Kings of Camouflage

Mating Trickery

Giant cuttlefish off the coast of Australia, long known as masters of camouflage, can use their color-changing abilities in a remarkable act of sexual deception: smallish males, unfit for winning wrestling matches with stronger rivals, disguise themselves as females in order to elude their adversaries and discretely mate with the genuine article. It's astounding, but not entirely unusual. The animal kingdom is rife with such "sneaker" males as well as an array of courtship and mating tactics more devious than any found in a Harlequin romance. Below, meet a menagerie of fish, insects, reptiles, and mammals with intriguing sexual strategies.—Nicole Duarte and Susan K. Lewis

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Bluegill Sunfish
Lepomis macrochirus
In the mating game, male bluegills don't have just a single strategy for success; they have three. Most males take a conventional approach—becoming big and brawny. Their physical prowess allows them to build and defend nests from predators, and females spawn in their domains. But when a female enters a nest, she may be followed by a male similar to her in size and coloration. The territorial male may not notice this stealthy rival, who has come to fertilize the eggs he will protect. The third sort of male, the smallest of all, attempts to dive in amongst a mating territorial male and a female and add his sperm to the mix. Both types of non-territorial males reach sexual maturity years before the large nest-guarding type, and both are free to flit from nest to nest to try their wiles. The territorial males have countertactics, however. They can "taste" the eggs in their nests, distinguishing and saving those they have sired and devouring the rest.

Fruit Fly
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Fruit Fly       
Drosophila melanogaster
Females across the animal kingdom—from insects to mollusks to mammals—often hedge their reproductive bets by accepting the sperm of multiple males to ensure that their eggs will be fertilized. This leads to so-called "sperm competition," and in the common fruit fly, the sperm of the last male to copulate with a female often displaces rival sperm and wins out. Males can employ a strategy, however, to prevent such rematings: they release a pheromone in their seminal fluid that acts as an anti-aphrodisiac. It marks the female with the scent of a male, making her less attractive to subsequent suitors, at least for several hours. The chemical cocktails in the male's semen enhance his reproductive success but may be costly to her; it's thought that the compounds decrease female longevity.

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Side-Blotched Lizard
Uta stansburiana
Male side-blotched lizards are engaged in what herpetologist Barry Sinervo likens to a game of Rock, Paper, Scissors. There are three types of males, and whether one type triumphs in a particular match depends on which of the other two it is up against. One morph of male has a yellow throat. It resembles a female and can sneak into the territory of an orange-throated male to pair up with one of the orange throat's harem. To keep the ultra-aggressive orange throat at bay, the yellow throat bobs his head just as a female unreceptive to mating would do. But yellow throats can't pull the same trick with the third morph, blue-throated males. When yellows try to invade blue-throat territory, the blue throats, which are monogamous, quickly recognize the intruders and chase them away. The blue males even cooperate with neighboring blue males to drive off yellow "sneakers" and overtly aggressive oranges, at times sacrificing their own lives for the sake of their blue brethren.

Garter Snake
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Red-Sided Garter Snake
Thamnophis sirtalis parietalis
Sometimes outcompeting a rival suitor involves attracting his attention.

In the mating frenzy that takes place each spring among red-sided garter snakes, a hundred males may descend upon a single female emerging from her winter den. Within the resulting writhing mass, some males chemically mimic females, emitting a pheromone so alluring that other males pursue them rather than the female. Biologists hypothesize that this tactic allows the mimics to snake their way to the true female while their competitors are confused. This mimicry can come at a cost, however: at times, the mimics are mobbed by excited males even when no female is around, and they all lose out on a chance to mate. On the other hand, the warmth of the pursuing males heats up the mimic, which has only a 0°C body temperature when he emerges from his den, and thus may enhance his fitness to survive.

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Common Scorpionfly
Panorpa communis
Female scorpionflies expect dinner before they mate. A male will approach a female bearing what biologists term a nuptial gift—a prey insect or a gob of secreted saliva that she will find tasty. While she munches, the male copulates with her, and the bigger the present, the longer the male has for insemination. However, not all males want to pay for dinner. Some cunning fellows will assume the posture and behavior of a receptive female, then, when another male offers "her" a gift, the impersonator will snatch it and dart off. If the thief is successful, he'll turn around and offer his stolen gift to a female, with the chance, of course, that "she" might actually be another thief.

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Spotted Hyena
Crocuta crocuta
Many cases of males mimicking females exist in the animal world, but spotted hyenas turn this ruse around. Female hyenas have an enlarged clitoris that closely resembles the male's penis, and biological anthropologist Martin Muller speculates that this trait evolved, in part, by protecting young females from attack. Hyena prides are ruled by a dominant female that holds her position vis-à-vis other females through fiercely aggressive behavior, which can even include infanticide. Infant females that pass as males might avoid such a fate and survive, unlike their more obviously female counterparts.

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Green Frog
Rana clamitans melanota
A call-and-response courtship leads female green frogs to their mates, with females gauging the attractiveness of potential partners by their love songs. In this exchange, smallish males sometimes imitate the low-pitched vocalizations associated with larger, more desirable mates. Other males, called satellites, rather than talk the talk, station themselves near deep-voiced rivals and attempt to intercept approaching females. Male crickets practice similar tactics: some sing loudly—luring predators as well as females—while satellite male crickets wait by at a safe distance to catch females crawling in. If few predators are around, the singing strategy likely wins out, but when danger abounds, it pays to remain silent.

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California Tiger Salamander
Ambystoma californiense
Reproductive success often involves undermining the competition. Male tiger salamanders encase multitudes of sperm in packets called spermatophores, which they secrete in the paths of females after an elaborate mating dance. In the standard version of the ritual, a female picks up the spermatophore with her genitals. But in a con game, a male assumes the role of a dancing female and then destroys his rival's genetic material. A male mimicking a female can also join a mating pair and deposit his spermatophore on top of his rival's. The female will take only the spermatophore on top, wasting the efforts of the first male.

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Cimex lectularius & Afrocimex constrictus
Mating amongst bedbugs isn't pretty. The namesake species responsible for itchy welts on human victims, C. lectularius, practices "traumatic copulation." With a saberlike penis, males puncture the abdomens of females to inseminate them. Interestingly, the females can benefit from this violent act by using the sperm for nutrition as well as to fertilize eggs. In another species, A. constrictus, which lives on African bats, males possess a genital structure closely mimicking that of the female. They entice other males to mate with them and can feed off the sperm, but the greater aim is simply to diminish the reproductive capacity of their competitors.


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