epididymis of the indian wall lizard (hemidactylus flaviviridis) during the sexual cycle and in...

JOURNAL OF MORPHOLOGY 191:151-160 (1987)

Epididyrnis of the Indian Wall Lizard (Hemidactylus fkviviridis) During the Sexual Cycle and in Response to Mammalian Pituitary Gonadotropins and Testosterone

SHAMIM HAIDER AND UMESH RAI Department of Zoology, Banaras Hindu University, Varanasi, 221005, India

ABSTRACT The histology and histochemistry of the epididymis of the Indian wall lizard Hemidactylus flaviviridis (Ruppell) was studied in normal and hormone-treated males. The ductus epididymidis showed a considerable variation in epithelial cell height and lumenal diameter along its length. It can be divided approximately into anterior, middle, and posterior regions. Epithelial cell height was maximal in the middle region and minimal in the posterior region. The lumen of the ductus epididymidis increased markedly in diameter from anterior to posterior ends with a concomitant increase in the sperm density. During the breeding phase, epithelial cell height and lumenal diameter of both ductuli and ductus epididymidis become markedly enlarged. The epithelium of reproductively active ducts was filled with secretory granules. Both the secretory granules of the epithelium and the secretory material mixed with sperm in the lumen showed a positive reaction to Sudan Black-B, indicating the presence of lipid. The relative effects of mammalian FSH and LH on the regressed epididymis revealed that only FSH was capable of stimulating the growth and secretory activity of the epididymis.

In mammals the ductus epididymidis can be morphologically and histologically divided into three distinct areas: the head (caput epi- didyrnidis), the body (corpus epididymidis) and the tail (cauda epididymidis). In reptiles, un- like mammals, the ductus epididymidis does not exhibit any morphological regional differ- entiation. Although the histology of the ductuli epididymidis and ductus epididymidis and their cyclical changes have been described in several reptilian species (review by Fox, '77), no report is available dealing with histological changes in diEerent regions of the ductus epididymidis.

Studies involving hypophysectomy and gonadotropin replacement clearly indicate that the pituitary gonadotropins in reptiles, as in other vertebrates, are essential for testicular androgenesis (Licht, '74, '84; Licht and Pap- koff, '74; Farmer et al., '75; Licht et al., '76, '77; Lofts, '78; Callard and Mei Ho, 'go), but it has not yet been confiirmed whether folli- cle-stimulating hormone (FSH) or luteinizing hormone (LH) or both are responsible for this stimulation of the testicular androgens, which in turn regulate the growth and secretory activity of the epididymis.

Most investigators have confined them- selves to reporting the modifications of the reptilian epididymis following castration and testosterone replacement therapy (Ramas- wami and Jacob, '63; Prasad and Sanyal, '69; Dufaure and Gigon, '75; Gigon-Depeiges and Dufaure, '77; Depeiges et al., '81; Akbarsha and Balasubramanian, '83; Haider, '85). Very little research on the differential effects of mammalian gonadotropins on this organ has been reported (Eyeson, '71; Jones, '73; Ange- lini et al., '78). In the present study the changes taking place in the ductuli epididymidis and varioq regions of the ductus epididymidis in reproductively active and in- active Indian wall lizards have been investigated. An attempt was also made to show the relative effects of mammalian gonadotropins on the histology and histochemistry of the ductus epididymidis.

MATERIALS AND METHODS

The seasonal cycle of the epididymis of Hemidactylus flaviviridis (Ruppell) may be divided into three phases: (1) a quiescent phase (June-August), (2) a recrudescent phase (September and October), and (3) an

0 1987 ALAN R. LISS, INC.

S. HAIDER AND U. RAI 152

active phase (November-May). The lizards pass through the winter months of Decem- ber-February in a state of quasidormancy. They emerge from their hideouts in early March and copulate during late March and April (Dutta, '46; Sanyal and Prasad, '67). In order to study the seasonal histological and histochemical changes, ten lizards collected from their natural habitat in Varanasi, In- dia, were killed in the months of April (reproductively active) and June (sexually quiescent).

For experimental study, 100 adult male lizards (averaging 7 gm in body weight) were obtained from a local supplier in the last week of June. They were acclimated to labo- ratory conditions for a week (ambient tem- perature: minimum 25.6 f l.O°C, maximum 32.8 +- 1.7"C) and were fed housefly maggots ad libitum. The lizards were divided into four groups of 25. The first two groups received i.p. injections of 30 pg of either purified FSH (NIH-FSH-S 11 ovine) or 30 pg of LH (NIH- LH-S19 ovine) on alternate days, respectively. The third group received, on alternate days, i.m. injections of 30 pg testosterone (17~-hydroxy-3-oxo-4-androstene, Sigma Chemical Company, U.S.A.). The fourth group of untreated lizards were kept as controls. A minimum of five experimental ani- mals were killed after 7, 15, and 21 days, each thus receiving a total quantity of 120 pg, 240 pg, and 330 pg of the respective hormones. The epididymis from one side of each animal was fixed in Bouin's fluid and pro- cessed for routine histological study. The other epididymides were used for histochemical demonstration of lipid by the Sudan black-B (SB) technique (Pearse, '68).

As an index of androgenic activity, the epithelial cell heights of the epididymis were measured by means of an ocular disc and a stage micrometer (mean of average epithelial cell height of all the epididymal tubules present in a cross sectiodanimal in five speci- mens of each group). For statistical eval- uation, the data were analyzed by analysis of variance (ANOVA) followed by Student- Newman Keuls' multiple-range test to deter- mine the differences between the pairs of means of treated groups. Seasonal changes in the ductuli and ductus epididymidis were evaluated by the Student's t-test.

RESULTS

The epididymis in H. flaviviridis consists of small convoluted tubules, the ductuli epidi-

dymis, and of a larger contorted tubule, the ductus epididymis, into which the former empty. The ductus epididymis increases markedly in diameter posteriorly and ends in a vas deferens. The tubules of both ductuli and ductus epididymis are lined by a single layer of epithelial cells followed by a smooth muscle layer. The epithelial cell height and lumen diameter of the ductus epididymis varies along its length, and on the basis of these dimensions it can be roughly divided into anterior, middle, and posterior regions.

Histological and histochemical changes in the ductuli as well as the ductus epididymis during the reproductive cycle of this species are appreciable. In April, when the reproductive phase was at its peak, the ductuli epididymides were lined by low columnar, nonciliated epithelial cells having rounded or oval nuclei with prominent nucleoli (Fig. 1). The hypertrophied epithelium of the ductuli at this time was filled with secretory granules. Spermatozoa were rarely seen in the lumen, however, probably due to rapid pas- sage through this region. During this phase the epithelium of the ductus epididymis was found to be columnar in the anterior region (Fig. 11, tall pseudostratified-columnar in the middle region (Fig. 2), and cuboidal in the posterior region (Fig. 3). A few cells of the epithelium were ciliated in the anterior and middle region, while the cells in the posterior region were nonciliated. The epithelium in all the regions of this duct was hypertrophied and filled with secretory granules. Lumen diameter and sperm number both markedly increased from anterior to posterior regions along the ductus epididymis. Intertubular connective tissue was poorly developed in all regions of the reproductively active ductus epididymis. The secretory granules present in the epithelium and the secretory sub- stance in the lumen showed a positive reaction to the SB-test for lipid (Fig. 4).

In June-July, when the lizards were sexually quiescent, the ductuli epididymal tubules were in a state of regression, lined by nonciliated, low cuboidal epithelial cells having shrunken nuclei. The epithelium exhibited atrophic changes and were devoid of any secretory granules. During this phase, the ductus epididymis was also regressed and its lumen was totally devoid of secretory material and sperm (Fig. 8). No striking histological differences were observed between the anterior and middle region of the regressed ductus epididymidis. The tubular epithelium

EPIDIDYMIS OF INDIAN WALL LIZARD 153

in these two regions was low cuboidal (Fig. 8). The posterior region, however, clearly differed from the other two regions; its epithelium was squamous and it had a larger lumen diameter (Fig. 9). The epithelium was nonciliated and intertubular connective tissue was markedly developed in all regions of the regressed ductus epididymidis. Further- more, in contrast to the breeding phase histology, the epithelium was devoid of secretory granules and exhibited a very weak reaction to the SB-test (Fig. 5).

Seasonal changes in the epithelial cell height and lumen diameter of ductuli epididymidis and those of ductus epididymidis are recorded in Table 1. The epithelial cell height and lumen diameter of ductuli epididymidis were significantly enlarged during the breeding phase as compared to these parameters in the sexually quiescent phase (P <.001). The ductus epididymidis exhibited significant variation in epithelial cell height and lumen diameter among its anterior, middle, and posterior regions. In the breeding phase, the epithelial cell height of the middle region was significantly more than that of the anterior region (P <.001), while the height of epithelium in the posterior region was significantly lower than that of any other regions (P <.001). The lumen of the ductus epididymidis became wider toward the posterior end (P c.05, anterior vs. middle; P <.001, middle vs. posterior). During the sexually quiescent phase, the height of the epithelium in the anterior and middle regions did not vary significantly, while the lumen diameter of the middle region was significantly more than that of the anterior region (P < .01). The posterior region of the ductus epididymidis significantly differed from any other region by displaying the smallest epithelial cell height (P <.005, posterior vs. anterior or middle) and the largest lumen diameter (P < .005, posterior vs. anterior; P < .01, posterior vs. middle). A significant increase in epithelial cell height as well as in lumen diameter was recorded in all regions of the reproductively active ductus epididymidis when compared to sexually regressed coun- terparts (P < .001).

Functional responses of the ductus epididymidis, were investigated by assessing the effects of FSH, LH, and testosterone on the histology and histochemistry of the different regions of the ductus epididymidis in the month of June. The relative effects of mammalian FSH, LH, and testosterone on epithe-

lial cell height in all three regions of the regressed ductus epididymidis are summa- rized in Table 2. Analyzed by ANOVA, cells of the three regions exhibited highly significant variations (P <.001) in the epithelial cell height in relation to treatment (t), dura- tion of experiment (d), and interaction (t x d). When the data of hormone-treated groups were compared to controls by using Student- Newman Keuls’ multiple range test, FSH and testosterone were found to have a statistically significant stimulatory effect on the height of the epithelium whereas LH had no significant effect.

Stimulation of seasonally regressed ductus epididymal tubules could be observed histologically after 7 days of FSH treatment (Fig. 13). Extending FSH treatment to 21 days resulted in hypertrophy of the epithelial cells and the presence of secretory granules in the epithelium as well as in the lumen (Fig. 14). The stimulated epithelium in the anterior and middle regions (Fig. 14) was columnar, while that in the posterior region was cuboidal to moderately columnar. After FSH treatment the intertubular connective tissue became reduced in all regions of the ductus epididymidis. The lumen of ductus epididy- ma1 tubules in all regions was markedly increased in response to FSH treatment (Fig. 14). In contrast, LH had no appreciable effect on the ductus epididymidis and induced histological changes similar to those in FSH- treated lizards (Fig. 14). In response to either testosterone (Fig. 6) or FSH (Fig. 7 ) the epithelium became sudanophilic in its response to SB; likewise the secretory material present in the lumen of the ductus epididymidis stained positively.

DISCUSSION

In H. flaviviridis, after the spermatozoa emerge from the efferent ducts, they enter the epididymis. The epididymis consists of numerous, small, convoluted, ductuli epididymidis which unite to form a larger ductus epididymidis. The arrangement of these ducts in this species corresponds to a general reptilian pattern, as described by Van den Broek (‘33). On the basis of histological changes, the ductus epididymidis of this species can be roughly divided into anterior, middle, and posterior regions. The epithelial cell height was highest in the middle region and lowest in the posterior region. Epithelium in the anterior and middle regions was columnar, while in the posterior region it changed from

154 S. HAIDER AND U. RAI


columnar to cuboidal. The lumen of this duct also exhibited a gradual increase in its diameter from its anterior to its posterior end. The histology of the anterior, middle, and posterior regions of the ductus epididymidis of H. flaviviridis appears to be more or less similar, to that of the head, body, and tail, respectively, of the mammalian ductus epididymidis, in which epithelium changes from columnar to cuboidal along the head-to-tail axis with a concomitant increase in diameter.

Among reptiles, the cyclical fluctuations in both ductuli and ductus epididymidis have been extensively studied in squamates (Henry, 1900; Morgera, '05; Herlant, '33; Re- gamey, '35; Reynolds, '43; Volsde, '44; Fox, '52). However, a great divergence has been observed among the squamates with respect to changes in epithelial cell height, tubular diameter, and the secretory activity of the ductuli and ductus of the epididymis during

Fig. 1. Section of anterior region of the ductus epididymidis of a reproductively active H. flauiuiridis, showing hypertrophy of the epithelium in both ductuli @) and ductus epididymidis (larger tubules). The lumen of the ductus epididymidis contains secretory material mixed with a few sperms. Reduced intertubular connective tissue can also be seen. H & E. X 360.

Fig. 2. Section of middle region of the ductus epididymidis of a reproductively active H. flauiuiridis, showing hypertrophied, tall-columnar, pseudostratified epithelium filled with secretory granules. The lumen (L) is also filled with eosinophilic secretory material mixed with sperm. H & E. ~ 3 6 0 .

Fig. 3. Section of posterior region of the ductus epididymidis of a reproductively active H. flauiuiridis. Note the cuboidal cells of epithelium. The lumen diameter and sperm population are markedly increased whereas the height of the epithelium is reduced in comparison with anterior and middle regions. H & E. X360.

Fig. 4. Section of middle region of the ductus epididymidis of a reproductively active H. flauiuiridis, showing the presence of sudanophilic secretory granules in the epithelium as well as in the lumen. Sudan black-B (SB). x600.

Fig. 5. Comparable middle region of the ductus epididymidis of a sexually quiescent lizard showing very weak sudanophilia. SB. X600.

Fig. 6. Section of middle region of the ductus epididymidis of a sexually quiescent lizard treated with testosterone for 21 days, showing hypertrophy of the epithelium and presence of sudanophilic secretory granules. SB. x600.

Fig. 7. Comparable middle region of the ductus epididymidis of a sexually quiescent lizard treated with FSH for 21 days, showing stimulated epithelium containing sudanophilic granules. SB. X600.


the annual cycle. In two species of Lacerta and in the snakes Zamenis uiridiflauus and Elaphis quadrifasciatus, an appreciable enlargement of the epithelium of the ductuli was observed by Morgera ('05) in spring. He also described a seasonal variation in the secretory activity of the epithelial cells of ductuli in Lacerta. In contrast, Volsde ('44) could not detect any apparent seasonal variation either in cell height or in tubular diameter or in the secretory activity of ductuli in the snake Vipera berus. However, in the garter snake Thamnophis, Fox ('52) has observed a marked increase in the epithelial cell height, tubule diameter, and secretory activity of ductuli during the appearance of spermatozoa in the lumen. Similarly, in H.

Fig. 8. Section of middle region of the ductus epididymidis of a sexually quiescent control lizard, showing regressed epididymal tubules lined by low cuboidal epi- ithelium with shrunken nuclei. Note the absence of secretory granules in the epithelium. Lumen is also totally devoid of secretory material and sperms. The intertubular connective tissue (IC) is markedly developed. H & E. x 360.

flauiuiridis a significant enhancement of epithelial cell height and tubule diameter of ductuli and the presence of secretory granules in the cells of this duct were observed during the breeding season.

Although a variation in the cell height and tubule diameter of the ductus epididymidis has been found in the garter snake (Fox, '52) and viper WoisBe, '44) during the annual cycle, these fluctuations are neither very striking nor very consistent. No secretory granules have been detected in the epithelium of the ductus epididymidis of these snakes. Volsde has suggested that the secretory activity of the ductus epididymidis has been largely lost in snakes and that its function is carried out almost entirely by the primary segments of the ductuli. This does not appear to be true in lizards. In all the lizards studied so far a significant increase in the height of the epithelium of the ductus epididymidis and the presence of a large number of secretory granules in the cells of this duct have been observed during the breeding season (Herlant, '33; Regamey, '35; Reynolds, '43). Similarly, during the breeding season the epithelial cell height and lu- m& diameter ofall the regions oFthe ductus epididymidis were significant.y increased in

flauiuiridis and the cells of this duct were filled with secretory granules. A comparative description of the histology of the ductus epididymidis and its secretory granules has been published Dufaure and Saint Girons ('84) for 89 species of SqUamata (Zacertilia, Am- phisbaenia, and Serpentes) during the repro-

Fig. 9. section of posterior region of the ductus epididymidis of a sexually quiescent control lizard, showing clear differences from the other two regions in the ex- treme flattening of its squamous epithelium (arrows) and in its very large lumen diameter. H & E. X 360.

Fig. 10. Section of middle region of the ductus epididymidis of a sexually quiescent lizard treated with LH for 21 days, showing no change in its histology in corn- parison to that illustrated in Figure 8. H & E. X 360.

Fig. 11. Section of posterior region of the ductus epididymidis of a sexually quiescent lizard treated with testosterone for 21 days showing enlargement of the epithelium. Note the presence of secretory granules in the epithelium as well as in the lumen (arrow). H & E. x 360.

Fig. 12. Section of middle region of the ductus epididymidis of a sexually quiescent lizard treated with testosterone for 21 days, showing hypertrophy of the epithelium and presence of secretory material in the lumen (arrow). A considerable reduction in the intertubular connective tissue can also be seen. H & E. x 360.

Fig. 13. Section of comparable middle region of the ductus epididymidis of a sexually quiescent lizard treated with FSH for 7 days, showing a slight stimulation of epididymal tubule. H & E. x 360.

duction period. According to the appearance of secretory granules in the epithelial cells, they have categorized five types of ductus epididymidis in Squamata, ranging from a type with abundant and voluminous secretions consisting of big secretory granules as in Lacertidae to a type totally lacking secretions despite a hypertrophied epithelium as in Ophidia. Three intermediate stages occur between these extremes. The epididymal secretions of H. flauiuiridis, a member of the family Gekkonidae, are comparable to those of the other nine species of the same family studied by Dufaure and Saint Girons. There- fore, this species can also be categorized as

Fig, 14. &&ion of middle region of the having an intermediate type Of ductus epidi- ductus epididymidis of a sexually quiescent lizard treated with FSH for 21 days. Note the highly stimulated epithelium and presence of an abundance of secretory granules in the epithelium as well as in the lumen (arrows). Growth of the ductus epididymidis can also be seen by the presence of prominent blood vessels (BV) and poorly developed intertubular connective tissue. H & E. x 360.

%'midis along with the other studied mem- bers of the Gekkonidae.

The inhibition of growth and secretory activity of the epididymis in castrated menS and their maintenance by exogenous testosterone have been observed in several


TABLE 2. Effects of mammalian FSH, LH, and testosterone on the auerage epithelial cell height in anterior, middle, and posterior regions of

ductus epididymidis in H. flauiuiridis'

Epithelial cell height (pm) No. of Treatments days Anterior Middle Posterior

Control

LH 30 pgiday on alternate days

FSH 30 pgiday on alternate days

Testosterone 30 pgiday on alternate davs

7 7.51 i: 0.14a 15 7.12 i: 0.21a 21 8.43 i: 0.40a 7 8.33 i: 0.44a

15 8.69 i: 0.2ga 21 9.32 k 0.45a*e 7 16.56 k 1.04'

15 30.75 i: 0.67' 21 31.33 F 1.55'

15 15.98 i: 1.24' 7 11.34 k 0.81d,e

21 20.33 k 1.96f

7.25 f 0.18a 6.97 i: 0.27a 7.49 f 0.34a

1.91 i: O.loa 2.49 i: 0.31a 2.12 i: 0.27a

8.57 i: 0.22a.e 2.22 F 0 . 3 1 ~ 8.39 i: 0.35a 8.43 i: 0.30a

15.97 rt 0.58' 21.78 f 2.20' 29.53 k 1.56d 11.16 k 0.30"~~ 15.47 rt 1.16' 26.18 i: 0.78g

2.46 rt 0.30a 3.01 k 0.07a

10.74 k 0.56' 13.48 i: 0.50' 13.94 ~t 0.70' 6.66 i: 0.24d 7.79 f 0.42e

13.70 k 0.37'

'Values on a vertical line bearing same superscript are not statistically different from each other (Newman-Keul's multiple range test, P < .05 or .01).

squamates (Dufaure and Gigon, '75; Gigon, '75; Gigon-Depeiges and Dufaure, '77; Ak- barsha and Balasubramanian, '831, includ- ing H. flaviviridis (Haider, '85), suggesting the dependence of the epididymis on testicular androgens. It is now rather widely ac- cepted that the source of testicular androgens is the Leydig cells, which have been shown to undergo a well-defined annual cycle. In H. flauiviridis maximum secretory activity of the Leydig cells was found during the breeding season and minimum activity during the sexually quiescent phase (Rai and Haider, '86). At the time of breeding, the epithelium of both ductuli and the ductus epididymidis was markedly enlarged, hypertrophied, and filled with secretory granules. It seems that secretory activity of the epididymis in H. flaviviridis is parallel to the functional activity of the Leydig cells. A similar positive correlation was drawn by Courrier ('29) in Ure rnastk and by Herlant ('33) in Lacerta and Anguis. In contrast, no such correlation has been found in Tharnnophis (Fox, '52). In this species, growth of the epididymis occurs at the time when mature sperm are passing through it. Fox ('52) has suggested the possi- bility that some mechanical or chemical in- fluence originating in the sperm may be partly responsible for this hypertrophy. How- ever, in Vipera berus a significant correlation between growth of the epididymis and the hypertrophy of the Leydig cells has been described (Volsde, '44).

In all vertebrates, it is well established that

androgen by the Leydig cells, which in turn maintains the accessory reproductive organs. In mammals withdrawal of LH by hypophysectomy (Morat, '77; Ewing et al., '831, by injection of LH antisera (Dym and Raj, '77), or by implantation of testosterone-estradiol 17@ (T-El-filled polydimethylsiloxane (PDS) capsules (Ewing et al., '83) caused atrophy of the Leydig cells. Furthermore, the capacity of testes from hypophysectomized rats or from rats implanted with T-E PDS capsules to se- crete testosterone is maintained at control levels by treatment with LH but not with certain pituitary hormones (FSH, PRL, TSH, or GH, Ewing et al., '83). As in mammals, hypophysectomy in reptiles also causes regression of both the Leydig cells and accessory reproductive organs (Licht and Pearson, '69; Eyeson, '71; Licht, '721, but the gonadotropin responsible for this regression has not been established. In the hypophysectomized lizard Agarna agarna, only mammalian LH has been reported to be capable of maintain- ing the activity of the Leydig cells as well as the epididymis (Eyeson, '71). In the intact lizard Lacerta sicula during the autumn re- fractory period, both FSH and LH caused hypertrophy of the Leydig cells and develop- ment of the epididymis but the effect of FSH was much less than that of LH (Angelini et al., '78). In the lizard Leiolopisrna laterale three mammalian gonadotropins (FSH, HCG, PMSG) have been found to produce hypertrophy of the Leydig cells and a significant increase in the epithelial cell height of the

pituitary gonadotropins regulate secretion of quiescent epididymis (Jones, '737, whereas


LH notably has no such stimulatory effects. In the present investigation only FSH was found to be responsible for the growth and secretory activity of the quiescent epididymis. A marked hypertrophy of the Leydig cells has also been demonstrated when sexually quiescent individuals of H. flauiuiridis were treated with FSH (Rai and Haider, ’86). In the light of our earlier and present inves- tigations it may be suggested that the most active gonadotropin in the male of this species is similar to mammalian FSH and that this agent in turn regulates androgenic secretion.

ACKNOWLEDGMENTS

This work was supported by a grant from the University Grants Commission, Govern- ment of India, under its special assistance program. We express our appreciation to the National Institutes of Health, Bethesda, Maryland, U S A . , for a gift of FSH and LH hormones.

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