Morphology and Development of Reproductive System of Male Adult Tirumala limniace(Cramer)

LIU Wei-fen; LIAO Huai-jian; LIU Hong-ping; SHI Lei; DU Ting; ZHOU Cheng-li; DENG Jiang

Volume 29 Issue 6

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Morphology and Development of Reproductive System of Male Adult Tirumala limniace(Cramer)

1.
1. Research Institute of Resources Insects of the Chinese Academy of Forestry, Key Laboratory of Cultivation and Utilization of Resource Insects, State Forestry Administration, Kunming 650224, Yunnan, China
2.

2. Yunnan Forest Nature Center, Kunming 650224, Yunnan, China

Received Date: 2016-06-17

Abstract

[Objective] To study the morphology and development of internal reproductive organs of Tirumala limniace so that to provide theoretical guidance for the artificial breeding of T. limniace. [Methods] By anatomy method, the morphologies of internal reproductive organs of male T. limniace with ages from one-to twelve-day-old were observed, in the meanwhile, the numerical characteristic parameters were measured, and the development of internal reproductive organs was graded according to the characteristics of each organ so as to understand the morphologies and development of internal reproductive organs of male T. limniace systematically. [Results] (1) The internal reproductive organs of male T. limniace contain one testis, two vesicula seminalis, a pair of vas deferens, a pair of ejaculatory duct duplex, an ejaculatory duct simplex and accessory gland. (2) With the increase of age, the diameter of ejaculatory duct duplex and the length of ejaculatory duct simplex increased. (3) The length of sperm bundles in testis sustainable increased with the age increased, the length of sperm bundles in vesicula seminalis increased constantly before 7-day-old and tended to stability then. (4) With age increasing, the number of sperm bundles in testis decreased gradually, that in vesicula seminalis increased gradually from 1-to 7-day-old and maintained stability after 7 days, and that in ejaculatory duct duplex increased gradually. (5) The development of internal reproductive organs of male T. limniace could be divided into 4 grades, i.e. milky and translucent stage, transporting and growing of sperm bundle stage, mass transporting and maturing of sperm bundles stage, and replenishing of sperm bundle stage, based on the developmental characteristics of vesicula seminalis and ejaculatory duct duplex. [Conclusion] The internal reproductive organs of male T. limniace were the same as that of other butterflies; the sperms matured at 6-day-old, and were released to vesicula seminalis and ejaculatory duct duplex in turn, then joined in fertilization. In this study, the developmental process of the internal reproductive organs of male T. limniace was divided into 4 grades for the first time.
- Tirumala limniace(Cramer),
- testis,
- spermatogenesis,
- development grading

References

[1]	Fu X W, Li C, Feng H Q, et al. Seasonal migration of Cnaphalocrocis medinalis(Lepidoptera: Crambidae) over the Bohai Sea in northern China[J]. Bulletin of Entomological Research, 2014, 104(5): 601-609.
[2]	Justus K A, Mitchell B K. Reproductive morphology, copulation, and inter-populational variation in the diamondback moth, Plutella xylostella(L.) (Lepidoptera: Plutellidae)[J]. International Journal of Insect Morphology and Embryology, 1999, 28(3): 233-246.
[3]	Alves L, Mancini K, Lino-Neto J, et al. Morphology of the male reproductive system and sperm ultrastructure of Leucoptera coffeella (Lepidoptera: Lyonetiidae)[J]. Acta Zoologica, 2006, 87(2): 131-139.
[4]	Mancini K, Dolder H. Sperm morphology and arrangement along the male reproductive tract of the butterfly Euptoieta hegesia(Insecta: Lepidoptera)[J]. Invertebrate Reproduction & Development, 2003, 44(2-3): 107-117.
[5]	孟银凤, 尚素琴, 张雅林. 橙黄豆粉蝶生殖系统形态学研究[J]. 应用昆虫学报, 2013, 50(3): 813-817.
[6]	Jahnke S M, Redaelli L R, Diefenbach L M G. Internal reproductive organs of Cosmoclopius nigroannulatus (Hemiptera: Reduviidae)[J]. Brazilian Journal of Biology, 2006, 66(2A): 509-512.
[7]	Presgraves D C. Sperm heteromorphism and precedence in the stalk-eyed fly, Cyrtodiopsis whitei. University of Maryland, 1997.
[8]	Katsuno S. Studies on eupyrene and apyrene spermatozoa in the silkworm, Bombyx mori L. (Lepidoptera: Bombycidae): I. The intratesticular behaviour of the spermatozoa at various stages from the 5th~instar to the adult[J]. Applied Entomology and Zoology, 1977, 12(2): 142-153.
[9]	Morrow E H, Gage M J G. The evolution of sperm length in moths[J]. Proceedings of the Royal Society of London B: Biological Sciences, 2000, 267(1440): 307-313.
[10]	Osanai M, Chen P S. A comparative study on the arginine degradation cascade for sperm maturation of Bombyx mori and Drosophila melanogaster[J]. Amino Acids, 1993, 5(3): 341-350.
[11]	Osanai M, Kasuga H, Aigaki T. Isolations of eupyrene sperm bundles and apyrene spermatozoa from seminal fluid of the silkmoth, Bombyx mori[J]. Journal of Insect Physiology, 1989, 35(5): 401-408.
[12]	Swallow J G, Wilkinson G S. The long and short of sperm polymorphisms in insects[J]. Biological Reviews, 2002, 77(2): 153-182.
[13]	Friedländer M. Control of the eupyrene-apyrene sperm dimorphism in Lepidoptera[J]. Journal of Insect Physiology, 1997, 43(12): 1085-1092.
[14]	Silberglied R E, Shepherd J G, Dickinson J L. Eunuchs: The role of apyrene sperm in Lepidoptera?[J]. The American Naturalist, 1984, 123(2): 255-265.
[15]	周尧. 中国蝶类志[M]. 郑州: 河南科学技术出版社, 1999.
[16]	陈晓鸣, 周成理, 史军义, 等. 中国观赏蝴蝶[M]. 北京: 中国林业出版社, 2008.
[17]	Liao H J, Qian Q, Liu X D. Heat shock suppresses mating and sperm transfer in the rice leaf folder Cnaphalocrocis medinalis[J]. Bulletin of Entomological Research, 2014, 104(3): 383-392.
[18]	O'woma. O O, Chigozirim. U P, Emmanuel O, et al. Reproductive and survival strategies utilized by insect. A Review[J]. American Journal of Zoological Research, 2016, 4(1): 1-6.
[19]	刘琳, 冯启理. 鳞翅目昆虫精巢融合的研究[J]. 华南师范大学学报:自然科学版, 2014, 46(5): 1-7.
[20]	Callahan P S. Serial morphology as a technique for determination of reproductive patterns in the corn earworm, Heliothis Zea (Boddie)[J]. Annals of the Entomological Society of America, 1958, 51(5): 413-428.
[21]	Giebultowicz J M, Weyda F, Erbe E F, et al. Circadian rhythm of sperm release in the gypsy moth, Lymantria dispar: ultrastructural study of transepithelial penetration of sperm bundles[J]. Journal of Insect Physiology, 1997, 43(12): 1133-1147.
[22]	Giebultowicz J M, Zdarek J. The rhythms of sperm release from testis and mating flight are not correlated in Lymantria moths[J]. Journal of Insect Physiology, 1996, 42(2): 167-170.
[23]	Gieultowicz J M, Riemann J G, Raina A K, et al. Circadian System Controlling Release of Sperm in the Insect Testes[J]. Science, 1989, 245(4922): 1098-1100.
[24]	刘绪生, 李国清, 陈长琨. 棉铃虫精子在雌蛾生殖道内的转移动态[J]. 南京农业大学学报, 2001, 24(2): 45-48.
[25]	Arnqvist G, Nilsson T. The evolution of polyandry: multiple mating and female fitness in insects[J]. Animal Behaviour, 2000, 60(2): 145-164.
[26]	Steiner S, Henrich N, Ruther J. Mating with sperm-depleted males does not increase female mating frequency in the parasitoid Lariophagus distinguendus[J]. Entomologia Experimentalis et Applicata, 2008, 126(2): 131-137.
[27]	孙芳, 陈中正, 段毕升, 等. 蝇蛹金小蜂的交配行为及雄蜂交配次数对雌蜂繁殖的影响[J]. 生态学报, 2013(14): 4354-4360.
[28]	Damiens D, Boivin G. Why do sperm-depleted parasitoid males continue to mate[J]. Behavioral Ecology, 2006,17(1):138-143.

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通讯作者: 陈斌, bchen63@163.com

1.
沈阳化工大学材料科学与工程学院沈阳 110142

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Morphology and Development of Reproductive System of Male Adult Tirumala limniace(Cramer)

1. 1. Research Institute of Resources Insects of the Chinese Academy of Forestry, Key Laboratory of Cultivation and Utilization of Resource Insects, State Forestry Administration, Kunming 650224, Yunnan, China

2.
2. Yunnan Forest Nature Center, Kunming 650224, Yunnan, China

Received Date: 2016-06-17

Abstract: [Objective] To study the morphology and development of internal reproductive organs of Tirumala limniace so that to provide theoretical guidance for the artificial breeding of T. limniace. [Methods] By anatomy method, the morphologies of internal reproductive organs of male T. limniace with ages from one-to twelve-day-old were observed, in the meanwhile, the numerical characteristic parameters were measured, and the development of internal reproductive organs was graded according to the characteristics of each organ so as to understand the morphologies and development of internal reproductive organs of male T. limniace systematically. [Results] (1) The internal reproductive organs of male T. limniace contain one testis, two vesicula seminalis, a pair of vas deferens, a pair of ejaculatory duct duplex, an ejaculatory duct simplex and accessory gland. (2) With the increase of age, the diameter of ejaculatory duct duplex and the length of ejaculatory duct simplex increased. (3) The length of sperm bundles in testis sustainable increased with the age increased, the length of sperm bundles in vesicula seminalis increased constantly before 7-day-old and tended to stability then. (4) With age increasing, the number of sperm bundles in testis decreased gradually, that in vesicula seminalis increased gradually from 1-to 7-day-old and maintained stability after 7 days, and that in ejaculatory duct duplex increased gradually. (5) The development of internal reproductive organs of male T. limniace could be divided into 4 grades, i.e. milky and translucent stage, transporting and growing of sperm bundle stage, mass transporting and maturing of sperm bundles stage, and replenishing of sperm bundle stage, based on the developmental characteristics of vesicula seminalis and ejaculatory duct duplex. [Conclusion] The internal reproductive organs of male T. limniace were the same as that of other butterflies; the sperms matured at 6-day-old, and were released to vesicula seminalis and ejaculatory duct duplex in turn, then joined in fertilization. In this study, the developmental process of the internal reproductive organs of male T. limniace was divided into 4 grades for the first time.

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Reference (28)

[1]	Fu X W, Li C, Feng H Q, et al. Seasonal migration of Cnaphalocrocis medinalis(Lepidoptera: Crambidae) over the Bohai Sea in northern China[J]. Bulletin of Entomological Research, 2014, 104(5): 601-609.
[2]	Justus K A, Mitchell B K. Reproductive morphology, copulation, and inter-populational variation in the diamondback moth, Plutella xylostella(L.) (Lepidoptera: Plutellidae)[J]. International Journal of Insect Morphology and Embryology, 1999, 28(3): 233-246.
[3]	Alves L, Mancini K, Lino-Neto J, et al. Morphology of the male reproductive system and sperm ultrastructure of Leucoptera coffeella (Lepidoptera: Lyonetiidae)[J]. Acta Zoologica, 2006, 87(2): 131-139.
[4]	Mancini K, Dolder H. Sperm morphology and arrangement along the male reproductive tract of the butterfly Euptoieta hegesia(Insecta: Lepidoptera)[J]. Invertebrate Reproduction & Development, 2003, 44(2-3): 107-117.
[5]	孟银凤, 尚素琴, 张雅林. 橙黄豆粉蝶生殖系统形态学研究[J]. 应用昆虫学报, 2013, 50(3): 813-817.
[6]	Jahnke S M, Redaelli L R, Diefenbach L M G. Internal reproductive organs of Cosmoclopius nigroannulatus (Hemiptera: Reduviidae)[J]. Brazilian Journal of Biology, 2006, 66(2A): 509-512.
[7]	Presgraves D C. Sperm heteromorphism and precedence in the stalk-eyed fly, Cyrtodiopsis whitei. University of Maryland, 1997.
[8]	Katsuno S. Studies on eupyrene and apyrene spermatozoa in the silkworm, Bombyx mori L. (Lepidoptera: Bombycidae): I. The intratesticular behaviour of the spermatozoa at various stages from the 5th~instar to the adult[J]. Applied Entomology and Zoology, 1977, 12(2): 142-153.
[9]	Morrow E H, Gage M J G. The evolution of sperm length in moths[J]. Proceedings of the Royal Society of London B: Biological Sciences, 2000, 267(1440): 307-313.
[10]	Osanai M, Chen P S. A comparative study on the arginine degradation cascade for sperm maturation of Bombyx mori and Drosophila melanogaster[J]. Amino Acids, 1993, 5(3): 341-350.
[11]	Osanai M, Kasuga H, Aigaki T. Isolations of eupyrene sperm bundles and apyrene spermatozoa from seminal fluid of the silkmoth, Bombyx mori[J]. Journal of Insect Physiology, 1989, 35(5): 401-408.
[12]	Swallow J G, Wilkinson G S. The long and short of sperm polymorphisms in insects[J]. Biological Reviews, 2002, 77(2): 153-182.
[13]	Friedländer M. Control of the eupyrene-apyrene sperm dimorphism in Lepidoptera[J]. Journal of Insect Physiology, 1997, 43(12): 1085-1092.
[14]	Silberglied R E, Shepherd J G, Dickinson J L. Eunuchs: The role of apyrene sperm in Lepidoptera?[J]. The American Naturalist, 1984, 123(2): 255-265.
[15]	周尧. 中国蝶类志[M]. 郑州: 河南科学技术出版社, 1999.
[16]	陈晓鸣, 周成理, 史军义, 等. 中国观赏蝴蝶[M]. 北京: 中国林业出版社, 2008.
[17]	Liao H J, Qian Q, Liu X D. Heat shock suppresses mating and sperm transfer in the rice leaf folder Cnaphalocrocis medinalis[J]. Bulletin of Entomological Research, 2014, 104(3): 383-392.
[18]	O'woma. O O, Chigozirim. U P, Emmanuel O, et al. Reproductive and survival strategies utilized by insect. A Review[J]. American Journal of Zoological Research, 2016, 4(1): 1-6.
[19]	刘琳, 冯启理. 鳞翅目昆虫精巢融合的研究[J]. 华南师范大学学报:自然科学版, 2014, 46(5): 1-7.
[20]	Callahan P S. Serial morphology as a technique for determination of reproductive patterns in the corn earworm, Heliothis Zea (Boddie)[J]. Annals of the Entomological Society of America, 1958, 51(5): 413-428.
[21]	Giebultowicz J M, Weyda F, Erbe E F, et al. Circadian rhythm of sperm release in the gypsy moth, Lymantria dispar: ultrastructural study of transepithelial penetration of sperm bundles[J]. Journal of Insect Physiology, 1997, 43(12): 1133-1147.
[22]	Giebultowicz J M, Zdarek J. The rhythms of sperm release from testis and mating flight are not correlated in Lymantria moths[J]. Journal of Insect Physiology, 1996, 42(2): 167-170.
[23]	Gieultowicz J M, Riemann J G, Raina A K, et al. Circadian System Controlling Release of Sperm in the Insect Testes[J]. Science, 1989, 245(4922): 1098-1100.
[24]	刘绪生, 李国清, 陈长琨. 棉铃虫精子在雌蛾生殖道内的转移动态[J]. 南京农业大学学报, 2001, 24(2): 45-48.
[25]	Arnqvist G, Nilsson T. The evolution of polyandry: multiple mating and female fitness in insects[J]. Animal Behaviour, 2000, 60(2): 145-164.
[26]	Steiner S, Henrich N, Ruther J. Mating with sperm-depleted males does not increase female mating frequency in the parasitoid Lariophagus distinguendus[J]. Entomologia Experimentalis et Applicata, 2008, 126(2): 131-137.
[27]	孙芳, 陈中正, 段毕升, 等. 蝇蛹金小蜂的交配行为及雄蜂交配次数对雌蜂繁殖的影响[J]. 生态学报, 2013(14): 4354-4360.
[28]	Damiens D, Boivin G. Why do sperm-depleted parasitoid males continue to mate[J]. Behavioral Ecology, 2006,17(1):138-143.

Morphology and Development of Reproductive System of Male Adult Tirumala limniace(Cramer)

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通讯作者: 陈斌, bchen63@163.com

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Morphology and Development of Reproductive System of Male Adult Tirumala limniace(Cramer)

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