Traumatic insemination: Difference between revisions

Traumatic insemination, also known as hypodermic insemination, is the mating practice in some species of invertebrates in which the male pierces the female's abdomen with his penis and injects his sperm through the wound into her abdominal cavity (hemocoel).^[1] Although traumatic insemination evolved independently in many species, it is most highly adapted and thoroughly studied in bedbugs, particularly Cimex lectularius.^{[1] [2]}

Traumatic insemination is detrimental to the female's health. It creates an open wound, requiring energy to heal and impairing the female until it does. The wound can become infected, or the injection of sperm and ejaculatory fluids into the hemocoel can trigger an immune reaction in the female. Bedbugs, which reproduce solely by traumatic insemination, have evolved a pair of sperm-receptacles, known as the spermalege. The spermalege reduce the damage inflicted by traumatic insemination.

Traumatic insemination is not limited to male-female couplings, or couplings of the same species. Both homosexual and inter-species traumatic inseminations have been observed.

Traumatic insemination has been likened to sadomasochism, stabbing, and rape.^[3] However, such coercive sex practices are common in nature.

Although the practice is most widely practiced among heteropteran insects, other taxa in which traumatic insemination has been observed include:

• Pinworms ^{[1] [4]}
• Acanthocephalans ^[1]
• Rotifers ^[1]
• Free living flatworms ^[1]
• Gastropod snails ^[1]
• Strepsiptera ^[1] —In Xenos vesparum, fertilization can occur either via extragenital ducts, or by traumatic insemination into the hemocoel.^[5]
• Drosophila ^[6] —Ejaculates are injected through the body wall into the genital tract, not the abdomen.
• Leaf bugs ^[7] —Traumatic insemination occurs at the bursa copularix.
• Sea slugs ^[8] —Characterized by "repeated small injections into the dorsal surface of the partner, interrupted by synchronised circling movements", culminating in a standard genital insemination.

In humans and other complex life forms, blood and lymph circulate in two different systems, the circulatory system and lymphatic system. This is known as a closed circulatory system. Insects, however, have an open circulatory system in which blood and lymph 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. Following insemination, sperm can migrate through the hemolymph to the female's ovaries, resulting in fertilization.

The exact mechanics of traumatic insemination 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 copularix. 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.^[9] Females in other genera resist mating and attempt to escape.^[10] However, this resistance might not be an aversion to pain caused by traumatic insemination, as the concept of insects feeling pain is questioned.^[11]

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.^[12]

Many reasons for the origins of traumatic insemination as a mating strategy have been suggested. One position is that traumatic insemination evolved in response 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".^[3] 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 evolved as a means for males to circumvent female resistance to mating;^[1] to eliminate courtship time, allowing one male to inseminate many mates when contact with between them is brief,^[13] 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.

— Gilbert Waldbauer, ^[14]

Traumatic insemination appears to be another of the evolutionarily stable reproductive strategies that may appear questionable or even counterproductive, but that once established, resist change. It is possible that the behavior or trait in question came about in response to an evolutionary pressure that is no longer present, but the response to it remains.

While advantageous to the reproductive success of the individual male, traumatic insemination imposes a cost on females. Traumatic insemination results in 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, further reducing female lifespan.^[12] 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 bedbugs kept in laboratories to go extinct, starting with adult females.^[15] In such an environment, where mating occurs frequently, this high rate of adult female mortality is evidence that traumatic insemination is detrimental to the female's health.^[1]

The deleterious effects of traumatic insemination created evolutionary pressure towards the development of a mechanism to mitigate the damage caused by traumatic insemination.

In response, female bedbugs have developed specialized pair of reproductive organs ("paragenitalia") at the site of penetration. Known as the ectospermalege and mesospermalege (and known collectively as spermalege), they are sperm-receptacles from which sperm can migrate to the ovaries.^{[16] [17]} All reproduction occurs via traumatic insemination and the spermalege—the genital tract, though functional,^[18] is used only for laying fertilized eggs.^[2]

The ectospermalege is a swelling in the abdomen, often folded, filled with hemocytes. The ectospermalege is visible externally in most bedbug species, giving the male a visible 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.^[18]

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.^[18]

The mesospermalege is a sac attached to the inner abdomen, under the ectospermalege. Sperm is injected through the male's penis 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 bedbugs.)^[1]

The spermalege are generally found only in females. However, males in the Afrocimex genus posses a ectospermalege.^[1]

Homosexual traumatic inseminations have been observed in Xylocoris maculipennis^[3] and the Afrocimex genus.^[1]

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, Carayson (1966) found showed that male Acrocimex suffer actual homosexual traumatic inseminations. He found that the male ectospermalege often showed characteristic mating scars, and histological studies showed that "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, in [sic ] any, of homosexual traumatic insemination in Afrocimex remain unknown.

— Arnqvist, ^[1]

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 Cimex 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 bred by a male Hesperocimex cochimiensis.^[1]

In the animal kingdom, traumatic insemination is not unique as a form of coercive sex. Penis fencing is a behavior seen in hermaphroditic flatworms in which the species "fence" with penises to inject sperm. The "loser" is the flatworm which is inseminated and must bear the energy costs of reproduction.^{[19] [20]}

Research suggests that in the Acilius genus of water beetles 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 shapings (to prevent males from gaining a grip). Foreplay is "limited to the female desperately trying to dislodge the male by swimming frantically around".^[21]

Bachelor herds of bottlenose dolphins will sometimes gang up on a female and coerce her to have sex with them, by swimming in close proximity to her, chasing her if she attempts to escape, and making vocalized or physical threats.^{[22] [23]}

• Reproduction
• Animal sexuality
• Mating

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