- Email: [email protected]
Male reproductive system of three species of polistes (hymenoptera: vespidae)
Int. J. Insect Morphol. & Embryol. 1 (4): pp. 315-320. 1972. Pergamon Press. Printed in Great Britain.
MALE REPRODUCTIVE SYSTEM OF THREE SPECIES OF POLISTES
(HYMENOPTERA: VESPIDAE)*
TOBIAS F. DIRKSt and JAMES G. STEI~NBUR6 Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, U.S.A.
(Accepted 9 June 1972) Abstract--The adult male reproductive system of 3 species of North American Polistes wasps is described. The testes are paired, but united within a common testicular sheath. Three testicular follicles are present in each testis. The follicles are packed with mature spermatozoa arranged in bundles with heads facing the lumen. From each testis arises a vas deferens which possesses a bulbous seminal vesicle. The paired bulbous accessory glands are positioned immediately posterior and laterad to the seminal vesicles to form compact seminal vesicle-accessory gland complexes which are surrounded by a common sheath. The absence of complex musculature on the seminal vesicles and accessory glands is noteworthy. Index deseriotors (in addition to those in title): Seminal vesicle, accessory gland, testis, spermatozoa, histology.
INTRODUCTION MUCH VARIATION exists in the male reproductive system of Hymenoptera. The testes of all hymenopterous males are paired and may or may not be fused medially above the digestive tract. T h r o u g h o u t the order, the seminal vesicles show several variations: (1) relatively undifferentiated vasa deferentia, as in some ants (Forbes, 1954, 1958); (2) cylindrical sacs, as in the honey bee, Apis mellifera L. and Vespa spp. (Bordas, 1895); (3) slightly enlarged areas o f the vasa deferentia, as in Polemon liparae Giraud ( D ' R o s a r i o , 1942), and Eumenes pomiformis F. (Bordas, 1895); or (4) distinct bulbs, as in Sceliphron cementarium (Drury) (observations of authors). The accessory glands, which arise posterior to the seminal vesicles, also vary: (l) sac-like, as in Cephus pygmaeus (Norton) (D'Rosaria, 1942), Camponotus pennsylvanicus De Geer (Forbes, 1954) and Vespa spp. (Bordas, 1895) ; (2) tubular, as in Neivamyrmex harrisi (Haldeman) (Forbes and Do-Van-Quy, 1965) and Eciton hamatum F. (Forbes, 1958); or (3) bulbous, as in Sceliphron cementarium (observations o f authors). Little attention has been directed to the male reproductive systems of polistine wasps. Bordas (1895) described the general m o r p h o l o g y o f the internal system o f Polistes gallicus (L.). In a paper devoted to spermatogenesis in several species of Polistes, Machida (1934) only covered the m o r p h o l o g y o f the testes. Snelling (1970) illustrated the external genitalia o f certain species o f Polistes, and indicated that these structures are o f taxonomic value. * A portion of this investigation was supported by USPH Training Grant GM-1076 and is included in the senior author's Ph.D. thesis completed at the University of Illinois. ~ Present address: Department of Entomology, University of Georgia, Athens, Georgia 30601, U.S.A. 315
316
TOBIAS F. DIRKS and JAMES G. STERNBURG
The reproductive system of the polistine males described here differs from Polistes gallicus (Fig. 2) and the hornets (Vespa spp.) described by Bordas (1895). Two compact units, each consisting of a seminal vesicle and an accessory gland, are present in the wasps considered here, while the European vespids possess sac-like seminal vesicles and accessory glands which are closely associated only at their bases (Figs. 1 and 2). Because of this unusual feature, the reproductive system o f these New World Polistes is considered worthy of description. MATERIALS AND METHODS Three species o f Polistes were used in this study. Polistes metricus Say and P. exclamans Viereck were collected from nests in Marion Co., Kansas, during the fall of 1969. Specimens of P. annularis (L.) were taken from fall populations in Clarke Co., Georgia, in 1970. Alcoholic Bouin's solution was used for fixation of tissues for sectioning. These tissues were embedded in Paraplast R (54°C melting point) and sectioned at 7 t~. A Delafield's hematoxylin-eosin (H and E) stain was employed. F o r general observation, the reproductive system was bathed in saline in situ and stained with 0-1 per cent aqueous Janus Green B. To observe detail of the seminal vesicle--accessory gland complex, phase microscopy was employed. The testes were cleared in methyl salicylate to allow for observation of testicular follicles.
OBSERVATIONS AND DISCUSSION General structure The reproductive system of P. metrieus is illustrated as representative of the 3 species considered (Fig. 1). The remaining species are similar as evidenced by the enlarged view of the seminal vesicle-accessory gland complex of P. exclamans (Fig. 3) and the testes of P. annularis (Fig. 4). The testes are positioned above the posterior region o f the midgut just anterior to the malpighian tubules. They are paired but fused within a testicular capsule. A b u n d a n t fat body overlies the capsule. Three tubular testicular follicles are present in each testis and arranged as shown in Fig. 4. A similar observation was made by Bordas (1895) for P. gallicus. The follicles are constricted posteriorly to form short vasa efferentia, which immediately join the origin o f the vas deferens (Fig. 4). Some individuals possessed atrophied testes, indicating that the spermatozoa had been voided.
FIGS. 1-4. General structure of Polistes male reproductive system. FIG. 1. Ventral aspect of male reproductive system of Polistes metricus. FIG. 2. Male reproductive system of P. gallicus, redrawn from Bordas (1895). FIG. 3. Seminal vesicle--accessory gland complex of P. exclarnans. FIG. 4. Ventral aspect of P. annularis testes.
AcG1 Aed CE Dej Dej C GM
= = ~ -~ ~
accessory gland aedeagus columnar epithelium ejaculatory duct common ejaculatory duct granular mass
Abbreviations used in figures L = lumen LC -- low columnar epithelium SE = squamous epithelium Sec = accessory gland secretion Sp = spermatozoa T = trophocyte
TC Tes TF Vd Ve Vsm
= -= ---
testicular capsule testes testicular follicle vas deferens vas efferens seminal vesicle
Male Reproductive System of Three Species of Polistes (Hymenoptera: Vespidae)
A/
V._--
.......
i
t i,
Vd
I
¢
,
' ,, '~ ,
i
I mrn
i
Dej
c°e
2
1 Aed
--TC
I
/'
!/ ij mO,25mml
4
i
317
318
TOBIAS F. DIRKS and JAMES G. STERNBURG
The paired seminal vesicles and accessory glands are complexed somewhat posterior to the testes (Figs. 1 and 3). Each complex is enclosed within a common sheath, which is tracheated by small tracheal elements branching from trunks which also lead to the alimentary canal. The bulbous seminal vesicle is an enlarged portion of the vas deferens and the accessory gland lies immediately posterior and laterad to it (Figs. 1 and 3). The short accessory gland duct joins the vas deferens immediately behind the seminal vesicle to form the ejaculatory duct. In fresh specimens the accessory gland appears milky white due to granular accessory gland fluid, while the sperm packed seminal vesicle is translucent. The European species (P. gallicus) described by Bordas does not possess the compact seminal vesicle-accessory gland complexes present in the North American forms discussed here (Fig. 2). Perhaps this feature has evolved subsequent to the geographic isolation of ancestral forms. An understanding of this apparent difference could probably be gained if more species of this cosmopolitan genus were examined.
Histology of Polistes annular& testes The testicular follicle is packed with sperm bundles arranged radially with heads pointing toward the lumen (Fig. 5). Only mature spermatozoa appear to be present in the adult stage of the wasp. Machida (1934) states that spermatogonia are found in the larva of Polistes. Trophocytes are scattered among the bundles of spermatozoa (Fig. 6). The lumen is filled with granular material similar to that described by Forbes and Do-Van-Quy (1965). Squamous epithelium makes up the follicle walls and the testicular capsule. The atrophied follicle is virtually void of spermatozoa (Fig. 7). It is much smaller than its active counterpart. The squamous epithelium appears thicker than that of the normal follicle, apparently a reorientation caused by the voiding of spermatozoa.
Histology of the seminal vesicle--accessory gland complex of Polistes annularis The vas deferens leading to the bulbous seminal vesicle is composed of simple cuboidal epithelium. The epithelial lining of the seminal vesicle is made up of columnar cells (Figs. 8 and 10). This columnar epithelium is apparently glandular. The cells were not well delineated by the stains employed (Fig. 10). The nuclei can be seen against the basement membrane, but the cell membranes are indistinct. Certain sections show a close relationship between the heads of spermatozoa and these cells (Fig. 10). Such an observation was made by Forbes and Do-Van-Quy (1965) for the ant Neivamyrmex harrisi. Squamous epithelium surrounds the seminal vesicle to form the sheath common also to the accessory gland. Muscle is found only around the lower end of the bulb of the seminal vesicle and on the continuation of the vas deferens lying alongside the accessory gland. This muscle is circular and appears to be only ! layer thick.
FIGS. 5-10. Histology of P. annularis male reproductive system. The reference line in lower left of each Figure represents 50/~. FIG. 5. Frontal section of testis, showing 2 of 3 follicles, vasa efferentia, and vas deferens. FIG. 6. Section similar to 5 at higher magnification. FIG. 7. Frontal section of atrophied testes, showing one follicle of each testis. FIG. 8. Cross section of accessory gland--seminal vesicle complex. FIG. 9. Cross section of seminal vesicle and accessory gland walls. FTG. 10. Cross section of seminal vesicle.
Male Reproductive System of Three Species of Polistes (Hymenoptera: Vespidae)
5
6
7
8
9
10
319
320
TOBIAS F. DIRKS and JAMES G. STERNBURG
The accessory gland possesses an epithelial lining composed of low columnar cells (Fig. 9). Terminal vacuoles are present in these cells, indicating that they are secretory. The secretion present in the lumen is strongly acidophilic and is sometimes shattered by the sectioning process. Forbes and D o - V a n - Q u y (1965) found basophilic secretion in the accessory gland o f N e i v a m y r m e x harrisi. The accessory gland duct is surrounded by a single layer of circular muscle similar to that on the lower portion o f the vas deferens. Circular muscle is also present on the ejaculatory duct. It is evident from the above discussion that neither of these bulbs is surrounded by complex musculature. In contrast, both circular and longitudinal muscles are present on the accessory glands and seminal vesicles of N e i v a m y r m e x (Forbes and Do-Van-Quy, 1965). In Polistes, spermatozoa and accessory gland fluids are apparently voided by rhythmic contractions o f circular muscles on the lower portions o f the bulbs and on the ejaculatory ducts. Acknowledgements--The authors wish to thank Mrs. Alice Prickett, Illustrator, Division of Biological Sciences, University of Illinois, for preparing Figs. 1 and 3. Dr. Henry R. Hermann and Mr. Allen N. Hunt, Department of Entomology, University of Georgia, assisted with histological interpretations, photography, and review of the manuscript.
REFERENCES BORDAS, M. S. 1895. Appareil g6nital m~le des Hym6nopt~res. Ann. Sci. Natur. 20: 101-84. D'ROSARIO,A. M, 1942. On the development and homologies of the genitalia and their ducts in Hymenoptera. Trans. Roy. Entomol. Soc. London 92 (2): 363-415. FORBES, J. 1954. The anatomy and histology of the male reproductive system of Camponotus pennsylvanicus DeGeer (Formicidae, Hymenoptera). J. Morphol. 95 (3): 523-55. FORBES, J. 1958. The male reproductive system of the army ant, Eciton hamatum Fabricius. Proc. IOth Int. Congr. Entomol. 1: 593-96. FORBES, J. and D. Do-VAN-Quv. 1965. The anatomy and histology of the male reproductive system of the legionary ant, Neivamyrmex harrisi (Haldeman) (Hymenoptera: Formicidae). J. New York Entomol. Soc. 73 (2): 95-111. MACH1DA,J. 1934. Spermatogenesis of three species of Polistes. Proc. Imp. Acad. Japan 10: 515-18. SNELL1NG, R. R. 1970. The social wasps of lower California, Mexico (Hymenoptera: Vespidae). Contributions Sci., Los Angeles Co. Museum. No. 1971.
MALE REPRODUCTIVE SYSTEM OF THREE SPECIES OF POLISTES
(HYMENOPTERA: VESPIDAE)*
TOBIAS F. DIRKSt and JAMES G. STEI~NBUR6 Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, U.S.A.
(Accepted 9 June 1972) Abstract--The adult male reproductive system of 3 species of North American Polistes wasps is described. The testes are paired, but united within a common testicular sheath. Three testicular follicles are present in each testis. The follicles are packed with mature spermatozoa arranged in bundles with heads facing the lumen. From each testis arises a vas deferens which possesses a bulbous seminal vesicle. The paired bulbous accessory glands are positioned immediately posterior and laterad to the seminal vesicles to form compact seminal vesicle-accessory gland complexes which are surrounded by a common sheath. The absence of complex musculature on the seminal vesicles and accessory glands is noteworthy. Index deseriotors (in addition to those in title): Seminal vesicle, accessory gland, testis, spermatozoa, histology.
INTRODUCTION MUCH VARIATION exists in the male reproductive system of Hymenoptera. The testes of all hymenopterous males are paired and may or may not be fused medially above the digestive tract. T h r o u g h o u t the order, the seminal vesicles show several variations: (1) relatively undifferentiated vasa deferentia, as in some ants (Forbes, 1954, 1958); (2) cylindrical sacs, as in the honey bee, Apis mellifera L. and Vespa spp. (Bordas, 1895); (3) slightly enlarged areas o f the vasa deferentia, as in Polemon liparae Giraud ( D ' R o s a r i o , 1942), and Eumenes pomiformis F. (Bordas, 1895); or (4) distinct bulbs, as in Sceliphron cementarium (Drury) (observations of authors). The accessory glands, which arise posterior to the seminal vesicles, also vary: (l) sac-like, as in Cephus pygmaeus (Norton) (D'Rosaria, 1942), Camponotus pennsylvanicus De Geer (Forbes, 1954) and Vespa spp. (Bordas, 1895) ; (2) tubular, as in Neivamyrmex harrisi (Haldeman) (Forbes and Do-Van-Quy, 1965) and Eciton hamatum F. (Forbes, 1958); or (3) bulbous, as in Sceliphron cementarium (observations o f authors). Little attention has been directed to the male reproductive systems of polistine wasps. Bordas (1895) described the general m o r p h o l o g y o f the internal system o f Polistes gallicus (L.). In a paper devoted to spermatogenesis in several species of Polistes, Machida (1934) only covered the m o r p h o l o g y o f the testes. Snelling (1970) illustrated the external genitalia o f certain species o f Polistes, and indicated that these structures are o f taxonomic value. * A portion of this investigation was supported by USPH Training Grant GM-1076 and is included in the senior author's Ph.D. thesis completed at the University of Illinois. ~ Present address: Department of Entomology, University of Georgia, Athens, Georgia 30601, U.S.A. 315
316
TOBIAS F. DIRKS and JAMES G. STERNBURG
The reproductive system of the polistine males described here differs from Polistes gallicus (Fig. 2) and the hornets (Vespa spp.) described by Bordas (1895). Two compact units, each consisting of a seminal vesicle and an accessory gland, are present in the wasps considered here, while the European vespids possess sac-like seminal vesicles and accessory glands which are closely associated only at their bases (Figs. 1 and 2). Because of this unusual feature, the reproductive system o f these New World Polistes is considered worthy of description. MATERIALS AND METHODS Three species o f Polistes were used in this study. Polistes metricus Say and P. exclamans Viereck were collected from nests in Marion Co., Kansas, during the fall of 1969. Specimens of P. annularis (L.) were taken from fall populations in Clarke Co., Georgia, in 1970. Alcoholic Bouin's solution was used for fixation of tissues for sectioning. These tissues were embedded in Paraplast R (54°C melting point) and sectioned at 7 t~. A Delafield's hematoxylin-eosin (H and E) stain was employed. F o r general observation, the reproductive system was bathed in saline in situ and stained with 0-1 per cent aqueous Janus Green B. To observe detail of the seminal vesicle--accessory gland complex, phase microscopy was employed. The testes were cleared in methyl salicylate to allow for observation of testicular follicles.
OBSERVATIONS AND DISCUSSION General structure The reproductive system of P. metrieus is illustrated as representative of the 3 species considered (Fig. 1). The remaining species are similar as evidenced by the enlarged view of the seminal vesicle-accessory gland complex of P. exclamans (Fig. 3) and the testes of P. annularis (Fig. 4). The testes are positioned above the posterior region o f the midgut just anterior to the malpighian tubules. They are paired but fused within a testicular capsule. A b u n d a n t fat body overlies the capsule. Three tubular testicular follicles are present in each testis and arranged as shown in Fig. 4. A similar observation was made by Bordas (1895) for P. gallicus. The follicles are constricted posteriorly to form short vasa efferentia, which immediately join the origin o f the vas deferens (Fig. 4). Some individuals possessed atrophied testes, indicating that the spermatozoa had been voided.
FIGS. 1-4. General structure of Polistes male reproductive system. FIG. 1. Ventral aspect of male reproductive system of Polistes metricus. FIG. 2. Male reproductive system of P. gallicus, redrawn from Bordas (1895). FIG. 3. Seminal vesicle--accessory gland complex of P. exclarnans. FIG. 4. Ventral aspect of P. annularis testes.
AcG1 Aed CE Dej Dej C GM
= = ~ -~ ~
accessory gland aedeagus columnar epithelium ejaculatory duct common ejaculatory duct granular mass
Abbreviations used in figures L = lumen LC -- low columnar epithelium SE = squamous epithelium Sec = accessory gland secretion Sp = spermatozoa T = trophocyte
TC Tes TF Vd Ve Vsm
= -= ---
testicular capsule testes testicular follicle vas deferens vas efferens seminal vesicle
Male Reproductive System of Three Species of Polistes (Hymenoptera: Vespidae)
A/
V._--
.......
i
t i,
Vd
I
¢
,
' ,, '~ ,
i
I mrn
i
Dej
c°e
2
1 Aed
--TC
I
/'
!/ ij mO,25mml
4
i
317
318
TOBIAS F. DIRKS and JAMES G. STERNBURG
The paired seminal vesicles and accessory glands are complexed somewhat posterior to the testes (Figs. 1 and 3). Each complex is enclosed within a common sheath, which is tracheated by small tracheal elements branching from trunks which also lead to the alimentary canal. The bulbous seminal vesicle is an enlarged portion of the vas deferens and the accessory gland lies immediately posterior and laterad to it (Figs. 1 and 3). The short accessory gland duct joins the vas deferens immediately behind the seminal vesicle to form the ejaculatory duct. In fresh specimens the accessory gland appears milky white due to granular accessory gland fluid, while the sperm packed seminal vesicle is translucent. The European species (P. gallicus) described by Bordas does not possess the compact seminal vesicle-accessory gland complexes present in the North American forms discussed here (Fig. 2). Perhaps this feature has evolved subsequent to the geographic isolation of ancestral forms. An understanding of this apparent difference could probably be gained if more species of this cosmopolitan genus were examined.
Histology of Polistes annular& testes The testicular follicle is packed with sperm bundles arranged radially with heads pointing toward the lumen (Fig. 5). Only mature spermatozoa appear to be present in the adult stage of the wasp. Machida (1934) states that spermatogonia are found in the larva of Polistes. Trophocytes are scattered among the bundles of spermatozoa (Fig. 6). The lumen is filled with granular material similar to that described by Forbes and Do-Van-Quy (1965). Squamous epithelium makes up the follicle walls and the testicular capsule. The atrophied follicle is virtually void of spermatozoa (Fig. 7). It is much smaller than its active counterpart. The squamous epithelium appears thicker than that of the normal follicle, apparently a reorientation caused by the voiding of spermatozoa.
Histology of the seminal vesicle--accessory gland complex of Polistes annularis The vas deferens leading to the bulbous seminal vesicle is composed of simple cuboidal epithelium. The epithelial lining of the seminal vesicle is made up of columnar cells (Figs. 8 and 10). This columnar epithelium is apparently glandular. The cells were not well delineated by the stains employed (Fig. 10). The nuclei can be seen against the basement membrane, but the cell membranes are indistinct. Certain sections show a close relationship between the heads of spermatozoa and these cells (Fig. 10). Such an observation was made by Forbes and Do-Van-Quy (1965) for the ant Neivamyrmex harrisi. Squamous epithelium surrounds the seminal vesicle to form the sheath common also to the accessory gland. Muscle is found only around the lower end of the bulb of the seminal vesicle and on the continuation of the vas deferens lying alongside the accessory gland. This muscle is circular and appears to be only ! layer thick.
FIGS. 5-10. Histology of P. annularis male reproductive system. The reference line in lower left of each Figure represents 50/~. FIG. 5. Frontal section of testis, showing 2 of 3 follicles, vasa efferentia, and vas deferens. FIG. 6. Section similar to 5 at higher magnification. FIG. 7. Frontal section of atrophied testes, showing one follicle of each testis. FIG. 8. Cross section of accessory gland--seminal vesicle complex. FIG. 9. Cross section of seminal vesicle and accessory gland walls. FTG. 10. Cross section of seminal vesicle.
Male Reproductive System of Three Species of Polistes (Hymenoptera: Vespidae)
5
6
7
8
9
10
319
320
TOBIAS F. DIRKS and JAMES G. STERNBURG
The accessory gland possesses an epithelial lining composed of low columnar cells (Fig. 9). Terminal vacuoles are present in these cells, indicating that they are secretory. The secretion present in the lumen is strongly acidophilic and is sometimes shattered by the sectioning process. Forbes and D o - V a n - Q u y (1965) found basophilic secretion in the accessory gland o f N e i v a m y r m e x harrisi. The accessory gland duct is surrounded by a single layer of circular muscle similar to that on the lower portion o f the vas deferens. Circular muscle is also present on the ejaculatory duct. It is evident from the above discussion that neither of these bulbs is surrounded by complex musculature. In contrast, both circular and longitudinal muscles are present on the accessory glands and seminal vesicles of N e i v a m y r m e x (Forbes and Do-Van-Quy, 1965). In Polistes, spermatozoa and accessory gland fluids are apparently voided by rhythmic contractions o f circular muscles on the lower portions o f the bulbs and on the ejaculatory ducts. Acknowledgements--The authors wish to thank Mrs. Alice Prickett, Illustrator, Division of Biological Sciences, University of Illinois, for preparing Figs. 1 and 3. Dr. Henry R. Hermann and Mr. Allen N. Hunt, Department of Entomology, University of Georgia, assisted with histological interpretations, photography, and review of the manuscript.
REFERENCES BORDAS, M. S. 1895. Appareil g6nital m~le des Hym6nopt~res. Ann. Sci. Natur. 20: 101-84. D'ROSARIO,A. M, 1942. On the development and homologies of the genitalia and their ducts in Hymenoptera. Trans. Roy. Entomol. Soc. London 92 (2): 363-415. FORBES, J. 1954. The anatomy and histology of the male reproductive system of Camponotus pennsylvanicus DeGeer (Formicidae, Hymenoptera). J. Morphol. 95 (3): 523-55. FORBES, J. 1958. The male reproductive system of the army ant, Eciton hamatum Fabricius. Proc. IOth Int. Congr. Entomol. 1: 593-96. FORBES, J. and D. Do-VAN-Quv. 1965. The anatomy and histology of the male reproductive system of the legionary ant, Neivamyrmex harrisi (Haldeman) (Hymenoptera: Formicidae). J. New York Entomol. Soc. 73 (2): 95-111. MACH1DA,J. 1934. Spermatogenesis of three species of Polistes. Proc. Imp. Acad. Japan 10: 515-18. SNELL1NG, R. R. 1970. The social wasps of lower California, Mexico (Hymenoptera: Vespidae). Contributions Sci., Los Angeles Co. Museum. No. 1971.