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Positional Relationships among Male Reproductive Organs in Insects

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Satoshi Hiroyoshi and Gadi V.P. Reddy

Submitted: April 21st, 2021 Reviewed: June 9th, 2021 Published: July 4th, 2021

DOI: 10.5772/intechopen.98798

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The location, morphology and function of male internal reproductive organs in insects have been extensively studied, but the relative positioning of those organs is less understood. Position and morphology of the testis, vas deferens, seminal vesicle, accessory gland and ejaculatory duct determine the migration or ejaculation of sperm and other substances. In species where the testis is connected with the seminal vesicle directly or the seminal vesicle is lacking, males usually store complete sperm in the testis and thus can use them immediately for mating. In contrast, the testis of lepidopteran insects is separated from the duplex (sperm storage organ) via the vas deferens, and the sperm are not mature, requiring morphological development in the vas deferens. Here, we discuss the significance of various positional relationships of male reproductive organs and how this relates to their morphology and function with a focus on sperm.


  • Testis
  • seminal vesicle
  • vas deferens
  • sperm reflux
  • sperm migration

1. Introduction

The morphology, structure and size of organs have functional significance. Insects are the most abundant of all organisms in terms of species number, resulting in female and male reproductive organs being highly diverse in their structure. While the general pattern of spermatogenesis in insects is basically similar to that in mammals, the morphology, structure, and size of sperm in insects are highly variable [1, 2].

Because available resources are usually limited, the number of sperm produced should be inversely proportional to their size [3]. Although smaller testes do not necessarily produce many sperm, sperm size is closely related to testis size. Among Drosophilagroups, there are positive relationships between testis length and sperm length [4, 5, 6]. Moreover, sperm length correlates positively with body size in butterfly species [7]. How much sperm a female receives and stores in the spermatheca (female sperm storage organ) should be determined by how many sperm are used for fertilization during the post-mating period. Many insect species are known to over-ejaculate under laboratory conditions but it is unclear whether excessive ejaculation is common in the field.

In general, sperm size in animals including insects is not proportional to body size. Drosophilaflies, as is well known, are tiny and thus have small testes, although D. bifurcahave large testes containing very long sperm reaching a length of 5.8 cm [8]. Therefore, the number of giant sperm that they produce is small [9]. This may be due to the size of the testes as well as other reproductive organs. Giant sperm are coiled [10], but their length and thickness must not hinder the movement within the male and female reproductive tract. It is thought that not only the cost of sperm production but also the control of sperm migration would be restricted to make the gamete larger, but in fact some Drosophilasperm have become giant beyond this constraint.

Sperm produced in the testes are usually stored in the seminal vesicles, if they are present. In insects, when present within the male reproductive organs, sperm are either not motile or their motility is more suppressive than when they are retained in the female reproductive organs. Therefore, males need to both store sperm in the seminal vesicles, and limit the energy costs associated with those sperm until mating. Recent studies have revealed that sperm age or die in the spermatheca [11, 12] or male reproductive organs [13], and it is interesting to see how aging affects sperm quality and survival in the seminal vesicles because the morphology of the seminal vesicles may be associated with sperm aging, as mentioned below. Furthermore, a recent molecular biology study indicates that increased expression of seminal fluid protein incorporated in spermatophore genes is correlated with increased sperm viability in the ejaculates [14].

During mating, male insects pass a spermatophore or bolus of seminal fluid to females. In many species, a spermatophore is produced by male reproductive accessory glands, whereas in lepidopteran insects, spermatophores are produced mainly from parts of the simplex (ejaculatory duct). In a nymphalid butterfly, Polygonia c-aureumL., the contents of the simplex are initially ejaculated followed by the contents of the duplex (male sperm storage organ) and then by the accessory glands just before the end of copulation [15]. In the Coleoptera, the accessory glands and seminal vesicles open directly into the ejaculatory duct, allowing seminal fluids in the accessory glands and sperm in the seminal vesicles to ejaculate simultaneously. Molecules transferred from males to females via the seminal vesicles that originated from the accessory glands, seminal vesicle, ejaculatory duct and/or testes affect female physiology, reproductive behavior, and longevity [16, 17]. The shape, size, and weight of the spermatophore made from the seminal fluids are greatly influenced by the structures of both male and female reproductive organs.


2. Function and structure of testes

Testes function is to produce sperm and in turn intake or excrete the various substances including nutrients and hormones for spermatogenesis. In species lacking seminal vesicles, mature sperm are stored in the testis near the vas deferens. The shape of the testis is circular, oval or elongated, perhaps corresponding to sperm length, probably because sperm develop greatly during spermiogenesis (from the spermatid to the sperm) [5]. The testes are usually paired and the numbers vary widely from species to species. The color of the testes also varies greatly depending on the species; for example, many lepidopteran insects have white, yellow, red, or purple testes. Although the pigments that are no longer needed in the body may be deposited in their testes, their function and evolutionary significance have not been clarified.

In P. c-aureum, the testis is completely covered with a yellow membrane from the last instar larval stage to the early adult stage while spermiogenesis is positively occurring [18]. Although the composition and function of this membrane are unknown, it is possible that it actively protects the testis and sperm cells from ultraviolet rays and/or various substances in the hemolymph, that are unsuitable or toxic to spermatogenesis. Alternatively, this membrane may positively improve the nutritional and/or humoral conditions for spermatogenesis. Interestingly, the time when this membrane begins to degenerate coincides with the time when adult development of wings is almost complete, the scale of spermatogenesis and testis size begin to shrink, and sperm begin to migrate from the testes to the vas deferens [18, 19, 20]. These synchronous events are strongly suspected to be associated with hormones in the hemolymph, such as ecdysteroid. Interestingly, it is shown in Calpodes ethliusStoll (Lepidoptera, Hesperiidae) that the testis is surrounded by the yellow pigment [21].

Testis development including spermatogenesis is affected by developmental stages, temperatures, nutritional conditions, and hormones [22, 23]. In the yellow dung fly Scathophaga stercoraria(L.), the testes atrophy after mating [24]. Similarly, in Drosophila melanogasterMeigen, there was a significant reduction in the testes size after five successive matings [25]. In general, testis development is closely related to spermatogenesis [26], and testis size usually increases as spermatogenesis becomes more active [27]. However, the relationship between testis size and spermatogenesis depends on the species and developmental stage.


3. Sperm polyphenism

Sperm polymorphism is apparent in the various insect orders [1, 2]. Generally, one sperm is long whereas the other is short; giant sperm have been observed in some Drosophilaand beetles. Giant sperm fertilize the eggs and short sperm do not participate in fertilization [28, 29], although contradictory findings raise the possibility that both morphs of sperm can fertilize [30]. In lepidopteran insects, there are fertile nucleated eupyrene sperm and infertile non-nucleated apyrene sperm [31, 32, 33, 34, 35]. Eupyrene sperm fertilize the eggs, whereas apyrene sperm cannot fertilize the eggs because they lose their nuclei during meiosis [36]. In general, apyrene sperm are produced more or transferred to females more than are eupyrene sperm [37, 38, 39], although spermatogenesis of eupyrene and apyrene sperm is not markedly different in the diamondback moth Plutella xylostella[40]. This seems to be related to the fact that apyrene sperm are shorter than eupyrene sperm and the former is generated later in development.


4. Storage and migration of sperm

The production and storage of sperm can be a lifelong event for males. There are four types of sperm migration within the male reproductive organs. First, sperm formed in the testis move to the vas deferens or the seminal vesicle. In lepidopteran insects, sperm migration occurs from the testis to the duplex via the vas deferens, with a circadian rhythm. Second, sperm move from the seminal vesicle through the ejaculatory duct to the female reproductive tract during mating. Third, there is a process called sperm reflux. In P. c-aureum, the accessory glands open into the duplex, but not into the ejaculatory duct, thus when the accessory gland material passes the duplex, it ejaculates all sperm present. This prevents sperm from being preserved in the next copulation. Thus this butterfly regurgitates excess sperm in the duplex into the vas deferens during mating. Finally, sperm migration sometimes occurs immediately after mating. Male sweetpotato weevils Cylas formicarius(F.) can mate several times a night, and sperm migrate from the testes to the seminal vesicles immediately after mating [41, 42]. This may be due to the fact that the seminal vesicles are adjacent to the testes, that spermatogenesis is active during the adult stage, and that sperm production is completed in the testes. Thus, the positional relationship between the testes and the seminal vesicles, the degree of sperm perfection in the testes, and the stage at which sperm are formed determine the male ejaculation pattern.

Sperm migration from the testis to the duplex via the vas deferens has been well studied in lepidopteran insects. Conversely, many dipteran insects do not have the seminal vesicles, which are sometimes called sperm reservoirs, however the distal end of the testis stores sperm. Their sperm are functionally complete. However, in lepidopteran insects, sperm are not mature in the testis and change morphologically when passing through the vas efferens from the testis to the vas deferens. It has been demonstrated that eupyrene sperm migration occurs in a circadian rhythm even in cases of in vitro culture of the testis- vas deferens-duplex complex [43]. It has also been reported that there is a circadian rhythm in the secretory activity of the upper vas deferens [44]. Although the reasons for sperm migration in lepidopteran insects being rhythmical are unclear, sperm migration is a time-consuming and energy-intensive process and thus it is reasonable to expect to be time managed.

Sperm formed in the testes are stored in the seminal vesicles until mating. At the time of mating, sperm are ejaculated into the female along with spermatophore. Interestingly, when Heliothis virescens(F.) are irradiated at the early adult stage, the sperm are not incorporated into the spermatophore because the sperm in the duplex has not moved to the simplex where the spermatophore is formed, resulting in no transfer of sperm [45]. Some studies have revealed that the so-called ‘mating failure’ often occurs in insects [46, 47, 48]. That is, they may mate but not pass spermatophore or sperm to females.

In Drosophila melanogasterMeigen, proteins within the seminal fluid of the male accessory gland are required for efficient accumulation of sperm in the female’s sperm storage organs, and morphological changes in the shape and position and tissues within the female reproductive tract may be needed for successful sperm storage [49]. In species with a long life span, for example, the wood-feeding cockroach, Cryptocercus punctutatus, sperm are viable in the spermatheca for at least three years [50]. In these cases, female condition as well as the longevity of sperm is important for sustaining their survival.

Although the function of the seminal vesicles is to store and protect sperm, it is known that organs other than the seminal vesicles also store sperm. In lepidopteran insects, several species have a dilated part, also called a secondary seminal vesicle, between the lower vas deferens and the duplex [46, 51, 52, 53]. Even if all the sperm in the duplex are ejaculated during mating, these stored sperm can be replenished immediately from the secondary seminal vesicle. In addition, even species with a large swelling in the middle vas deferens may store sperm there to some extent temporarily [54], and may transfer sperm to the duplex after mating to prepare for subsequent matings. In species with these functions, sperm reflux would not be present.


5. Insemination

In insects, a spermatophore is passed into the female reproductive organs during mating directly or indirectly. The system of insemination varies greatly from species to species, the main cause of which is species diversity and complexity of the female reproductive organs. Probably, the female complex of reproductive organs have co-evolved with the male complex of reproductive organs.

The timing of transfer of sperm to females during mating varies greatly from species to species. Copula duration also varies widely, from minutes in parasitoid wasp and mosquitoes [55] to days in stick insects [17], but in the latter the ejaculation duration could be shorter than the copula one. The post-mating guard guarantees female oviposition behavior and ovarian development. It has been suggested that sperm progression to the spermatheca is supported by the activity of the muscles and nerves of the male and female reproductive organs in addition to sperm motility [56].

Fertilization efficiency also affects the number of ejaculations. As is well known, ants and wasps can efficiently fertilize many eggs with a small amount of sperm. For example, in a parasitoid wasp Anisopteromalus calandrae(Howard) (Hymenoptera: Pteromalidae), males have small (several hundred) numbers of sperm in the seminal vesicle and the fertilizing efficiency of stored sperm in the female genital organs is extremely high [57], although in the majority of insects the ratio of fertilized eggs/stored sperm is low due to polyspermy at fertilization. Orthopteran insects can ejaculate a bit at a time, probably because their seminal vesicles and accessory glands have an elongated gland-like structure and open separately into the ejaculatory duct. Therefore, in the desert locust, spermatophore and sperm can be gradually transferred to females gradually during mating from the proximal part of the gland near the ejaculatory opening. Because sperm migration starts to occur actively several days after adult emergence, it seems likely that new sperm are constantly stored near the entrance of the seminal vesicles and ejaculated into the females (Hiroyoshi, unpublished). This might be related to sperm aging and sperm competition. In the migratory grasshopper Melanoplus sanguinipes(F.), several spermatophores are passed to females in a single mating [58]. If the accessory glands and seminal vesicles were not elongated, it would be difficult to transfer spermatophore and sperm a bit at a time.


6. Positional relationship

The arrangement of male internal reproductive organs of various species is listed in Table 1. Figure 1 shows the positional relationship between reproductive organs. Alphabetical order does not represent the phylogenetic relationship between species. Most probably other formats of organ positioning are yet to be discovered. Some insects lack the accessory glands. Of particular importance is the positional relationship between the testes, vas deferens, seminal vesicles, accessory glands, and ejaculatory duct, because the placement of these organs is important for ejaculation.

OrderFamilyScientific nameTypeReferences
ThysanuraLepismatidaeCtenolepisma campbelliF[59]
EphemeropteraLeptophlebiidaeMiroculis amazonicusH[60]
PlecopteraTaeniopterygidaeObipteryx sp.B[61]
PerlidaePerlesta placidaG[62]
DermapteraLabiduridaeLabidura ripariaH[63]
AnisolabididaeEuborellia brunneriH[64]
IsopteraTermitidaeSilvestritermes euamignathusH[27]
BlattodeaBlattidaeLeucophaea maderaeE[65]
MantodeaLiturgusidaeCiulfina klassiE[66]
OrthopteraCaeliferaOrphulella punctataE[67]
TetrigidaeTetrixarenosa angustaE[68]
PyrgomorphidaePoekilocerus pictusE[69]
PsocopteraPsyllipsocidaeDorypteryx domesticaH[70]
PsoqvillidaePsoquilla marginepunctataH[71]
HomopteraDelphacidaePeregrinus maidisB[72]
CicadellidaeGraminella nigrifronsB[73]
Bothrogonia ferrugineaB[74]
CicadoideaTamasa tristigmaB[75]
HemipteraReduviidaeRhodnius prolixusB[76]
Perillus bioculatus
Acyrthosiphon pisum
HymenopteraColletidaeColletes rufipesF[79]
AndrenidaeOxaea flavencensF[79]
MegachilidaeAnthidium manicatumB[79]
ApidaeCentris violaceaF[79]
EulophidaeDahlbominus fuscipennisB[80]
FormicidaeSolenopsis invictaF[81]
NeuropteraChrysopidaeChrysopa oculataB[82]
IthonidaePolystoechotes punctatusB[83]
NemopteridaePalmipenna sp.B[84]
MegalopteraCorydalidaeParachauliodes continentalisB[85]
ColeopteraRhysodidaeYamatosa nipponensisB[86]
Rhysodes comesB[87]
CarabidaeCampalita chinenseC[88]
Damaster fruhstorferiC[88]
Leistus prolongatusC[88]
TenebrionidaeParastizopus armaticepsB[89]
TrogossitidaeBolbocerosoma farctumB[90]
Meracantha contractaB[90]
ChrysomelidaeGalerucella birmanicaB[91]
Leptinotarsa docemlineataB[92]
ElateridaeMelanotus communisB[90]
ScarabaeidaePopillia japonicaB[90]
CiidaeHadraule blaisdelliB[93]
CurculionidaeAnthonomus grandisB[94]
Dendroctonus armandiB[95]
BruchidaeBruchidius atrolineatusB[96]
BrentidaeCylas formicarius elegantulusD[97]
SiphonapteraPulicidaeSpilopsyllus cuniculiC[98]
DipteraCulicidaeAnopheles gambiaeB[99]
PsychodidaeCulex pippiens
Lutzomyia longipalpis
TephritidaeAnastrepha ludensC[102]
Strumeta tryoniC[103]
TachinidaeExorista sorbillansB[104]
GlossindaeGlossina morsitans morsitansC[105]
DrosophilidaeDrosophila melanogasterB[106]
LepidopteraCrytophasidaeOpisina arenosellaA[107]
OlethreutidaeLaspeyresia caryanaA[51]
PyralidaeOstrinia nubilalisA[108]
TortricidaeChoristoneura fumiferanaA[53]
NoctuidaeTrichoplusia niA[109]
Pseudaletia unipunctaA[110]
Agrotis ipsilonA[111]
Heliothis aremigeraA[112]
Heliothis zeaA[113]
Spodoptera lituraA[114]
GeometridaeBoarmia selenariaA[115]
BombycidaeBombyx moriA[116]
SaturnidaeAntheraea pernyiA[117]

Table 1.

Classification of the male internal reproductive organs in various insects.

Figure 1.

Simple illustration of each type of configuration of male internal reproductive organs. TS, VD, SV, AG, and ED indicate testis, vas deferens, seminal vesicle, accessory gland, and ejaculatory duct, respectively. Arrow indicates the direction of ejaculates (semen or sperm).

In type A, ejaculates reach the seminal vesicle or duplex form the testis via the vas deferens, to which the accessory glands are open. Thus far, all lepidopteran insects studied represent type A. As the accessory gland material passes through the duplex during mating, it flushes out all sperm and semen in the duplex. This relies on constant daily sperm replenishment form the testis to support multiple matings. Type B is similar to type A, but the seminal vesicles differ in that they connect to the ejaculatory duct along with the accessory glands. Type B is common in the homopteran, coleopteran and dipteran insects. In these insects, sperm production is typically completed in the testes, and in contrast to the Lepidoptera, the sperm do not require the vas deferens to mature. Type C lacks the seminal vesicles, but is basically the same as type B and more common in dipteran insects. Similarly, mature sperm can immediately be ejaculated from the testes during mating. Type C is an effective arrangement for multiple matings by adult males. Type D is found in some weevil species, where both the seminal vesicles and accessory glands are connected to the ejaculatory duct via the vas deferens. Type E is found in cockroaches and orthopteran insects, and through the testes the vas deferens leads to the tubular accessory glands and tubular seminal vesicles, both of which lead to the ejaculatory duct. In Type F, the testes open into the vas deferens or seminal vesicles and then the ejaculatory duct. Some hymenopteran insects belong to type F. Types G and H represent those insects that lack the accessory glands.


7. Conclusion

The position, as well as the morphology, structure and function of the male internal reproductive organs, is presumably adaptive, probably for successful reproduction. The complex folds of these organs, which are surrounded by the tracheae and fat bodies, suggests that they require large amounts of oxygen and nutrients. However, until now, research on the arrangement of the reproductive organs has not been prioritized. We hope that this chapter will serve as an opportunity and foundation for studying not only the morphology, structure and function of reproductive organs, but also their positional relationships.



This work is supported by USDA-ARS Research Project# 6066-22000-091-00D - Ecologically Sustainable Approaches to Insect Resistance Management in Bt Cotton.


  1. 1. Dallai R: Overview on spermatogenesis and sperm structure of Hexapoda. Arthropod Structure & Development. 2014;43:257-290
  2. 2. Dallai R, Gottardo M, Beutel RG: Structure and evolution of insect sperm: New interpretations in the age of phylogenomics. 2016;61:1-23
  3. 3. Samani P: Digest: Evolution of sperm size and number in external fertilizers. Evolution. 2017;72:211-212
  4. 4. Hatsumi M, Wakahama KI: The sperm length and the testis length inDrosophila nasutasubgroup. Japanese Journal of Genetics. 1986;61:241-244
  5. 5. Joly D. Bressac C: Sperm length in Drosophilidae (Diptera): Estimation by testis and receptacle lengths. International Journal of Insect Morphology & Embryology. 1994;23:85-92
  6. 6. Pitnick S: Investment in testes and the cost of making long sperm inDrosophila. The American Naturalist. 1996;148:57-80
  7. 7. Gage MJG: Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proceedings of the Royal Society of London B. 1994;258:247-254
  8. 8. Joly D, Bazin C, Zeng LW, Singh RS: Genetic basis of sperm and testis length differences and epistatic effect on hybrid inviability and sperm motility betweenDrosophila simulansandD. sechellia. Heredity. 1995;78:354-362
  9. 9. Immler S, Pitnick S, Parker GA, Durrant KL, Lüpold S, Calhim S, Birkhead TR: Resolving variation in the reproductive tradeoff between sperm size and number. Proceedings of the National Academic Sciences of the United States of America. 2011;108:5325-5330
  10. 10. Mojica JM, Bruck DL: Sperm bundle coiling: Transporting long sperm bundles inDrosophila dunni dunni. Journal of Insect Physiology. 1996;42:303-307
  11. 11. Pizzari T: Evolution: sperm ejection near and far. Current Biology. 2004;14:R511-R513
  12. 12. Sepil I, Hopkins BR, Dean R, Bath E, Friedman S, Swanson B, Ostridge, HJ, Harper L, Buehner NA, Wolfner MF, Konietzny R, Thézénas ML, Sandham E, Charles PD, Fischer B, Steinhauer J, Kessler BM, Wigby S: Male reproductive aging arises via multifaceted mating-dependent sperm and seminal proteome declines, but is postponable inDrosophila. Proceedings of the National Academic Sciences of the United States of America. 2020;117:17094-17103
  13. 13. Strobl V, Sstraub L, Bruckner S, Albrecht M, Maitip J, Kolari E, Chantawannakul P, Williams GR, Neumann P: Not every sperm counts: Male fertility in solitary bees,Osmia cornuta. PLoS ONE. 2019;14:e0214597
  14. 14. Simmons LW, Lovegrove M: Socially cued seminal fluid gene expression mediates responses in ejaculate quality to sperm competition risk. Proceedings of the Royal Society B. 2017;284:1486
  15. 15. Hiroyoshi S: Regulation of sperm quantity transferring to females at mating in the adult male ofPolygonia c-aureum(Lepidoptera: Nymphalidae). Applied Entomology and Zoology. 1995;30:111-119
  16. 16. Sirot LK, Lapointe SL, Shatters R, Bausher M: Transfer and fate of seminal fluid molecules in the beetle,Diaprepes abbreviatus: Implications for the reproductive biology of a pest species. Journal of Insect Physiology. 2006;52:300-308
  17. 17. Chapman RF: SJ, Simpson SJ, Douglas AE, editors. The insects. Structure and function. 5th ed. UK: Cambridge University Press; 2013. 929p
  18. 18. Hiroyoshi S: Effects of aging, temperature and photoperiod on testis development ofPolygonia c-aureum(Lepidoptera: Nymphalidae). Entomological Science. 2000;3:227-236
  19. 19. Hiroyoshi S: Effects of photoperiod and age on the initiation of sperm movement in malePolygonia c-aureumLINNAEUS (Lepidoptera: Nymphalidae). Applied Entomology and Zoology. 1997;32:19-25
  20. 20. Hiroyoshi S, Reddy GVP, Mitsunaga T: Effects of photoperiod and aging on the adult spermatogenesis ofPolygonia c-aureum(Lepidoptera: Nymphalidae), in relation to adult diapause. Journal of Comparative Physiology A. 2020;206:467-475
  21. 21. Lai-Fook J: Testicular development and spermatogenesis inCalpodes ethliusStoll (Hesperiidae, Lepidoptera). Canadian Journal of Zoology. 1982;60:1161-1171
  22. 22. Dumser JB: The regulation of spermatogenesis in insects. Annual Review of Entomology. 1980;25:341-369
  23. 23. Droney DC: The influence of the nutritional content of the adult male diet on testis mass, body condition and courtship vigour in a HawaiianDrosophila. Functional Ecology. 1998;12:920-928
  24. 24. Ward PI, Simmons LW: Copula duration and testes size in the yellow dung fly,Scathophaga stercoraria(L.): the effects of diet, body size, and mating history. Behavioral Ecology and Sociobiology. 1991;29:77-85
  25. 25. Linklater JR, Wertheim B, Wigby S, Chapman T: Ejaculate depletion patterns evolve in response to experimental manipulation of sex ratio inDrosophila melanogaster. Evolution. 2007;61:2027-2034
  26. 26. Du Q , Wen L, Zheng SC, Bi HL, Huang YP, Feng QL, Liu L: Identification and functional characterization ofdoublesexgene in the testis ofSpodoptera litura. Insect Science. 2019;26:1000-1010
  27. 27. Laranjo LT, Haifig I, Costa-Leonardo AM: Morphology of the male reproductive system during post-embryonic development of the termiteSilvestritermes euamignathus(Isoptera: Termitidae). Zoologischer Anzeiger. 2018;272:20-28
  28. 28. Snook RR, Markow TA: Possible role of nonfertilizing sperm as a nutrient source for femaleDrosophila pseudoobscura frolova(Diptera: Drosophilidae). Pan-Pacific Entomologist. 1996;72:121-129
  29. 29. Snook, RR: Is the production of multiple sperm types adaptive? Evolution. 1997;51:797-808
  30. 30. Bressac C, Hauschteck-Jungen E:Drosophila subobscurafemales preferentially select long sperm for storage and use. Journal of Insect Physiology. 1996;42:323-328
  31. 31. Silbergried RE, Shepherd JG, Dickinson JL: Eunuchs: The role of apyrene sperm in Lepidoptera? The American Naturalist. 1984;123:255-265
  32. 32. Friedländer M, Seth RK, Reynolds SE: Eupyrene and apyrene sperm: Dichotomous spermatogenesis in Lepidoptera. Advanced Insect Physiology. 2005;32:206-308
  33. 33. Friedländer M, Miesel S: Spermatid anucleation during the normal atypical spermatogenesis of the warehouse mothEphestia cautella. Journal of Submicroscopic Cytology 1977;9:173-185
  34. 34. Mongue AJ, Hansen ME, Gu L, Sorenson CE, Walters JR: Nonfertilizing sperm in Lepidoptera show little evidence for recurrent positive selection. Molecular Ecology. 2019;28
  35. 35. Esfandi K, He XZ, Wang Q : Sperm allocation strategies in a sperm heteromorphic insect. Current Zoology. 2020;66:285-292
  36. 36. Chen S, Liu Y, Yang X, Liu Z, Luo X, Xu J, Huang Y: Dysfunction of dimorphic sperm impairs male fertility in the silkworm. Cell Discovery. 2020;6:60
  37. 37. Hiroyoshi S: Eupyrene and apyrene spermatogenesis in the Asian comma butterfly,Polygonia c-aureum(Lepidoptera: Nymphalidae). Entomological Science. 1999;2:297-305
  38. 38. TengZ-Q , Zhang Q-W: Determinants of male ejaculate investment in the cotton bollwormHelicoverpa armigera: mating history, female body size and male age. Physiological Entomology. 2009;34:338-344
  39. 39. Win AT, Ishikawa Y: Effects of diapause on post-diapause reproductive investment in the mothOstrinia scapulalis. Entomologia Experimentalis et Applicata. 2015;157:346-353
  40. 40. Li X, Zhang K, Deng Y, He R, Zhang X, Zhong G, Hu Q , Weng Q : Effects of 60Co-γirradiation on testis physiological aspects ofPlutella xylostella(Linnaeus). Ecotoxicology and Environmental Safety. 2019;169:937-943
  41. 41. Hiroyoshi S, Kohama T, Reddy GVP: Age-related sperm production, transfer, and storage in the sweet potato weevil,Cylas formicarius(Fabricius) (Coleoptera: Curculionidae). Journal of Insect Behavior. 2016;29:689-707
  42. 42. Hiroyoshi S, Reddy GVP, Kohama T: Sperm supply from the testes to the seminal vesicle over consecutive matings in the sweetpotato weevil,Cylas formicarius(FABRICIUS) (Coleoptera: Curculionidae). American Journal of Life Sciences. 2014;5:103-107
  43. 43. Giebultowicz JM, Riemann JG, Raina AK, Ridgway RL: Circadian system controlling release of sperm in the insect testes. Science. 1989;245:1098-1100
  44. 44. Bebas P, Maksimiuk E, Gvakharia B, Cymborowski B, Giebultowicz JM: Circadian rhythm of glycoprotein secretion in the vas deferens of the moth,Spodoptera littoralis. BMC Physiology. 2002;2:15
  45. 45. Flint HM, Kressin EL: Transfer of sperm by irradiatedHeliothis virescens(Lepidoptera: Noctuidae) and relationship to fecundity. The Canadian Entomologist. 1969;101:500-507
  46. 46. Drummond BA: Multiple mating and sperm competition in the Lepidoptera. In: Smith RL, editor. Sperm competition and the evolution of animal mating systems. London: Academic Press; 1984. P. 291-360
  47. 47. Rhainds M: Female mating failures in insects. Entomologia Experimentalis et Applicata.;2010;136:211-226
  48. 48. Balfour VL, Black D, Shuker, DM: Mating failure shapes the patterns of sperm precedence in an insect. Behavioral Ecology and Sociobiology. 2020;74:25
  49. 49. Adams EM, Wolfner MF: Seminal proteins but not sperm induce morphological changes in theDrosophila melanogasterfemale reproductive tract during sperm storage. Journal of Insect Physiology. 2007;53:319-331
  50. 50. Nalepa CA, Mullins DE: Repeated copulation in the wood-feeding cockroachCryptocercus punctulatusdoes not influence number or development of offspring. Journal of Insect Behavior. 2011;24:44-54
  51. 51. Tedders Jr WL, Calcote VR: Male and female reproductive systems ofLaspeyresia caryana, the hickory shuckworm moth (Lepidoptera: Olethreutidae). Annals of the Entomological Society of America. 1967;60:280-282
  52. 52. Tedders Jr WL, Osburn M: Morphology of the reproductive systems ofGretchena bolliana, the pecan bud moth. Annals of the Entomological Society of America. 1970;63:786-789
  53. 53. Outram I: Morphology and histology of the reproductive system of the male spruce budworm,Choristoneura fumiferana. The Canadian Entomologist. 1970;102:404-414
  54. 54. Ferro DN, Akre RD: Reproductive morphology and mechanics of mating of the codling moth,Laspeyresia pomonella. Annals of the Entomological Society of America. 1975;68:417-424
  55. 55. Boes KE, Ribeiro JMC, Wong A, Harrington LC, Wolfner MF, Sirot LK: Identification and characterization of seminal fluid proteins in the Asian tiger mosquito,Aedes albopictus. PLOS Neglected Tropical Diseases. 2014;8:e2946
  56. 56. Barcellos MS, Martins LCB, Cossolin JFS, Serrão JE, Delabie JHC, Lino-Neto J: Testes ant spermatozoa as characters for distinguishing two species of the genusNeoponera(Hymenoptera: Formicidae). Florida Entomologist. 2015;98:1254-1256
  57. 57. Bressac C, Khanh HDT, Chevrier C: Effects of age and repeated mating on male sperm supply and paternity in a parasitoid wasp. Entomologia Experimentalis et Applicata. 2009;130:207-213
  58. 58. Pickford R, Gillott C: Insemination in the migratory grasshopper,Melanoplus sanguinipes(Fabr.). Canadian Journal of Zoology. 1971;49:1583-1588
  59. 59. Barnhart Sr CS: The internal anatomy of the silverfishCtenolepisma campbelliandLepisma saccharinum(Thysanura: Lepismatidae). Annals of the Entomological Society of America. 1961;54:177-196
  60. 60. Brito P, Salles FF, Dolder H: Characteristics of the male reproductive system and spermatozoa of Leptophlebiidae (Ephemeroptera). Neotropical Entomology. 2011;40:103-107
  61. 61. Endoh S, Niwa N, Matsuzaki M: Comparative anatomy of the male reproductive organs and a brief description on the spermatozoon structure ofKamimuria quadrata(Plecoptera). Fukushima University. Science Report. 1995;56:13-23
  62. 62. Stewart KW, Atmar GL, Solon BM: Reproductive morphology and mating behavior ofPerlesta placida(Plecoptera: Perlidae). Annals of the Entomological Society of America. 1969;62:1433-1438
  63. 63. Kamimura Y: Right-handed penises of the earwigLabidura riparia(Insecta, Dermaptera, Labiduridae): Evolutionary relationships between structural and behavioral asymmetries. Journal of Morphology. 2006;267:1381-1389
  64. 64. van Lieshout E: Male genital length and mating status differentially affect mating behaviour in an earwig. Behavioral Ecology and Sociobiology. 2011;65:149-156
  65. 65. van Wyk LE: The morphology and histology of the genital organs of Leucophaea maderae (Fabr.) (Blattidae, Orthoptera). Journal of the Entomological Society of South Africa. 1952;15:1-62
  66. 66. Winnick CG, Holwell GI, Herberstein ME: Internal reproductive anatomy of the praying mantidCiulfina klassi(Mantodea: Liturgusidae). Arthropod Structure & Development. 2009;38:60-69
  67. 67. Silva DSM, Cossolin JFS, Pereira MR, Lino-Neto J, Sperber CF, Serrão JE: Male reproductive tract and spermatozoa ultrastructure in the grasshopperOrphulella punctata(De Geer, 1773) (Insecta, Orthoptera, Caelifera). Microscopy Research Technique. 2017:1-6
  68. 68. Widdows RE, Wick JR: Morphology of the reproductive system ofTetrix arenosa angusta(Hancock) (Orthoptera, Tetrigidae). Proceedings of the Iowa Academy of Science. 1959;66:484-503
  69. 69. Wagan MS, Pitafi KD: The anatomy and histology of male reproductive organs ofPoekilocerus pictus(Fabricius) (Pyrgomorphidae: Acridoidea: Orthoptera). Pakistan Journal of Zoology. 1990;22:117-121
  70. 70. Golub NV, Kučerová Z: Karyotype and reproductive organs of maleDorypteryx domestica(Smithers, 1958) (Psocoptera: Trogiomorpa: Psyllipsocidae). Folia biologica (Kraków). 2008;56:21-23
  71. 71. Kai WS, Thornton IWB: The internal morphology of the reproductive systems of some psocid species. Proceedings of the Royal Society of London (A). 1968;43:1-12
  72. 72. Tsai JH, Perrier JL: Morphology of the digestive and reproductive systems ofPeregrinus maidis(Homoptera: Delphacidae). Florida Entomologist. 1993;76:428-436
  73. 73. Tsai JH, Perrier JL: Morphology of the digestive and reproductive systems ofDalbulus maidisandGraminella nigrifrons(Homoptera: Cicadellidae). Florida Entomologist. 1996;79:563-578
  74. 74. Hayashi F, Kamimura Y: The potential for incorporation of male derived proteins into developing eggs in the leafhopperBothrogonia ferruginea. Journal of Insect Physiology. 2002;48:153-159
  75. 75. Moulds MS: An appraisal of the higher classification of cicadas (Hemiptera: Cicadoidea) with special reference to the Australian fauna. Records of the Australian Museum. 2005;57:375-446
  76. 76. Khalifa A: Spermatophore production and egg-laying behaviour inRhodnius prolixusStal. (Hemiptera; Reduviidae). Parasitology. 1950;40:283-289
  77. 77. Adams TS: Morphology of the internal reproductive system of the male and female two-spotted stink bug,Perillus bioculatus(F.) (Heteroptera: Pentatomidae) and the transfer of products during mating. Invertebrate Reproduction and Development. 2001;39:45-53
  78. 78. Wieczorek K, Kanturski M, Sempruch C, Świątek P: The reproductive system of the male and oviparous female of a model organism-the pea aphid, Acythosiphon pisum (Hemiptera, Aphididae). PeerJ. 2019;7:e7573
  79. 79. Ferreira A, Avdalla FC, Kerr WE, da Cruz-Landim C: Comparative anatomy of the male reproductive internal organs of 51 species of bees. Neotropical Entomology. 2004;33:569-576
  80. 80. Araújo VA, Freitas FV, Moreira J, Neves CA, Lino-Neto J.: Morphology of male reproductive system of two solitary bee species (Hymenoptera: Apidae). Neotropical Entomology. 2010;39
  81. 81. Wilkes A: Sperm transfer and utilization by the arrhenotokous waspDahlbominus fuscipennis(Zett.) (Hymenoptera: Eulophidae). The Canadian Entomologist. 1965;97:647-657
  82. 82. Ball DE, Vinson SB: Anatomy and histology of the male reproductive system of the fire ant,Solenopsis invictaBuren (Hymenoptera: Formicidae). International Journal of Insect Morphology & Embryology. 1984;13:283-294
  83. 83. Hwang JC, Bickley WE: The reproductive system ofChrysopa oculata(Neuroptera: Chrysopidae). Annals of the Entomological Society of America. 1961;54:422-427
  84. 84. de Jong GD: Observations on the biology ofPolystoechotes punctatus(Fabricius) (Neuroptera: Ithonidae): Adult trophic status, description of the male reproductive system, and associations with mites. Proceedings of the Entomological Society of Washington. 2011;113:291-298
  85. 85. Walker MH, Picker MD, Leon B: Eversible abdominal vesicles and some observations of the male reproductive system of the spoon wing lacewingPalmipenna(Neuropera: Nemopteridae). Journal of Morphology. 1994;219:47-58
  86. 86. Hayashi F: Insemination through an externally attached spermatophore: Bundled sperm and post-copulatory mate guarding by male fishflies (Megaloptera: Corydalidae). Journal of Inset Physiology. 1996;42:859-866
  87. 87. Yahiro K: Comparative morphology of the alimentary canal and reproductive organs of the terrestrial Caraboidea (Coleoptera: Adephaga) Part 1. Japanese Journal of Entomology. 1996;64:536-550
  88. 88. Yahiro K: Comparative morphology of the alimentary canal and reproductive organs of the terrestrial Caraboidea (Coleoptera: Adephaga) Part 2.Entomological Science. 1998;1:47-53
  89. 89. Brits JA: The anatomy, histology and physiology of the internal adult male reproductive system ofParastizopus armaticepsPéringuey (Coleoptera: Tenebrionidae). Journal of the Entomological Society of south Africa. 1982;45:239-260
  90. 90. Williams JL: The anatomy of the internal genitalia of some Coleoptera. Proceedings of the Entomological Society of Washington. 1945;47:73-91
  91. 91. Verma KK: Functional and developmental anatomy of the reproductive organs in the male ofGalerucella birmanicaJac (Coleoptera, Phytophaga, Chrysomelidae). Annales des Sciences Naturelles, Zoologie, Paris. 1969;12:139-234
  92. 92. Smid HM: Transfer of a male accessory gland peptide to the female during mating inLeptinotarsa decemlineata. Invertebrate Reproduction and Development. 1998;34:47-53
  93. 93. Klopfenstein WG, Graves RC: Morphology of the digestive and reproductive systems of adultHadraule blaisdelli(Casey) (Coleoptera: Ciidae). The Coleoptersist Bulletin. 1992;46:344-356
  94. 94. Burke HR: Morphology of the reproductive systems of the cotton boll weevil (Coleoptera, Curculionidae). Annals of the Entomological Society of America. 1959;52:287-294
  95. 95. Wu YF, Wei LS, Torres MA, Zhang X, Wu S-P, Chen H: Morphology of the male reproductive system and spermiogenesis ofDendroctonus armandi(Coleoptera: Curculionidae: Scolytinae). Journal of Insect Science. 2017;17:1-9
  96. 96. Glitho IA, Huignard J: A histological and ultrastructural comparison of the male accessory reproductive glands of diapausing and non-diapausing adults inBruchidius atrolineatus(Pic) (Coleoptera: Bruchidae). International Journal of Insect Morphology & Embryology. 1990;19:195-209
  97. 97. Calder AA: Gross morphology of the soft parts of the male and female reproductive systems of Curculionoidea (Coleoptera). Journal of Natural History. 1990;24:453-505
  98. 98. Mead-Briggs AR: The structure of the reproductive organs of the European rabbit-flea,Spilopsyllus cuniculi(Dale) (Siphonaptera). Proceedings of the Royal Society of London (A). 1962;37:79-88
  99. 99. Huho BJ, Ng’habi KR, Killeen GF, Nkwengulila G, Knols BGJ. Ferguson HM: A reliable morphological method to assess the age of maleAnopheles gambiae. Malaria Journal. 2006;5:62
  100. 100. Meuti ME, Short SM: Physiological and environmental factors affecting the composition of the ejaculate in mosquitoes and other insects. Insects 2019;10:74
  101. 101. Spiegel CN, Bretas JAC, Peixoto AA, Vigoder FM, Bruno RV, Soares MJ: Fine structure of the male reproductive system and reproductive behavior ofLutzomyia longipalpissandflies (Diptera: Psychodidae: Phlebotominae). PLoS ONE. 2013:8:e74898
  102. 102. Valdez JM: Ultrastructure of the testis of the Mexican fruit fly (Diptera: Tephritidae). Annals of the Entomological Society of America. 2001;94:251-256
  103. 103. Drew RAI: Morphology of the reproductive system ofStrumeta tryoni(Froggatt) (Diptera: Trypetidae) with a method of distinguishing sexually mature adult males. Journal of the Australian Entomological Society; 1969;8:21-32
  104. 104. Veeranna G, Prasad NR: Reproductive biology of uzi flyExorista sorbillans(Diptera: Tachinidae). In: Recent advances in uzi fly research; 16-17 January 1992; Bangalore, India; 1993.p13-22
  105. 105. Odhiambo TR, Kokwaro ED, Sequeira LM: Histochemical and ultrastructural studies of the male accessory reproductive glands and spermatophore of the tsetse,Glossina morsitans morsitansWestwood. Insect Science and its Application. 1983;4:227-236
  106. 106. Ram KR, Wolfner MF: Seminal influences:DrosophilaAcps and the molecular interplay between males and females during reproduction. Integrative and Comparative Biology. 47;2007:427-445
  107. 107. Santhosh-Babu PB: Development and differentiation of male reproductive organs inOpisina arenosellaWalker. Entomon. 1995;20:59-66
  108. 108. Jones JA, Guthrie WD, Brindley TA: Postembryonic development of the reproductive system of male European corn bores,Ostrinia nubilalis(Lepidoptera: Pyralidae). Annals of the Entomological Society of America. 1984;77:155-164
  109. 109. Holt GG, North DT: Effects of gamma irradiation on the mechanisms of sperm transfer inTrichoplusia ni. Journal of Insect Physiology. 1970;16:2211-2222
  110. 110. Callahan PS, Chapin JB: Morphology of the reproductive systems and mating in two representative members of the family Noctuidae,Pseudaletia unipunctaandPeridroma margaritosa, with comparison toHeliothis zea. Annals of the Entomological Society of America. 1960;53:763-782
  111. 111. Gemeno C, Anton S, Zhu JW, Haynes KF: Morphology of the reproductive system and antennal lobes of gynandromorphic and normal black cutworm moths,Agrotis ipsilon(Hufnagel) (Lepidoptera: Noctuidae). International Journal of Insect Morphology & Embryology. 1998;27:185-191
  112. 112. Hoque MR: Comparative morphology of the reproductive systems ofHeliothis armigera(Hubner) andHeliothis punctigeraWallengren (Lepidoptera: Noctuidae). Bangladesh Journal of Zoology. 1992;20:17-26
  113. 113. Callahan PS: Serial morphology as a technique for determination of reproductive patterns in the corn earworm,Heliothis zea(Boddie). Annals of the Entomological Society of America. 1958;51:413-428
  114. 114. Etman AAM, Hooper GHS: Developmental and reproductive biology ofSpodoptera litura(F.) (Lepidoptera: Noctuidae). Journal of the Australian Entomological Society. 1979;18:363-372
  115. 115. Scheepens MHM, Wysoki M: Reproductive organs of the giant looper,Boarmia selenariaSchiffermüller (Lepidoptera: Geometridae). International Journal of Insect Morphology & Embryology. 1986;15:73-81
  116. 116. Omura S: Studies on the reproductive system of the male ofBombyx mori, IV.Post-testicular organs and post-testicular behaviour of the spermatozoa. Journal of Faculty of Agriculture of Hokkaido Imperial University Sapporo. 1938;40:129-170
  117. 117. Shepherd JG: Activation of saturniid moth sperm by a secretion of the male reproductive tract. Journal of Insect Physiology. 1974;20:2107-2122

Written By

Satoshi Hiroyoshi and Gadi V.P. Reddy

Submitted: April 21st, 2021 Reviewed: June 9th, 2021 Published: July 4th, 2021