Bizarre Animal Courtships: The Power of Sexual Selection

In preparation for Valentine’s Day, humans across the world are investing in chocolates, flowers, lacy garments, and, for those who have read 50 Shades of Grey, perhaps a few additional supplies. For some of us, it’s the perfect excuse to stuff our faces with chocolate and sulk over singledom. In my case, I sat around craving chocolate and randomly announcing disturbing aspects of animal mating behavior to my resigned friends and family. In honor of this lovey-dovey holiday, I present a blog on how the epic battle to get laid has led to the development of some extremely peculiar methods of winning over a potential mate and competing with rivals.

The struggle is real, ladies and gents, and you’re not alone!

Valentines

Sexual Selection

If you’ve taken an introductory biology course you’ve probably been hit over the head with the concept of natural selection. It’s the process by which, over generations, heritable biological traits become more or less common in a population based on whether the traits offer advantages to survival and reproduction. If there’s a trait that helps you survive and reproduce, you’ll pass that trait onto more offspring than someone without that trait. This is a nice, clean theory, but some animal traits and behaviors just don’t seem to make sense in a survival context (five foot long peacock tails? Those are just asking to get pounced on).

4sexual selection

Many of these strange traits or behaviors arise through a mode of natural selection known as sexual selection, which falls under the umbrella of social selection. Competition between members of a species for resources is the force behind social selection, which includes displays or ornaments used to attract breeding partners or repel rivals, traits to enhance fighting prowess to access mating partners, territory, resources, or social rank, and suppression of reproduction by rivals[1,2,4]*. Some folks are just better at getting laid and making more babies than others. This leads to an increased frequency of traits that don’t enhance survival (in fact, they can even be detrimental to survival), but they do enhance reproductive success. It can also lead to sexual dimorphism: differences in physical characteristics between males and females in a species, such as size differences, coloring, horns, fancy feathers, etc[5,7].

*There is an ongoing debate in the scientific community about the exact definition of sexual selection, especially with respect to female competition and selection[4].

Intrasexual

richmond-fighting_1737376i

In intrasexual sexual competition, males compete with males for mates or, less frequently, females compete with females over mates. This mode of selection favors traits enhancing the ability to intimidate, deter, or defeat rivals in order to secure mates. When this occurs in females, it can actually result in sexual mimicry: heightened testosterone levels result in masculinization of the female genitalia, along with a hefty dose of aggression helping them to dominate rivals[5]. This is thought to be part of the reason that, in the matriarchal species of Spotted Hyenas, females have developed a pseudopenis despite the costs of such an appendage (60% of first births are stillborn due to suffocation as they travel through the appendage)[22]. And yes, it is exactly what it sounds like.

SpottedHyena

A fun example of intrasexual selection is the elusive, waterborne unicorn (boring people call these Narwhals). These strange creatures have a canine tooth that developed into a long, spiraling horn in the males. Classified as whales, they dwell in some of the most frigid waters in the world and frequently suffocate or starve while trapped beneath the ice. Their name, derived from the old Norse nár, means corpse whale because their speckled grey coloring is apparently similar to a drowned corpse. Lovely. Their ancestral relatives (white whales) used to live in tropical waters, so they really get the short end of the stick these days[16]. If they aren’t suffering due to their environment, the males might be rubbing their 10-foot-long (4’-10’) tusks together in order to establish a dominance hierarchy. Interestingly, this tusk also acts as a sensory organ[17].

5Narwhal

Sometimes these traits can get a little out of hand. Once upon a time, there existed the mighty Irish Elk, Megaloceros giganteus. Surprisingly, they didn’t drink themselves into extinction nor were they Irish or even closely related to elk species[18]. These giant deer existed 400,000 – 10,900 years ago and were a whopping 7 feet tall at the shoulder, with antlers spanning 12 feet and weighing almost 100 pounds. The proposed explanation for these unwieldy antlers is pressure from sexual selection due to epic battles between males along with female choice (see intersexual, below). The antlers got so ridiculously cumbersome that they might have even factored into the extinction of the species, although the main cause seems to have been starvation[19,20].

6elk

Intersexual

We also have intersexual competition, where one sex chooses a mate. Consequently, there is competition using traits (secondary sexual characteristics) that determine the relative attractiveness of one sex to the other. According to Bateman’s principle, the sex that invests the most in producing offspring becomes the limiting resource over which the other sex will compete; for example, in many species females put in a greater portion of the care for offspring, and will therefore be more picky about a mate[9].

We are still working to understand how and why these preferences have evolved. Direct benefit models suggest that mates are chosen for providing an immediate benefit, such as parental care, territory defense, or nuptial gifts (like food offerings!). However, when none of the immediate benefits are present and we’re looking at bizarrely elaborate ornaments, it is more likely due to indirect benefits. The preference and physical trait may be linked: a female with a preference for long-tailed mates with a male with a long tail, and has offspring with both a long tail and a preference for long-tails. This is described in the Fisherian model and Condition-Independent Indicator model, and results in genetic correlation between the ornament and preference, leading to never-ending trait elaboration until natural selection opposes it[5,8,9]. Another model is the Condition-Dependent Indicator model, which suggests a correlation of 3 factors: ornament, preference, and viability. The ornament is a costly trait dependent on the physical condition of a male: more viable males will be in a better physical condition to maintain more elaborate ornaments, and consequently the ornament acts as an indicator of health (and the offspring will be healthier and make more babies, etc etc)[5].

BoP

This type of selection pressure is frequently seen in birds, especially Birds of Paradise. Just look at some of these ridiculous get ups!  Females tend to be more modestly colored (or lackluster, if you want to be harsh) and choose mates based on the condition and color of their plumage. Not only do these birds have fancy feathers, but males even compete for attention via dance. They will puff up to display their feathers, vibrating and buzzing them in a series of discrete motions in order to win over the hard-to-impress gals[11].

Birddance

Male bowerbirds supplement their color and dance by building elaborate shrines filled with colorful objects. These twig constructions are known as bowers. At the north end of the bower, male birds build a stick platform and place an assortment of special objects on it. In Vogelkop bowerbirds, the males focus on the novelty value of objects. Satin bowerbirds, however, focus on specific colors, picking up yellow objects from their collections during their courtship dance. Females will fly between bowers and watch the presentations, choosing mates with the best constructed bowers and the most interesting treasures[11,12].

BOWER

A couple other fun examples are the moonwalking skills of red-capped, long-tailed manakins and the incredible mimicking skills of the superb lyrebird, serenading their potential mates with everything from bird songs to chainsaws, gunfire, and car alarms.

Manakin

Thanks DR for the stunning artwork!

Thanks DR for the museum-worthy artwork!

Post-Copulatory Competition

But wait, the competition doesn’t stop with sex! So you may have successfully completed the act, but the battle isn’t over – now comes sperm competition. This crops up in species where females have multiple mating partners. While having a variety of mates improves a female’s chance to have more viable offspring, males have a decreased chance to pass their genes on. Thus, guys have to get crafty at adapting to increase their chance of success post-copulation. A basic example of this is mate guarding, when a male will keep his mating partner close by following sex in order to prevent another male close enough to jump her.

Copulatory plugs is another example that frequently shows up in insects, reptiles, spiders, and even some mammals. These are exactly what they sound like: a plug inserted into the female following sex to physically block further insemination. These can be simply physical (such as in the Indian Meal Moth), or they could be a little more high tech; in bumblebees, the mating plugs also contain linoleic acid, which influences the female’s behavior to reproduce less. They can also be a little more sinister; in Drosophila fruit fly semen, toxins dampen the female’s sex drive and kill her slowly, ensuring fewer male competitors will get a chance with her in the future.

drosophila

There’s also the straight forward method of sperm removal. Black-winged damselfly females collect the sperm from several males in her spermatheca. When a new male mates with her, he will actually use his male organ as a scrub brush to remove the sperm of other males in order to increase his chances of fertilizing her eggs.

On the female side of the battle, cryptic female choice is a poorly understood process by which proteins in the female reproductive tract can affect which sperm successfully fertilizes her eggs. This has been shown to include the ability to avoid inbreeding in insects, where the sperm of non-relatives is preferentially selected[21].

Extra examples of odd courtships

We don’t typically think of insects as being overly romantic, but there are some unique examples of mating behavior in bugs (when they aren’t busy poisoning their partners). For those of us living in the countryside, we might be lucky enough to watch the beautiful courtship of fireflies. As dusk falls, males begin to perform flash patterns as they loop-de-loop through the air. Females take this opportunity to relax and watch the show from near the ground. When they’re particularly impressed by the flashiness of a male, they will respond with their own glowing signal. The male then lands and continues to flash in a bioluminescent dialogue while approaching the lucky lass by foot. And then, under the beautiful moon (or not, depending on the time of month), they embrace in bioluminescent love making[13].

firefly

Water striders have a slightly less romantic take on mating. Males will tap the water’s surface to indicate that they’re in the neighborhood when approaching another water strider. Another male will return the same signal, but a female will not signal back. Seizing his chance, the approaching male will switch to a courtship signal. If a female consents and presents herself, they will remain attached to each other for the entire reproductive season! While this sounds just dandy, something far more sinister is going on. It turns out that the courtship signal is actually a form of intimidation coercion by the male: the signal attracts predatory fish and insects that will target the female. The male will continue to make it until the female consents to be mated – the faster a female acquiesces to the male’s demands, the more likely she is to survive the encounter!

waterstriders

Meanwhile, sagebrush lizards are the jocks of courtships. These little guys will perform a physically demanding chain of push-ups to impress their potential females and outmatch males.

Thanks to my coworker, SCS, for the fun guest illustration!

Thanks to my coworker, SCS, for the fun guest illustration!

When spiders aren’t eating their mates, they can actually be quite romantic. Peacock spiders are a species of jumping spider (which would be cutest type of 8-legged monstrosity if they didn’t have the tendency to fling themselves at your face after you engage in an adrenaline-fueled staring contest). These little guys sport a truly impressive physical display with bold colors and ornaments. When a male is trying to get some action, he will raise his abdomen and expand colored flaps in a spectacular presentation. Just to top things off, he will also raise his third pair of legs into the air and perform the arachnid version of an interpretive wooing dance, waving and vibrating his legs as he hops back and forth[15]. This dance can last up to 50 minutes!

peacockspiderHeather

Thanks to my coworker, HB, for the guest masterpiece!

peacockspider1

 

On the mammalian side of things, if you’ve ever seen a male hooded seal display to a rival male, you may have been concerned that you were witnessing the final moments of a terribly diseased creature. In the world of hooded seals,  there is nothing more fearsome than blowing up a giant pink, tumor-looking balloon out of one nostril and flapping it around. The size of the balloon allows males to establish dominance for mates. If a pair of males is evenly matched for nasal balloons, they will physically fight it out instead.

seal

Thanks to my coworker DR for the b-e-a-utiful illustration!

 

hooded_seal

If there’s one species out there that really makes you scratch your head regarding sex, it is probably the porcupine. Because, lets face it…ouch.

Surprisingly, the actual mechanism of intercourse is the least disturbing aspect of porcupine courtship. This indelicate process can take days. First of all, during mating season both sexes spend their time announcing it’s breeding time by wailing, shrieking, screaming, moaning, and chattering their teeth. Males battle over females, thrashing each other with their quills and biting at any available flesh. The victor will then get the dubious honor of approaching the female. The two enter a standoff that can last days: the male edging toward the female, while the female backs away and squawking. When the female finally gives in, the male stands on his hind legs and sprays her with urine. This is apparently the key to getting her in the mood, as the female porcupine then flips her tail over her back, covering her quills and initiating a sexual marathon. Several hours later, the encounter is terminated by the female screaming and shrieking at the male.

On that note, I hope you all have a wonderful Valentine’s Day! And if you’re single, just remember… it could be so much worse. You could be a porcupine.

porcupine

References

[1] Clutton-Brock TH, Huchard E. “Social competition and selection in males and females.” Philosophical Transactions of the Royal Society B. 368:20130074. 2013.

[2] West-Eberhard MJ. “Sexual selection, social competition and evolution.” Proc R Soc Lond. B. 123. 1979.

[3] Velando A, Beamonte-Barrientos R, and Torres R. “Pigment-based skin color n the blue-footed booby: an honest signal of current condition used by females to adjust reproductive investment.” Oecologia. 149. 2006.

[4] Tobias JA, Montgomerie R, Lyon BE. “The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition.” Philosophical Transactions of the Royal Society B. 367. 2012.

[5] Jones AG, Ratterman NL. “Mate choice and sexual selection: what have we learned since Darwin?” PNAS. 106. 2009.

[6] Darwin, C. The Origin of species by means of natural selection. London, UK: John Murray. 1859.

[7] West-Eberhard, MJ. “Sexual selection, social competition, and evolution.” Proc. Am. Philos. Soc. 123. 1979.

[8] Lande R. “Models of speciation by sexual selection on polygenic traits.” Proc Natl Acad Sci. 78. 1981.

[9] Kokko H, et al. “The evolution of mate choice and mating biases.” Proc R Soc London Ser B. 270. 2003.

[10] Kotiaho JS, Puurtinen M. “Mate choice for indirect genetic benefits: scrutiny of the current paradigm.” Funct Ecol. 21. 2007.

[11] Diamond J. “Biology of birds of paradise and bowerbirds.” Annual Review of Ecology and Systematics. 17. 1986.

[12] Borgia G. “Bower quality, number of decorations and mating success of male satin bowerbirds (Ptilonorhynchus violaceus): an experimental analysis” Animal Behavior. 33. 1985.

[13] Demary K, et al. “Firefly courtship: behavioral and morphological predictors of male mating success in Photinus greeni.” Ethology. 112. 2006.

[14] Han CS, Jablonski PG. “Male water striders attract predators to intimidate females into copulation.” Nature Communications. 1(5). 2010.

[15] Girard MB, Kasumovic MM, Elias DO. “Multi-Modal Courtship in the Peacock Spider, Maratus volans.” PLoS ONE. 6(9). 2011.

[16] Heide-Jørgensen, MP and Laidre, KL. Greenland’s Winter Whales: The beluga, the narwhal and the bowhead whale. Ilinniusiorfik Undervisningsmiddelforlag, Nuuk, Greenland. 2006.

[17] Nweeia MT et al. “Sensory ability in the narwhal tooth organ system.” The Anatomical Record. 297(4). 2014.

[18] Lister AM et al.”The phylogenetic position of the giant deer Megaloceros giganteus”. Nature 438(7069). 2005.

[19] Gould SJ. “Origin and Function of ‘Bizarre’ Structures – Antler Size and Skull Size in ‘Irish Elk’, Megaloceros giganteus.” Evolution. 28(2). 1974.

[20] Worman C, Kimbrell T. “Getting to the Hart of the Matter: Did Antlers Truly Cause the Extinction of the Irish Elk?” Oikos. (9). 2008.

[21] Tregenza T, Wedell N. “Polyandrous females avoid costs of inbreeding.” Nature. 415. 2002.

[22] Glickman SE et al. “Mammalian sexual differentiation: lessons from the spotted hyena.” Trends in Endocrinology and Metabolism. 17(9). 2006.

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