A male bed bug (Cimex lectularius) traumatically inseminates a female bed bug (top). The female's ventral exoskeleton is visibly cracked around the point of insemination.
Traumatic insemination, also known as hypodermic insemination, is the matingpractice in some species of invertebrates in which the male pierces the female's abdomen with his aedeagus and injects his sperm through the wound into her abdominal cavity (hemocoel).[1] The sperm diffuses through the female's hemolymph, reaching the ovaries and resulting in fertilization.
The process is detrimental to the female's health. It creates an open wound which impairs the female until it heals, and is susceptible to infection. The injection of sperm and ejaculatory fluids into the hemocoel can also trigger an immune reaction in the female. Bed bugs, which reproduce solely by traumatic insemination, have evolved a pair of sperm-receptacles, known as the spermalege. It has been suggested that the spermalege reduces the direct damage to the female bed bug during traumatic insemination. However experiments found no conclusive evidence for that hypothesis; as of 2003, the preferred explanation for that organ is hygienic protection against bacteria.[2]
The evolutionary origins of traumatic insemination are disputed. Although it evolved independently in many invertebrate species, traumatic insemination is most highly adapted and thoroughly studied in bed bugs, particularly Cimex lectularius.[1][3] Traumatic insemination is not limited to male-female couplings, or even couplings of the same species. Both homosexual and inter-species traumatic inseminations have been observed.
Mechanics
The aedeagus of a Callosobruchus analisbean weevil. Some species of insect have evolved aedeagal spines, which damage the female reproductive tract. This has led to females using various techniques to resist mating.Video of traumatic insemination in Stylops ovinae (Strepsiptera)
In humans and other vertebrates, blood and lymph circulate in two different systems, the circulatory system and lymphatic system, which are enclosed by systems of capillaries, veins, arteries, and nodes. This is known as a closed circulatory system. Insects, however, have an open circulatory system in which blood and lymph circulate unenclosed, and mix to form a substance called hemolymph. All organs of the insect are bathed in hemolymph, which provides oxygen and nutrients to all of the insect's organs.[4]
Following traumatic insemination, sperm can migrate through the hemolymph to the female's ovaries, resulting in fertilization. The exact mechanics vary from taxon to taxon. In some orders of insects, the male genitalia (paramere) enters the female's genital tract, and a spine at its tip pierces the wall of the female's bursa copulatrix. In others, the male penetrates the outer body wall. In either case, following penetration, the male ejaculates into the female. The sperm and ejaculatory fluids diffuse through the female's hemolymph. The insemination is successful if the sperm reach the ovaries and fertilize an ovum.[1]
Female resistance to traumatic insemination varies from one species to another. Females from some genera, including Cimex, are passive prior to and during traumatic insemination.[5] Females in other genera resist mating and attempt to escape.[6] This resistance may not be an aversion to pain caused by the insemination, as observational evidence suggests that insects do not feel pain.[7]
Research into the paternity of offspring produced by traumatic insemination has found "significant" last-sperm precedence. That is, the last male to traumatically inseminate a female tends to sire most of the offspring from that female.[8]
Many reasons for the evolutionary adaptation of traumatic insemination as a mating strategy have been suggested. One is that traumatic insemination is an adaptation to the development of the mating plug, a reproductive mechanism used by many species. Once a male finishes copulating, he injects a glutinous secretion into the female's reproductive tract, thereby "literally glu[ing] her genital tract closed".[9] Traumatic insemination allows subsequent males to bypass the female's plugged genital tract, and inject sperm directly into her circulatory system.
Others have argued that the practice of traumatic insemination may have been an adaptation for males to circumvent female resistance to mating[1] to eliminate courtship time, allowing one male to inseminate many mates when contact between them is brief;[10] or that it evolved as a new development in the sperm competition as a means to deposit sperm as close to the ovaries as possible.
This bizarre method of insemination probably evolved as male bed bugs competed with each other to place their sperm closer and closer to the mother lode of eggs, the ovaries. Some male insects evolved long penises with which they enter the vagina but bypass the female's storage pouch and deposit their sperm further upstream close to the ovaries. A few males, notably among bed bugs, evolved traumatic insemination instead, and eventually this strange procedure became the norm among these insects.[11]
It has recently been discovered that members of the plant bug genus Coridromius (Miridae) also practice traumatic insemination. In these bugs, the male intromittent organ is formed by the coupling of the aedeagus with the left paramere, as in bed bugs. Females also exhibit paragenital modifications at the site of intromission, which include grooves and invaginated copulatory tubes to guide the male paramere. The evolution of traumatic insemination in Coridromius represents a third independent emergence of this form of mating within the true bugs.[12]
Health repercussions
While advantageous to the reproductive success of the individual male, traumatic insemination imposes a cost on females: reduced lifespan and decreased reproductive output. "These [costs] include (i) repair of the wound, (ii) leakage of blood, (iii) increased risk of infection through the puncture wound, and (iv) immune defence against sperm or accessory gland fluids that are introduced directly into the blood."[1]
The successive woundings each require energy to heal, leaving less energy available for other activities. Also, the wounds provide a possible point of infection which can reduce the female's lifespan.[8] Once in the hemolymph, the sperm and ejaculatory fluids may act as antigens, triggering an immune reaction.
There is a tendency for dense colonies of bed bugs kept in laboratories to go extinct, starting with adult females.[14] In such an environment, where mating occurs frequently, this high rate of adult female mortality suggests traumatic insemination is very detrimental to the female's health.[1] The damage done, and the (unnecessarily) high mating rate of captive bed bugs, have been shown to cause a 25% higher-than-necessary mortality rate for females.[15]
Bed bug adaptation
A traumatically inseminated female bed bug
The effects of traumatic insemination are deleterious to the female. Female bed bugs have evolved a pair of specialized reproductive organs ("paragenitalia") at the site of penetration. Known as the ectospermalege and mesospermalege (referred to collectively as spermalege), these organs serve as sperm-receptacles from which sperm can migrate to the ovaries.[2][16] All bed bug reproduction occurs via traumatic insemination and the spermalege. The genital tract, though functional,[17] is used only for laying fertilized eggs.[3]
The ectospermalege is a swelling in the abdomen, often folded, filled with hemocytes. The ectospermalege is visible externally in most bed bug species, giving the male a target through which to impale the female with the paramere. In species without an externally visible ectospermalege, traumatic insemination takes place over a wide range of the body surface.[17]
Exactly why males 'comply' with this aspect of female control over the site of mating is unclear, especially as male P. cavernis appear to be able to penetrate the abdomen at a number of points independent of the presence of an ectospermalege. One possibility is that mating outside the ectospermalege reduces female fecundity to such an extent that the mating male's paternity is significantly reduced ... The ectospermalege appears to act as a mating guide, directing the male's copulatory interest, and therefore damage, to a restricted area of the female's abdomen.[17]
The mesospermalege is a sac attached to the inner abdomen, under the ectospermalege. Sperm is injected through the male's aedeagus into the mesospermalege. In some species, the ectospermalege directly connects to the ovaries – thus, sperm and ejaculate never enters the hemolymph and thus never trigger an immune reaction. (The exact characteristics of the spermalege vary widely across different species of bed bugs.)[1] The spermalege are generally found only in females. However, males in the genus Afrocimex possess an ectospermalege.[1] Sperm remains in the spermalege for approximately four hours; after two days, none remains.[3]
Male bed bugs have evolved chemoreceptors on their aedeagi. After impaling a female, the male can "taste" if a female has been recently mated. If he does, he will not copulate as long and will ejaculate less fluid into the female.[18]
Use in the animal kingdom
Although traumatic insemination is most widely practiced among heteropterans (typical bugs), the phenomenon has been observed across a wide variety of other invertebrate taxa. These include:
Acanthocephala (parasitic, thorny-headed worms) – The presence of mating plugs on the sides of Pomphorhynchus bulbocolli suggests traumatic insemination occurs in this species. Because these parasites cannot move after anchoring themselves to a host's intestine, traumatic insemination may have evolved to compensate for their immobility.[1][21]
Rotifera (wheel animalcules) – In the genus Brachionus, the male pierces the syncytialintegument (equivalent to skin) and injects sperm; in Asplanchna brightwelli the male secretes an enzyme which breaks down the female integument and injects sperm through the hole.[22][23]
Turbellaria (free living flatworms) – Hermaphroditic flatworms reproduce by "penis fencing". Individuals "fence" with penises, attempting to use their penis to pierce the skin of the other and inject sperm. The 'loser' is the flatworm which is inseminated and must bear the energy costs of reproduction. One study of Pseudoceros bifurcus found "Most inseminations were unilateral. Even when reciprocal penis insertion could be achieved by the second partner, the first to inseminate obtained a longer injection time than the second."[24][25] In another species, Macrostomum hystrix, the worm may also inject its sperm into its own head if other mates are not available.[26]
Strepsiptera (twisted-winged parasites) – In Xenos vesparum, fertilization can occur either via extragenital ducts, or by traumatic insemination into the hemocoel.[27]
Drosophila (fruit flies) – Ejaculates are injected through the body wall into the genital tract, not the abdomen.[28]
Opisthobranchia (sea slugs) – Characterized by "repeated small injections into the dorsal surface of the partner, interrupted by synchronised circling movements", culminating in a standard genital insemination.[29]
Harpactea (spiders) – The male of the spider species Harpactea sadistica pierces the female's body cavity and inseminates her ovaries directly.[30]
In the genus Afrocimex, both species have well developed ectospermalege (but only females have a mesospermalege). The male ectospermalege is slightly different from that found in females, and amazingly enough, Carayon (1966) found that male Afrocimex bugs suffer actual homosexual traumatic inseminations. He found the male ectospermalege often showed characteristic mating scars, and histological studies showed "foreign" sperm were widely dispersed in the bodies of these homosexually mated males. Sperm cells of other males were, however, never found in or near the male reproductive tract. It therefore seems unlikely that sperm from other males could be inseminated when a male that has himself suffered traumatic insemination mates with a females. The costs and benefits, if any, of homosexual traumatic insemination in Afrocimex remain unknown.[1]
Klaus Reinhardt of the University of Sheffield and colleagues observed two morphologically different kinds of spermalege in Afrocimex constrictus, a species in which both male and females are traumatically inseminated. They found females use sexual mimicry as a way to avoid traumatic insemination. In particular, they observed males, and females who had male spermalege structures, were inseminated less often than females with female spermalege structures.[31]
In Xylocoris maculipennis, after a male traumatically inseminates another male, the injected sperm migrate to the testes. (The seminal fluid and most of the sperm are digested, giving the inseminated male a nutrient-rich meal.) It has been suggested, although there is no evidence, that when the inseminated male ejaculates into a female, the female receives both males' sperm.[32][33]
Interspecies traumatic insemination
Cases of traumatic insemination between animals of different species will sometimes provoke a possibly lethal immune reaction. A female Cimex lectularius traumatically inseminated by a male C. hemipterus will swell up at the site of insemination as the immune system responds to male ejaculates. In the process, the female's lifespan is reduced. In some cases, this immune reaction can be so massive as to be almost immediately fatal. A female Hesperocimex sonorensis will swell up, blacken, and die within 24–48 hours after being traumatically inseminated by a male H. cochimiensis.[1]
In the animal kingdom, traumatic insemination is not unique as a form of coercive sex. Research suggests that in the water beetle genus Acilius there is no courtship system between males and females. "It's a system of rape. But the females don't take things quietly. They evolve counter-weapons." Cited mating behaviors include males suffocating females underwater till exhausted, and allowing only occasional access to the surface to breathe for up to six hours (to prevent them breeding with other males), and females which have a variety of body shapes (to prevent males from gaining a grip). Foreplay is "limited to the female desperately trying to dislodge the male by swimming frantically around."[34]
"Rape behavior" has been observed in a number of duck species. In the blue-winged teal, "rape attempts by paired males may occur at any time during the breeding season." Cited reasons for this being beneficial to the paired males include successful reproduction, and chasing away intruders from their territory.[35]Bachelor herds of bottlenose dolphins will sometimes gang up on a female and coerce her to have sex with them, by swimming near her, chasing her if she attempts to escape, and making vocalized or physical threats.[36][37] In the insect world, male water striders unable to penetrate her genital shield, will draw predators to a female until she copulates.[38]
Sex is the trait that determines whether a sexually reproducing organism produces male or female gametes. During sexual reproduction, a male and a female gamete fuse to form a zygote, which develops into an offspring that inherits traits from each parent. By convention, organisms that produce smaller, more mobile gametes are called male, while organisms that produce produce larger, non-mobile gametes are called female. An organism, such as most flowering plants, that produces both types of gamete is a hermaphrodite.
In biology, mating is the pairing of either opposite-sex or hermaphroditic organisms for the purposes of sexual reproduction. Fertilization is the fusion of two gametes. Copulation is the union of the sex organs of two sexually reproducing animals for insemination and subsequent internal fertilization. Mating may also lead to external fertilization, as seen in amphibians, fishes and plants. For most species, mating is between two individuals of opposite sexes. However, for some hermaphroditic species, copulation is not required because the parent organism is capable of self-fertilization (autogamy); for example, banana slugs.
Sperm competition is the competitive process between spermatozoa of two or more different males to fertilize the same egg during sexual reproduction. Competition can occur when females have multiple potential mating partners. Greater choice and variety of mates increases a female's chance to produce more viable offspring. However, multiple mates for a female means each individual male has decreased chances of producing offspring. Sperm competition is an evolutionary pressure on males, and has led to the development of adaptations to increase male's chance of reproductive success. Sperm competition results in a sexual conflict between males and females. Males have evolved several defensive tactics including: mate-guarding, mating plugs, and releasing toxic seminal substances to reduce female re-mating tendencies to cope with sperm competition. Offensive tactics of sperm competition involve direct interference by one male on the reproductive success of another male, for instance by physically removing another male's sperm prior to mating with a female. For an example, see Gryllus bimaculatus.
The Cimicidae are a family of small parasitic bugs that feed exclusively on the blood of warm-blooded animals. They are called cimicids or, loosely, bed bugs, though the latter term properly refers to the most well-known member of the family, Cimex lectularius, the common bed bug and its tropical relation Cimex hemipterus. The family contains over 100 species. Cimicids appeared in the fossil record in the Cretaceous period. When bats evolved in the Eocene, Cimicids switched hosts and now feed mainly on bats or birds. Members of the group have colonised humans on three occasions.
Penis fencing is a mating behavior engaged in by many species of flatworm, such as Pseudobiceros hancockanus. Species which engage in the practice are hermaphroditic; each individual has both egg-producing ovaries and sperm-producing testes.
Sexual conflict or sexual antagonism occurs when the two sexes have conflicting optimal fitness strategies concerning reproduction, particularly over the mode and frequency of mating, potentially leading to an evolutionary arms race between males and females. In one example, males may benefit from multiple matings, while multiple matings may harm or endanger females, due to the anatomical differences of that species. Sexual conflict underlies the evolutionary distinction between male and female.
In human anatomy, the penis is an external male sex organ that additionally serves as the urinary duct. The main parts are the root (radix); the body (corpus); and the epithelium of the penis including the shaft skin and the foreskin (prepuce) covering the glans penis. The body of the penis is made up of three columns of tissue: two corpora cavernosa on the dorsal side and corpus spongiosum between them on the ventral side. The human male urethra passes through the prostate gland, where it is joined by the ejaculatory duct, and then through the penis. The urethra traverses the corpus spongiosum, and its opening, the meatus, lies on the tip of the glans penis. It is a passage both for urination and ejaculation of semen.
Xenos vesparum is a parasitic insect species of the order Strepsiptera that are endoparasites of paper wasps in the genus Polistes that was first described in 1793. Like other members of this family, X. vesparum displays a peculiar lifestyle, and demonstrates extensive sexual dimorphism.
Cimex is a genus of insects in the family Cimicidae. Cimex species are ectoparasites that typically feed on the blood of birds and mammals. Two species, Cimex lectularius and Cimex hemipterus, are known as bed bugs and frequently feed on humans, although other species may parasitize humans opportunistically. Species that primarily parasitize bats are known as bat bugs.
Afrocimex constrictus, also called the African bat bug, is an insect parasite of Egyptian fruit bats in bat caves in East Africa. Population sizes can comprise millions of individuals and in a cave there can be one to 15 bugs per bat. It was estimated that adult African bat bugs feed approximately once per week thus withdrawing 1-28 microlitre blood per day per bat.
The reproductive system of an organism, also known as the genital system, is the biological system made up of all the anatomical organs involved in sexual reproduction. Many non-living substances such as fluids, hormones, and pheromones are also important accessories to the reproductive system. Unlike most organ systems, the sexes of differentiated species often have significant differences. These differences allow for a combination of genetic material between two individuals, which allows for the possibility of greater genetic fitness of the offspring.
The spermalege is a special-purpose organ found in female bed bugs that appears to have evolved to mitigate the effects of traumatic insemination. The spermalege has two embryologically distinct parts, known as the ectospermalege and mesospermalege. The evolution of the spermalege as a female counter-adaptation for traumatic insemination was proposed by the French entomologist Jacques Carayon in 1966.
Harpactea sadistica is a species of dysderine spider, found only in Israel. It was first described in 2008.
An intromittent organ is any external organ of a male organism that is specialized to deliver sperm during copulation. Intromittent organs are found most often in terrestrial species, as most non-mammalian aquatic species fertilize their eggs externally, although there are exceptions. For many species in the animal kingdom, the male intromittent organ is a hallmark characteristic of internal fertilization.
Female sperm storage is a biological process and often a type of sexual selection in which sperm cells transferred to a female during mating are temporarily retained within a specific part of the reproductive tract before the oocyte, or egg, is fertilized. This process takes place in some species of animals, but not in humans. The site of storage is variable among different animal taxa and ranges from structures that appear to function solely for sperm retention, such as insect spermatheca and bird sperm storage tubules, to more general regions of the reproductive tract enriched with receptors to which sperm associate before fertilization, such as the caudal portion of the cow oviduct containing sperm-associating annexins. Female sperm storage is an integral stage in the reproductive process for many animals with internal fertilization. It has several documented biological functions including:
Sexual antagonistic co-evolution is the relationship between males and females where sexual morphology changes over time to counteract the opposite's sex traits to achieve the maximum reproductive success. This has been compared to an arms race between sexes. In many cases, male mating behavior is detrimental to the female's fitness. For example, when insects reproduce by means of traumatic insemination, it is very disadvantageous to the female's health. During mating, males will try to inseminate as many females as possible, however, the more times a female's abdomen is punctured, the less likely she is to survive. Females that possess traits to avoid multiple matings will be more likely to survive, resulting in a change in morphology. In males, genitalia is relatively simple and more likely to vary among generations compared to female genitalia. This results in a new trait that females have to avoid in order to survive.
The study of the genitalia of Lepidoptera is important for Lepidoptera taxonomy in addition to development, anatomy and natural history. The genitalia are complex and provide the basis for species discrimination in most families and also in family identification. The genitalia are attached onto the tenth or most distal segment of the abdomen. Lepidoptera have some of the most complex genital structures in the insect groups with a wide variety of complex spines, setae, scales and tufts in males, claspers of different shapes and different modifications of the ductus bursae in females.
Cryptic female choice is a form of mate choice which occurs both in pre and post copulatory circumstances when females in certain species use physical or chemical mechanisms to control a male's success of fertilizing their ova or ovum; i.e. by selecting whether sperm are successful in fertilizing their eggs or not. It occurs in internally-fertilizing species and involves differential use of sperm by females when sperm are available in the reproductive tract.
Lyctocoridae is a reconstituted family of bugs, formerly classified within the minute pirate bugs of the family Anthocoridae. It is widely distributed, with one species, being cosmopolitan.
Michael 'Mike' Siva-Jothy is an entomologist in the UK, he is Professor of Entomology at the University of Sheffield.
↑ Ruck, B.N.; Villares, G.J.; Welch, C.M.; Facey, D.E. "Circulatory System". Saint Michael's College. Archived from the original on June 19, 2009. Retrieved 2009-08-19.
↑ Arnqvist, citing A.D. Stutt, Reproductive Strategies and Sexual Conflict in the Bed Bug. PhD thesis. University of Sheffield, England.
↑ Arnqvist 89, citing personal observations and Monograph of Cimicidae
↑ Smith, Jane A. (1991). "A Question of Pain in Invertebrates". ILAR Journal. 33 (1–2): 25–31. doi:10.1093/ilar.33.1-2.25. Archived from the original on April 18, 2009. Retrieved 2009-04-07. In the majority of examples of invertebrate nociception noted above, there seems to be little, if any, evidence that the animals' responses persist in anything akin to the manner described for mammals. As Eisemann et al. (1984) have described in a review of the 'biological evidence' concerning pain in insects, 'No example is known to us of an insect showing protective behavior towards injured parts, such as by limping after leg injury or declining to feed or mate because of general abdominal injuries. On the contrary, our experience has been that insects will continue with normal activities even after severe injury or removal of body parts.'... Certainly, on the limited amount of evidence presented here, it seems very difficult to imagine that insects and the other simpler invertebrates mentioned above can 'suffer' pain in anything like the vertebrate sense. Nevertheless, the issue certainly is not closed, and further questions should be asked.{{cite journal}}: CS1 maint: unfit URL (link)
↑ Trowbridge, C. D. (1995). "Hypodermic insemination, oviposition, and embryonic development of a pool-dwelling ascoglossan (=sacoglossan) opisthobranch: Ercolania felina (Hutton, 1882) on New Zealand shores". The Veliger. 38: 203–211.
↑ Reinhardt, Klaus; Naylor, Richard A.; Siva-Jothy, Michael T. (2005-09-21). "Potential sexual transmission of environmental microbes in a traumatically inseminating insect". Ecological Entomology. 30 (5): 607–611. doi:10.1111/j.0307-6946.2005.00730.x. S2CID84344485.
↑ Hugot, JP (1982-04-19). "Traumatic insemination and tubular egg receptacle in the pinworm [Passalurus ambigus] parasite of the common domestic rabbit". Comptes Rendus de l'Académie des Sciences, Série III. 294 (14): 707–10.
↑ Doyle, Lester R.; Larry N. Gleason (June 1991). "Suckers and Other Bursal Structures of Pomphorhynchus bulbocolli and Acanthocephalus dirus (Acanthocephala)". The Journal of Parasitology. 77 (3): 437–40. doi:10.2307/3283132. JSTOR3283132. PMID2040955.
↑ Wallace, R. L. (1998). "Rotifera". In Knobil, Ernst; Neill, Jimmy D (eds.). Encyclopedia of Reproduction. Boston: Academic Press. pp.290–301. ISBN978-0-12-227020-8.
↑ Reinhardt, Klaus; Ewan Harney; Richard Naylor; Stanislav Gorb; Michael T. Siva‐Jothy (2007). "Female‐Limited Polymorphism in the Copulatory Organ of a Traumatically Inseminating Insect". American Naturalist. 170 (6): 931–35. doi:10.1086/522844. PMID18171174. S2CID21552124.
↑ Krebs, John R.; Davies, Nicholas B. (1993). An Introduction to Behavioural Ecology. Wiley-Blackwell. p.186. ISBN978-0-632-03546-5., citing Carayon, J. (1974). "Insemination traumatique heterosexuelle et homosexuelle chez Xylocoris maculipennis (Hem., Anthocoridae)". Comptes Rendus de l'Académie des Sciences. 278: 2803–06.
↑ Connor, Richard C.; F. Andrew; Rachel A. Smolker; Janet Mann (February 1996). "Patterns of Female Attractiveness in Indian Ocean Bottlenose Dolphins". Behaviour. 133 (1/2): 37–69. doi:10.1163/156853996X00026.
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