Valentine’s Day in the Animal Kingdom: Tough Love

Warning: This blog post contains descriptions of animal sexual behavior, in more detail than you probably ever wanted to read.

              In honor of this week’s holiday, I thought I’d break away from diseases and delve into some of the more bizarre romance that occurs in nature (the alternative would have been to write about STDs. Trust me, this subject is better). You thought being single on Valentine’s Day was bad? Try being in a relationship as one of these creatures!

Sexual Cannibalism

Image              There is no truer expression of love than offering up one’s body in sacrifice for a romantic dinner. No? Well, red back spiders might disagree with you! Sixty-five percent of mating encounters end in cannibalism for this species [1]. What is truly bizarre, however, is the fact that the male willingly offers himself up: during copulation, the male spider performs a somersault to present his abdomen to the female’s fangs! He even undergoes special muscle contractions of the abdomen to move his vital fluids out to ensure he survives as long as possible during his consumption [1,7].

Why on earth do the males want to get eaten? Scientists have proposed the adaptive male sacrifice hypothesis to explain it, where the increased reproductive success from a single cannibalistic mating outweighs their reproductive success if they were to survive the encounter. This only works because male redback spiders live rather harsh lives. There is an incredibly high mortality rate for their search for a mate–80% of them die virgins [1]. Additionally, on average a male will encounter less than one female (in other words, there is barely any chance of them encountering a second female to mate with if they’re lucky enough to find one in the first place!). Furthermore, males become functionally sterile after a single mating. With all these factors working against them, evolution has shaped the male redback’s behavior to maximize the success of a single encounter [1,2].

One of the ways to improve the efficiency of a mating encounter is to make it last as long as possible. By offering his body up as a bribe, a male redback spider copulates for longer than a male spider whose goal is to survive an encounter with the ‘fairer sex.’ Scientists have discovered that cannibalized spiders can actually double their paternity relative to non-cannibalized rivals. Consequently, these sacrificing behaviors have been passed on through generations [1,2,7].

Redback spiders aren’t alone in participating in sexual cannibalism. Praying mantis females are infamous for decapitating their mates; although their behavior partially stems from the resulting body spasms that the decapitated male undergoes which, apparently, provide for fantastic sex (don’t try this at home). Midge flies are even more morbid, with the females inserting their proboscis into the male’s head during copulation and injecting chemicals that liquefy the male’s innards, providing a tasty and nutritious meal to enjoy during sex.

Unsurprisingly, in species where it is not advantageous to the male to be eaten, they have evolved defenses against such rude bed behavior. Tetragnatha extensa spiders have spurs which they use to lock the female’s jaws open to avoid being bitten during intimacy. Male Xysticus cristatus, or crab spiders, actually tie the females down before having sex, and Argyrodes zonatus males secrete a drug that intoxicates the females and leaves them too high to chow down during sex.

Penis Fencing

Image              Members of the marine flatworm species Pseudoceros bifurcus are hermaphrodites, able to undergo female and male reproductive roles. They have evolved a peculiar technique to determine who plays which role; as the title of this section might suggest, an encounter between two flatworms proceeds with them rearing up and attempting to skewer the other on long, spear-shaped male organs. These battles can take up to an hour, with strong avoidance behaviors engrained in each participant due to evolutionary pressures to avoid the costs of the resulting wound. If a flatworm is stabbed, it receives an injection of sperm and is forced to play the female reproductive role. The first to gain a successful stab fathers more eggs and has far less stab wounds to heal, which has resulted in the development of the sparring behavior. Such ‘injections’ are common in hermaphroditic species of leeches, flatworms, and sea slugs [3,7,8]. Ouch!

Traumatic Insemination

Image               Similar stabbing behavior is also found in non-hermaphroditic species. The sexual behavior of bedbugs was shocking enough to earn its own term: traumatic insemination. Male bedbugs have a sharp organ called the paramere, which they use to pierce through the female’s exoskeleton and inject sperm directly into her body cavity. It then travels through the blood and into sperm storage structures. Such violent treatment reduces the female’s lifespan by 25% and her egg production by 50% [9].

              Unsurprisingly, the females aren’t too keen on this discourteous behavior (they have a fully functional female reproductive tract, thank you very much!). Sexual conflict between the two genders has resulted in females evolving counter adaptations to reduce the cost of being stabbed, since males are unwilling to desist due to the fact it allows their sperm to take precedence over any previous male’s. Female bedbugs have evolved a spermalege, a modified abdominal region in the most targeted area of their underbelly that completely nullifies the effect on her lifespan and egg production. And thus, the bedbug violent romance continues [9,10,12,13].

(Bedbugs are far from alone in this type of behavior–violent romance is more common than the alternative in nature. The oceanic squid Taningia danae participates in a slightly different ritual, where the male uses his beak or arm hooks to make incisions in the female’s mantle or neck before inserting packets of sperm into the wound. They truly make romantic engagements sound appealing[6].)

Exploding Genitals

              Image               When you admire the honeybees flitting through your flower gardens, you probably don’t give much thought to the rest of their life cycle. It all seems quite dull, really, the endless nectar collecting and buzzing. Their sex lives, however, end with quite the bang. Queen bees hold a mating event only once, so it’s understandable that the sex would have to be spectacular. On her special day, she takes off into the sky and as many as 25,000 males will compete to attempt to mate with her. Only 20-40 males will have the opportunity to do so during the event, and each one will die during orgasm (not a bad way to go, all things considered). The queen will store 3-5% of the collected sperm for the remainder of her life, which will probably be about 5 years, and use it to fertilize her half million or so eggs [4,7].

               Where do exploding genitals come in? Well, since most male honeybees die virgins, they really have nothing to lose by evolving suicidal behaviors that increase their reproductive success (ring a bell?). When a male bee copulates, he contracts his abdomen to build pressure until he explodes at the site of their joining. This provides an important advantage: it plugs the female, making it more difficult for subsequent males to mate and consequently fertilizing a larger proportion of the queen bee’s eggs [4,5].

Detaching Genitals

Image              In a slightly less violence twist, other males actually have detachable penises. Many cephalopods have a tentacle called a hectocotylus, a modified arm that is used to transfer packets of sperm to a female. In some genera, this is actually used to differentiate species as they are so unique. The behavior associated with them also varies significantly, from merely placing sperm, to directly inserting it, to detaching and swimming into the female. The latter occurs mainly in the paper nautiluses, also known as arognauts. At copulation, the hectocotylus detaches itself from the body and shoots off toward the female, entering the mantle cavity and releasing sperm. It’s a fantastic way to go if you’re too shy to face your love. Unfortunately, hectocotylus don’t grow back so it’s rather important not to miss your one shot [14,15].

Chomped-Off Genitals

Image               It’s quite hard to stay away from violence in the natural world, so here we are again. If fatal cannibalism, exploding, or stabbing isn’t up your alley, there’s always the option of gnawing off your partner’s family jewels.

               The hermaphroditic banana slugs of the Ariolimax  genus do just that. Banana slugs mate by reciprocal insertion (both playing the male and female role simultaneously!). It doesn’t always end violently, but if they are not properly size matched they can get, well, stuck. After several attempts to disengage, the receiving trapped partner will turn around and chew off the offending organ providing freedom and a tasty snack [7,11,12].

In Conclusion…

Nature is a harsh reality where sex is more often than not a violent affair charged with the conflict of each partner’s interests and the pressure to reproduce. As it is the main act of evolution, truly spectacular behaviors have evolved to optimize one’s success. The prior examples barely scratch the surface, and there are many other (less violent) wondrous behaviors revolving around the courtship and success of copulation. With this in mind, I hope you all have a fantastic Valentine ’s Day, whether you’re celebrating being human, single, or in a relationship!

References

[1] Andrade, M. “Risky mate search and male self-sacrifice in redback spiders.” Behavioral Ecology. 2003. 14(4):531-538.

[2] Andrade, M. and Banta, E. “Value of male remating and functional sterility in redback spiders.” Animal Behaviour. 2006. 63:857-870.

[3] Chase, R. and Kristin, V. “Independence, not conflict, characterizes dart-shooting and sperm exchange in a hermaphroditic snail.” Behavioral Ecology and Sociobiology. 2006. 59(6):732-739.

[4] Collins, A., et al. “Proteomic analyses of male contributions to honey bee sperm storage and mating.” Insect Molecular Biology. 2006. 15(5):541-549.

[5] Franck, P., et al. “Sperm competition and last-male precedence in the honeybee.” Animal Behaviour. 2002. 64:503-509.

[6] Hoving, J., et al. “Sperm storage and mating in the deep-sea squid Taningia danae.” Mar Biol. 2010. 157:393-400.

[7] Judson, Olivia. Dr. Tatiana’s Sex Advice to All Creation: The Definitive Guide to the Evolutionary Biology of Sex. London: Vintage, 2003.

[8] Michiels, N and Newman, L. “Sex and violence in hermaphrodites.” Nature, Scientific Correspondents. 1998. 391: 647.

[9] Morrow, H. and Arnqvist, G. “Costly traumatic insemination and a female counter-adaptation in bed bugs.” Proc. R. Soc. Lond. 2003. 270(10).

[10] Reinhardt, K., et al. “Reducing a cost of traumatic insemination: female bedbugs evolve a unique organ.” Proc. R. Soc. Lond. 2003. 270.

[11] Reise, H. “A review of mating behavior in slugs of the genus Deroceras.” Amer. Malac. Bull. 2007. 23:137-156.

[12] Reise, H. and Hutchinson, J. “Penis-biting slugs: wild claims and confusions.” Trends in Ecology and Evolution. 2002. 17(4):163.

[13] Stutt, A. and Siva-Jothy, M. “Traumatic insemination and sexual conflict in the bed bug Cimex lectularius.” PNAS. 2001. 98(10): 5683-5687.

[14] Sukhsangchan, C. et al. “Embryonic Development of Muddy Paper nautilus Argonauta hians Lightfoot, 1786, from Andaman Sea, Thailand. Kasetsart Journal Natural Science. 2007. 41:531-538.

[15]Zecchini, F., et al. “Development of the hectocotylus in Illex coindetii.” Scientia Marina. 2012. 76(3)

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