Cannibalism And Detachable Penises: The Unusual Sex Lives Of The Animal Kingdom

Fun for some. Bonobos are known to have recreational sex, but that's not always the case in the animal kingdom. anolisol/123rf.com

This is the second in a three-part guest series by Dr Carin Bondar, author of The Nature of Sex, which is available now in the UKAustralia and New Zealand. Read part one here.

We’ve all heard the horror stories of sexual cannibalism in the animal world. Sexual cannibalism represents perhaps the most extreme form of conflict between the sexes. This kind of behavior is observed in several species of praying mantids and spiders, and there is tremendous diversity in the extent to which it occurs.

Red back spider. Paul Looyen/123rf.com

Some male spiders, such as Australian red backs (Latrodectus hasselti), perform a specialized sexual ‘somersault’ into the awaiting jaws of their female lovers so as to encourage their own cannibalistic death. They position their abdomens directly above the female’s jaws, and the ladies typically nibble on their posterior bits while copulation occurs. Ideally, a male red back would like to mate twice. He has two pedipalps (appendages common to most arachnids, in this case utilized to carry sperm) that can only be used once each, and females have paired sperm storage organs which require two copulations to fill. To die after one bout of copulation (as happens in approximately 12.5% of the population) would almost be a cop-out for a male, since not only is he physically built with two pedipalps, he also significantly increases his biological fitness if he can utilize them both. If he only copulates once he will share paternity if the female remates with another male.

Males have therefore developed a nifty technique to minimize their chances of succumbing to a cannibalistic demise during the initial bout of copulation. They constrict their abdomens, thus pushing their vital organs to the anterior of the body where they are protected from the female’s nuptial nibbles. Males that undertake this constricting strategy minimize the damage to their bodies, yet still experience a successful copulation. They are then able to fulfil their biological destiny by engaging in a second bout of copulation. Finally, with both pedipalps spent, they allow themselves to be killed and consumed by their second female partner.

We see similar strategies in other spider species, such as the orb-weaving Nephilengys malabarensis. In this species males engage in ‘remote’ copulation with females, effectively transforming themselves into functional eunuchs. Remote copulation? More like remote control. You can have sex with your partner while sitting comfortably on the couch across the room.

Bed bugs tend to force the issue. istock

Although sexual cannibalism is extreme and horrifying, it’s not the only kind of sexual activity to involve pain. Take, for example, animals that exhibit traumatic insemination – yes it’s actually termed traumatic in the scientific literature, and for good reason. Perhaps the most well-studied examples of traumatic insemination come from the world of bed bugs (Cimex lectularius). Instead of using their sword-like penises (parameres) to deposit sperm into a female’s genital opening, male bed bugs of many different species will simply stab her outer body cavity and deposit sperm directly into her hemolymph (the insect equivalent of blood). Sperm will then migrate to her ovaries. In many species, females no longer have a primary genital opening – why keep it around if it’s never used? A similar scenario plays out during sexual relations in the spider Harpactea sadistica. Males have a needle-like penile organ and females have atrophied spermathecae (their traditional sperm storage organs).

Another bizarre mating ritual is demonstrated by the hermaphroditic sea slug Chromodoris reticulata, which carries both “male” and “female” sexual organs simultaneously. To date, this is the first species observed to have a completely disposable penis. Subsequent to each and every copulatory event, the individual autotomizes (casts off) its penis. It is then regenerated and able to successfully copulate again within twenty-four hours. It turns out that there is complex morphology behind sea slugs’ ability to discard their members after each mating.

Sea slug. Stephen Childs

The simultaneously hermaphroditic sea slug Chromodoris reticulata. Stephen Childs

The entire penile structure is quite large and attains a spiral shape within the body. Its overall length is enough for three copulations, which is why the male can regenerate it so quickly. Essentially, once copulation has taken place and the end of the penis is autotomized, the next part of the penis is uncoiled from the spiral and makes its way out of compression ready to inflate and copulate. Think about toilet paper coming off the roll. The autotomized members also play a role in removing sperm from previous reproductive partners, as observations show them to have numerous backward-pointed spines and to be covered in masses of sperm.

Sometimes the act of sex needn’t even involve two living partners, as demonstrated by a species of tree frog from Brazil. Necrophilia is alive and well! Males of the Amazonian frog Rhinella proboscidea have evolved a “functional necrophilia” reproductive strategy, whereby they promote extraction of the oocytes from the abdomens of dead females (killed by drowning during their explosive frog orgies) and fertilize them in a post-mortem necrophilic fashion. This strategy might sound appalling, but it functions to increase the reproductive success of both the females and the males.

Rhinella proboscidea. Izzo et al/Journal of Natural History

There are times when I have to chuckle at us biologists for creating a separate set of terms to describe behaviors in “other” animals as opposed to in humans. For example, sexual coercion is basically another term for rape. Yes, male animals rape female animals, but somehow it seems more politically correct to call it sexual coercion. There are several other primate species where sexual coercion is commonplace, most often where there is a large difference in size between males and females. In one of our closest relatives, the chimpanzee (Pan troglodytes), males tend to be most violent and coercive to females that are currently ovulating, which is an unfortunate consequence of the fact that females exhibit external sexual swellings during this phase.

Hamadryas baboons (Papio hamadryas) take the act of sexual coercion to another level. These primates live in small groups where males monopolize a semi-permanent harem of females. They guard ‘their’ females aggressively via herding, and females are generally compliant and sexually submissive to their leader. This is called female defense polygyny, indicating that the male defends his harem (and also keeps tight control over their sexual behaviors). Males will also fight with other males to defend their harem; however, takeovers by more aggressive males are a fairly common occurrence, especially for young males looking to begin their reproductive careers with a ‘set’ of fertile females.

Hamatryas baboons. Wrangel/123rf

Hamadryas baboons. Wrangel/123rf 

When a takeover happens, the losing male is forced to flee, and his resident females are forcibly and aggressively transferred to their new “owner.” Paternity confusion is impossible for females in this social scenario, and when a takeover happens the new dominant male kills all the existing offspring. The act of infanticide is clearly advantageous for the new dominant male, who should avoid providing care to unrelated offspring. In addition, the abrupt halt to lactation brings his new ladies into their estrous cycle, meaning that he can get to work creating some offspring of his own. Males that already have harems can also take over those of other males, thereby increasing the number of ladies at his service. They are especially aggressive towards newly acquired females, coercing them into compliance. One would imagine (and one would be right) that this is an intensely stressful time for the newly transferred ladies.

Although the immediate costs of sexual coercion in any species seem high for the female and low for the male, there could be benefits to the female’s biological fitness in the long term. The Hamadryas baboon scenario is indeed strange, what with males having such extreme dominance over females; but over the long-term a female could be transferred up the dominance chain of males in the local population, such that she eventually ends up with the most dominant, aggressive male. He will have successfully taken over the harems of all males before him, thereby proving his strength and power. On a level of pure biological significance, it makes sense for a female to mate as much as possible with the most aggressive male, so that she can have offspring with his genetic characteristics.

So is sex ever fun? Are there any animals that actually enjoy the acts of courtship and copulation?  While the number of cases pales in comparison to the gruesome horrific sexual lives of most animals, there are at least a few organisms out there that are enjoying themselves in the act.  All mammalian females have a clitoris, which in our own species affords a great deal of sexual pleasure, including orgasm. Does it serve the same purpose in other mammals? It’s difficult to say, although some general conclusions can be drawn with respect to the kinds of physiological processes that occur when human females experience climax.

For primates especially, many females exhibit an increase in heart rate, respiration and blood pressure associated with vaginal and clitoral stimulation. Involuntary, rhythmic muscle contractions in the vagina, uterus and anal sphincters occur at orgasm in human females, and these same contraction patterns are demonstrated in other primate females, leading to the obvious conclusion that other ladies experience orgasm as well. In chimpanzees, bonobos and macaques, female orgasm is also associated with a reach-back response, where females will clutch their sexual partner and reach backwards while emitting distinctive vocalizations and exhibiting a characteristic facial expression. Overall it seems abundantly clear that happy primate ladies all over the world are experiencing orgasm.

So there you have it!  While at least a few members of the animal kingdom are enjoying themselves in the act of copulation we can safely assume that the vast majority of others are not.  Sex is an entirely different sport for most animals, which makes me very happy to be human. In the third part of this series I will talk about the inevitable aftermath of successful sex: the offspring. It turns out that parenting in the animal kingdom is no easy task…

The Nature of Sex is now available in the UKAustralia and New Zealand. Stay tuned for release dates in the USA and Canada in spring 2016.

Image in text Red back spider. Paul Looyen/123rf.com

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