ovary-like left gonad; for a period of 5 months it continued to exhibit
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1 EXPERIMENTAL MODIFICATION OF THE ACCESSORY SEXUAL APPARATUS IN THE HEN. By ALAN W. GREEN- WOOD and J. S. S. BLYTH. Institute of Animal Genetics, University of Edinburgh. (Received for publication 6th April 1938.) INTRODUCTION. THE profound effect of the female hormone on the processes of differentiation of the sex glands and the associated accessory sexual apparatus in the developing chick embryo has been demonstrated by several independent groups of workers [Kozelka and Gallagher, 1934; Dantchakoff, 1935; Wolff and Ginglinger, 1935; and Willier, Gallagher, and Koch, 1937]. In the genetically predetermined male embryo the injection of suitable quantities of this substance into the egg prior to the onset of differentiation of the gonads into definitive testes has resulted in the transformation of the left gonad into an ovary or ovotestis. Variation in the amount of hormone administered induced grades of intersexuality. The highest doses employed by Willier et al. [1937], 1 mg. and 2 mg., led to the transformation of the indifferent gonads in the genetic male into left and right ovaries, while such individuals also possessed oviducts "strikingly similar to those of a normal female." In the female embryo subjected to the same treatment no apparent modifications in the normal mode of differentiation of the gonads were encountered, but the accessory sexual apparatus was affected in that both oviducts showed considerable hypertrophy and the length of the right was much increased. (Normally only minute remnants of the latter are present at hatching.) Since, with one exception, all the observations so far recorded have been made on embryos just prior to hatching, it was decided to extend the experiment in order to determine whether functional sex-reversal in the adult would follow the modifications induced in the male embryo by means of administration of female hormone to the incubating egg. The isolated case referred to was that described by Dantchakoff [1936] of a transformed White Leghorn male which at hatching possessed an ovary-like left gonad; for a period of 5 months it continued to exhibit the secondary sexual characters of the female, but subsequently gradually assumed the structures characteristic of its genetic sex. 61
2 62 Greenwood and Blyth Although the primary object of this investigation was a detailed study of the post-hatching behaviour of male birds in particular, certain peculiarities in the reproductive functioning of the mature females derived from the experiment have been encountered and are herein described. TECHNIQUE. Eggs from pure-bred Brown Leghorns of the Institute's flock were injected 48 hours after the commencement of incubation with a standard dose of 1 mg. cestrone dissolved in 1 ml. ethylene glycol, according to the method of Willier et al. [1937]. RESULTS. From 50 eggs injected with cestrone 31 chickens were hatched out, and of this number 21 have been raised to maturity. Classified, when of sufficient age, according to their external sex-dimorphic characters (plumage and head furnishings), 13 were females and 8 were males. Examination of the sexual equipment of the embryos dying during the last week of incubation, as well as that of hatched chicks failing to survive until maturity was reached, indicated that the range of sex abnormalities exhibited was similar to that found by other investigators; the apparent sex ratio obtaining in these two groups was 15 females to 7 males. The occurrence in the whole population of a large proportion of individuals which could be classified as females (28 females, 15 males, and 7 unsexable embryos) suggested, apart from a fortuitous distribution of the sexes in this experiment where small numbers are involved, that either embryonic mortality was confined almost exclusively to males, or that in some cases such extreme grades of sex transformation were induced that genetic males have been classified as females. Willier et al. [1937] found a considerable excess of females when their experimental embryos were sexed by macroscopical examination of the gonads and oviducts (64 females, 44 males), but when the criteria used were a sex-linked plumage character, together with a microscopical investigation of the sex gland tissue, a sex ratio more nearly equivalent to the normal was obtained (29 females, 37 males). The possibility of exposing the original genetic sex of our experimental females through an examination of the sex ratio of their offspring suggested itself, since transformed genetic males (presumably remaining XX in regard to sex chromosome equipment) when mated to normal males should have produced nothing but male progeny. Bi-weekly observations on body weight, comb size, and plumage changes have been made in both experimental and a control group of females from the age of 10 weeks; there was little difference in the
3 Modification of Accessory Sexual Apparatus in the Hen behaviour of the two groups, but the measurements indicated that the former were somewhat slower in maturing. The average age at which members of the control group laid their first egg was 205 days, the individual variation ranging from 193 to 222 days. When the experimental birds were about 5 months old it was noted that one of them exhibited the onset of sexual growth in its comb, which subsequently became erect and "cocky." A laparotomy performed on this bird, J. 2659, revealed on the left side a typical ovary in which the largest developing follicle was approximately 0 4 cm. in diameter. The comb continued to enlarge, and attained a size much beyond that in the mature control hens. This bird produced her first egg when 208 days old, and, while her age at sexual maturity is well within the range exhibited by the controls, her subsequent rate of eggproduction was markedly subnormal, for during the month of February she produced 6 eggs only. The latter are normally shelled, but are otherwise peculiar in being consistently pear-shaped. By 24th January this year (the birds then being 29 weeks old) six of the experimental group had all the outward signs of being in lay-large red combs, full soft abdomen, and widely spaced pliable pelvic bones-but for two weeks from this date no eggs, other than two produced by the female already referred to, J. 2659, were recorded from the pen, although three developed prolapsus of the oviduct. On the 7th February one of the birds, J. 2689, was seen on the floor of the pen straining as if in process of evacuating an egg, and on being handled ejected an egg lacking both membrane and shell, and consisting solely of yolk and albumin. On the same day another, J. 2676, which had been placed in a trap-nest, was found with what appeared to be the remains of a membraned but shell-less egg. In the two succeeding weeks two more shell-less eggs were found in the pen, and the possibility that they were being produced in greater numbers but being lost in the straw litter led to the transfer of the females to individual battery cages. In these the droppings trays were lined with white paper to facilitate the identification of yolk and albumin among the excrement. Within a week after the initiation of this change in husbandry five of the birds were recorded as having laid shell-less eggs either with or without a shell membrane. The birds which had exhibited prolapsus were killed at this time: two were sexually mature and had been shedding eggs into the bodycavity; in the third the ovary was apparently only approaching functional maturity, and, so far as could be ascertained, had not liberated any ripe ova. (This was confirmed by the size of the comb, which at the time of the prolapsus had not yet reached a stable maximum.) In one of the mature birds the prolapse had completely recovered, but in both the others the right oviduct was still inflamed and swollen, while 63
4 64 Greenwood and Blyth the left was perfectly healthy. It is difficult to assess the significance of this phenomenon, since, in view of the complete repair occurring in the first bird, the possibility that the left ducts in the others were also originally involved cannot be excluded. Further examination of the sexual apparatus of these birds exposed structural modifications in the oviduct which made it unlikely that normally shelled eggs could have been produced. It being suspected that these abnormalities would also be present in the hens laying shellless eggs, they too were killed as soon as laying had been recorded and their reproductive tracts subjected to a more detailed examination. FIG. 1.-Showing the relation between the shell gland and the anterior end of the vagina in a normal laying female. It was obvious that the inability to produce normal eggs rendered impossible the determination of their genetic constitution in regard to sex by breeding from them. So far 5 such laying females have been killed and carefully examined: in each of them the left ovary was similar in appearance to that from control hens in full reproductive activity, the number of large, rapidly maturing, yolked ova varying from one to three in the individual birds. The presence of ruptured follicles indicated that the glands had been functioning normally for some time before death. No reproductive tissue was visible macroscopically on the right side, but in all the birds two well-developed and perforate oviducts were found. These were dissected from their muscular attachments so that they could be measured and weighed. A careful examination of the left oviduct in situ indicated a possible cause of the delivery of shell-less eggs by these birds. In the normal female the vagina consists of a much convoluted tube, which from its point of junction with the shell gland forms a well-defined "S" bend (fig. 1). This characteristic appearance is determined by a series of
5 Modification of Accessory Sexual Apparatus in the Hen muscular attachments, and it is only when these are removed that the tube can be straightened out. As will be shown later, the vagina of the experimental females is relatively much shorter, and, seen in situ, shows only a slight tendency to the formation of convolutions; in addition, the characteristic "S" bend at its anterior end is either entirely missing or represented by a slight kinking only (fig. 2). It may be suggested from this series of observations that the function of the peculiarly convoluted anterior portion of the vagina is to prevent the premature passage of the egg through the shell gland before it has received its calcareous deposit. The absence of adequate vaginal flexures in the oviduct of the experimental birds allowed of no resistance to the passage of the eggs through those regions normally characterised by well-developed musculature, the action of which determines the 65 FIG. 2.-Showing the relation between the shell gland and the anterior end of the vagina in an experimental female. Note the absence of vaginal convolutions. movement of the egg, and they were therefore conducted without pause through shell gland and vagina to the exterior. The total length of the oviducts from the experimental birds was considerably less than in normal hens (Table I.): the length in all cases being taken from the beginning of the albumin gland to the point of entry of the duct into the cloaca. In order to determine whether the structural modifications involved all regions, measurements were also taken in some of the birds of its component sections, viz. albumin gland, isthmus, uterus (or shell gland), and vagina. While these regions are clearly delimited in the normal lien they are less readily distinguishable in the experimental birds. This applies particularly to the separation of albumin gland and isthmus; the only instance in which the characteristic non-glandular ring separating these two areas was discernible occurred in the right oviduct of J. 2666, where its posterior margin merged into the tubular a;nterior portion of the uterus and the isthmus seemed to be entirely absent. Because of the difficulty experienced in determining the precise boundaries of the various regions the measurements given may be open to some error, but they are still of value in assessing probable points of difference from the normal. The total length of the oviduct VOL. XXVIII., NO. l
6 66 Greenwood and Blyth TABLE I.-LENGTHS IN CMS. OF COMPONENT PARTS OF THE OVIDUCTS OF EXPERIMENTAL AND CONTROL HENS. Experimental. Total Albumin Isthmus. Uterus. Vagina. No. of length. gland. bird. Left. Right. Left. Right. Left. Right. Left. Right. Left. Right. J (15)t * (6.5)t (28)4 (28)t (8)t (6)t 2.5 Average X Control. J Average ' * t Laying intra-abdominally following prolapsus of the oviduct. Combined lengths of uterus and vagina. Combined lengths of albumin gland and isthmus. is a more reliable measure, since the end points are clearly marked and only a slight error due to the elasticity of the tissues is involved. From the data in Table I. it will be seen that the shortening of the left oviduct in the experimental birds is not restricted to any particular region, and that its component parts are affected almost without exception. Consideration of the weight of the oviducts exposes a complementary phenomenon. (Table II.); the differences in length are paralleled by weight differences, and the total weight of right and left ducts from individuals in the experimental group approximates to that of the single left oviduct of the normal laying hen. (That the average weight of the oviduct in the small control group used here is a fair measure of its behaviour in a relatively large population of this stock was found by reference to data previously collected from 105 laying birds where the average weight was 44-3 g., with a range of variation from 30 to 67 g.)
7 Modification of Accessory Sexual Apparatus in the Hen 67 TABLE II.-WEIGHT OF OVIDUCTS IN EXPERIMENTAL AND CONTROL HENS IN GRAMS. Experimental. Control. No. of bird. Left ovid. Right ovid. Total wt. No. of bird. Left ovid. J *0 J * Average wt * Vagina inflamed as result of prolapsus. DIscUSSION. Apart from the production of abnormal eggs by a number of the experimental females, the significance of which has already been mentioned, the main point of interest deriving from these studies concerns the incomplete differentiation of the oviducts in respect to both weight and form in the sexually mature hen. The investigations of previous workers using this technique have made it clear that, whatever its mode of action, the early injection of cestrone to the incubating egg is capable of retarding those processes normally leading to the more or less complete involution of the right mullerian duct of the female at about the twelfth day of incubation. It has also been possible to prevent the regression of these ducts in the male by modifying the conditions of incubation [Wilier and Yuh, 1928]. The discovery by Juhn and Gustavson [1932] that on rare occasions mullerian duct rudiments may persist in the male beyond the embryonic period, suggests that once the phase of regression has been passed in embryogeny they may continue to persist indefinitely. All the experimental females on which this study is based possessed paired oviducts, but in no instance has complete differentiation and development been attained. Two alternative hypotheses may be suggested for the interpretation of these facts. Allied with the persistence of the paired ducts in the embryo there is, at hatching, marked hypertrophy of both in a number of instances. It may be suggested that the action of the cestrone is not only to prevent the regressive processes in the right duct, but it may also, by premature stimulation, affect adversely the differentiation of the simple tube into the morphologically and histologically distinct regions of the completely developed oviduct, and render it incapable of complete function subsequently.
8 68 Greenwood and Blyth The close approximation of the total mass of the paired oviducts in the experimental females to that of the left in a mature intact female suggests another interpretation. From the behaviour of the oviduct in the female following ovariectomy, or during periods of ovarian inactivity, it is clear that the complete development of the duct is dependent on the presence of the activelv functioning ovary. The results of administration of female hormone to immature chickens [Juhn and Gustavson, 1930] indicated that cestrone is the controlling agent. Both the lapse of time and the quantity of cestrone employed in this experiment make it unnecessary to consider the original injection as responsible for the state of development of the paired oviducts in the experimental birds at the time of autopsy. Their condition, therefore, may be attributed to the action of hormone secreted by the bird itself. It is natural to postulate that the total mass of the paired ducts is a measure of the available stimulation, and that this amount of substance is only sufficient for the complete development of a single duct such as is present in the normal female. If this hypothesis is valid it is interesting to note that the functional oviduct of the normal hen is an instance of a naturally occurring compensatory hypertrophy -a state which is necessary for its efficient functioning. SUMMARY. 1. Peculiarities of form and function in the accessory sexual apparatus of a number of experimental pullets, derived from eggs injected with cestrone at an early stage of incubation, are described and discussed. 2. Only one of a group of 6 females laid normal eggs when sexually mature, the remainder producing eggs devoid of shell or lacking both shell and egg membranes. This phenomenon is ascribed to an abnormality of the oviduct. 3. All the experimental birds autopsied possessed two oviducts which showed incomplete development both as regards total length and length of component parts. 4. The total weight of the two ducts approximated that of the single left oviduct in the normal hen. 5. It is suggested that either the cestrone injection to the egg interfered with the normal processes of differentiation of the mullerian duct into the sex duct in the embryo, rendering it incapable of efficient response to the hormone stimulus subsequently supplied by the functional ovary of the individual, or that the normal level of secretion of female hormone by the fowl's ovary is sufficient only for the complete development of a single duct.
9 Modification of Accessory Sexual Apparatus in the Hen 69 BIBLIOGRAPHY. DANTCHAKOFF, V. (1935). C.R. Acad. Sc. 201, 161. DANTCHAKOFF, V. (1936). "Histoire d'un Coq," Actualite' Sc. et Ind., No. 370, Herman et Cie, Paris. JUHN, M., and GUSTAVSON, R. G. (1930). J. exp. Zool. 56, 31. JUHN, M., and GuSTAVSON, R. G. (1932). Anat. Rec. 52, 299. KOZELKA, A. W., and GALLAGHER, T. F. (1934). Proc. Soc. exp. Biol. N. Y. 31, WILLIER, B. H., and YUH, E. C. (1928). J. exp. Zool. 52, 65. WILLIER, B. H., GALLAGHER, T. F., and KOCH, F. C. (1937). Physiol. Zool. 10, 101. WOLFF, E., and GINGLINGER, A. (1935). C.R. Acad. Sc. 200, 2118.
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