Seasonal changes in some endocrine organs of the vole (Microtus agrestis)

Considerable progress has been made in determining the factors in the environment which are responsible for the control of seasonal breeding in mammals and birds. There is less information available about how these factors produce their physiological effects. Light has been shown to be very important in the control of vole breeding seasons. Temperature may also have some effect. How these factors act is not known. As part of an attempt to understand how the breeding season of the vole is controlled, an investigation of some of its endocrine organs has been undertaken.
Animals have been collected from the field in mid-summer (at the height of the breeding season) and in mid-winter (during the non-breeding period). A total of 174 adult field animals has been studied. As an approximate indication of the reproductive and endocrinological state of the animals, measurements have been made of the weights of their bodies, adrenals, thyroids, gonads and also certain accessory organs (the uteri of females in winter and the seminal vesicles and ventral prostates of males in both summer and winter). From the examination of this data it is clear that there are considerable endocrine changes with season. Furthermore, within both winter and summer populations reproductive sub-groups which show endocrine differences can be recognized. More detailed study of these endocrine differences has involved the use of cytological and histological methods.
Because of the trophic control which the adenohypophysis exercises over the other endocrine organs, it may be presumed to be important in bringing about seasonal changes. It has, therefore, received particular study. The adenohypophyses of field animals have been examined by the methods of cytology, histochemistry and bioassay. In order to identify the cells responsible for the production of gonadotrophin and thyrotrophin, the pituitary function of laboratory bred animals has been altered by castration and the administration of goitrogens.
In the adenohypophysis of the vole five cell types have been recognized.
Oval basophils which are periodic acid-Schiff (PAS) positive and aldehyde fuchsin (AF) negative. They react to castration by degranulation and the subsequent formation of colloid filled castration cells. They are considered to secrete gonadotrophins. In field animals it has been found that the gonadotrophin producing cells (gonadotrophs) of winter animals are markedly different from those of summer animals. The gonadotrophin content of the pituitaries of male voles in winter and in summer has been studied by means of bioassay. In the summer the vole pituitary contains well granulated gonadotrophs and gonadotrophic hormone can be detected. In winter the gonadotrophs are vesiculated and no gonadotrophic hormone can be detected. This indicates that the granulated gonadotrophs contain hormone, but that the vesiculated cells are depleted of active gonadotrophic principles.
Angular basophils which are PAS positive and AF positive. They react to the administration of goitrogen by the formation of colloid filled thyroidectomy cells. They are considered to secrete thyrotrophin. They show no marked changes with season, as would be anticipated from the lack of marked change in the thyroid itself.
Round acidophils which show no marked change with season. This study provides no indication as to their function.
A second type of acidophil which is numerous and well developed only in females which are pregnant or show signs of mammary development. It is suggested that they may be the source of prolactin.
The adenohypophysis also contains a few large cells with poor staining qualities. They do not show any marked changes with season or in response to either castration or the administration of goitrogens. Their function is not known.
The gonads were, in general, found to exhibit the expected seasonal change in activity. Sexually inactive males in winter may be divided into two groups on the basis of the structure of the tunica albuginea. It is suggested that these two groups represent, respectively, regressed males, which were sexually active in the preceding summer, and inhibited males, which were born late in the season and have never been sexually active. Similarly, on the basis of uterine weight, female voles in winter can be divided into two groups, parous and non-parous. The pituitary cytology of regressed and inhibited males, parous and non-parous females in winter is similar.
In one winter collection the males show considerable evidence of being sexually active. This suggests the operation of a factor or factors other than light and temperature in the control of vole breeding seasons. These males were distinguished from the males in other winters by differences in pituitary cytology.
The study of the pituitary suggests that gonadal changes at the end of the breeding season are secondary to changes in the pituitary. The alternative possibility, that the gonads are not competent to respond to pituitary hormones, was tested experimentally. Commercial gonadotrophins were injected into winter field animals and into laboratory bred animals whose sexual development had been inhibited by maintaining them on short days in the cold. The results suggest that the gonads of such animals are able to respond to gonadotrophins.
The adrenal has been found to undergo marked changes in weight with season. In summer there is also a sex difference in adrenal weight. These weight changes can be correlated with striking histological differences in the inner regions of the adrenal cortex. In winter voles the adrenal cortex possesses a juxtamedullary zone. It is similar in cytological appearance to the X zone of mice and the two zones are seemingly homologous. The zone is present in all winter field voles, whether regressed or inhibited males, parous or non-parous females. The zone is small or absent in the adrenals of sexually active males. It must, therefore, be formed secondarily in the adrenals of regressed males. It also reappears in a similar, though not identical, form in males after castration. The zone can also disappear from females, but is present in an especially well developed form in all pregnant and lactating animals. Multipara and primipara differ in the details of the structure of the juxtamedullary zone. These changes are clearly related to sexual activity, but their significance is not known.
The epithelium lining the ventral prostate is the site of marked stimulation in winter field males and in castrated laboratory animals. It is possible that the adrenal is the source of the hormone responsible for this stimulation.
The zona glomerulosa and zona fasciculata of the adrenal cortex also show cytological and histological change with season. Their structure in the winter males which may have been sexually active suggests that these changes are not primarily related to sexual activity.
The principal conclusions which can be drawn from this study are:
That in the vole there is functional differentiation of adenohypophyseal cells. Two cell, types have been recognized which are clearly related to the production and secretion of gonadotrophic and thyrotrophic hormones, respectively. A third cell type is probably the source of prolactin. There is no evidence available on the function of the other two cell types which have been recognized.
That the cessation of breeding in winter in the vole is apparently brought about by a cessation of both the synthesis and the secretion of gonadotrophin.
That there are striking changes in the juxtamedullary region of the vole adrenal which appear to be related to sexual activity.