and Michael Moore for comments on an early version of the manuscript, and Christy Strand and Madhusudan Katti for valuable discussions during its preparation.

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