UC SANTA CRUZ, BARRY SINERVO
As a postdoc at the University of California, Berkeley, in the early 1990s, Barry Sinervo uncovered a biological game of rock-paper-scissors. Researching the common side-blotched lizards (Uta stansburiana) that live along North America’s Pacific coast, he discovered three different male morphs—a term for animals of one species that display distinct behavioral strategies and/or physical phenotypes. Aggressive orange-throated lizards with large territories secured more mates than cooperative blue-throated males, which maintained smaller territories and helped each other defend their turf against orange-throats. But orange-throated lizards were vulnerable to a third, sneaky morph. Smaller in size and festooned with yellow throats—just like the females—these lizards would engage in furtive copulations with females on the larger males’ territories. The success of the yellow-throated female mimics drove down the number of aggressive males in subsequent generations, giving the blue-throated males a better chance at reproductive success. Having a buddy system and smaller territories than orange-throated males, blue throats could more successfully guard their females against the yellow sneaks. But as the blue-throats became more common, the aggressive orange-throated males regained the advantage, and the cycle started all over again.
Sinervo, now a professor at the University of California, Santa Cruz, has been studying the lizards of Los Banos, California, and their distinct mating strategies, known as alternative reproductive tactics (ARTs), for more than 20 years. Not only do the different morphs employ unique mating strategies, but blue-throated lizards appear to be better able to recognize genetically similar individuals and preferentially form altruistic alliances with them. Recently, Sinervo’s team found that the three male morphs also vary in terms of how they respond neurologically as their territories change: when allowed to roam in large spaces, territorial orange-throats and blue-throats have high rates of neuron growth in the part of the brain involved in spatial analysis, while nonterritorial yellow-throats do not exhibit such neuronal plasticity. The finding indicates that territorial morphs may be more attuned to changes in their environments and more equipped to deal with the demands of remembering information about their changing territories.
A lot of times people think, “Oh, alternative mating strategies, well, that’s just weird animal sex.” But in fact, it’s a powerful evolutionary tool.—Stephen Shuster,
Northern Arizona University
While the rock-paper-scissor dynamics of these three lizard morphs may be fairly uncommon in nature, ARTs are not. When Sinervo began studying the side-blotched lizard system, researchers relied almost exclusively on counts of juveniles in a territory to gauge reproductive success of different male morphs. Without genetic paternity tests, however, such studies would fail to identify all cases of cuckoldry, thereby overlooking the often-successful strategy of sneaking fertilizations. But over the last decade or so, advances in DNA technologies have provided concrete evidence to back up observations that, across the animal kingdom, males—and sometimes females—employ diverse mating strategies, often developing distinct morphologies and physiologies to help them succeed. “These mating strategies are an engine of biodiversity,” says Sinervo.
While theory predicts that the most successful male morph will rise to dominance, when there are big winners and losers, taking the gamble with an alternative mating strategy could pay off, explains evolutionary biologist Michael Wade of Indiana University in Bloomington. When a dominant morph—say, a beetle with large horns, or a red-winged blackbird with a large territory—is able to mate with many females, other males won’t get a chance to reproduce at all. “There’re only a tiny fraction that are successful and a huge number of losers,” says Wade. “To invade a population, a male using alternative tactics doesn’t have to beat the best males, just beat the average.”
As researchers continue to disentangle the genetic, epigenetic, and environmental factors that influence the development of ARTs, they may well uncover even more of these unconventional strategies for obtaining a mate. Moreover, such studies could yield insights into how such tactics arise and evolve, with implications for the mechanisms by which sexual selection shapes species. “A lot of times people think, ‘Oh, alternative mating strategies, well, that’s just weird animal sex,’” says Stephen Shuster of Northern Arizona University. “But in fact, it’s a powerful evolutionary tool. Because we’re trying to understand how selection acts on evolutionary traits and how phenotypes are changed.” —Rina Shaikh-Lesko
An ART Gallery
ESTER NAVARRAIn 2011 and 2012, behavioral researcher Luca Corlatti, then a PhD student at the University of Siena, spent hours observing the behavior of radio-collared Alpine chamois, mountain-dwelling relatives of sheep and goats. In Gran Paradiso National Park in the Italian Alps, he watched as females reared their kids in herds, while males lived primarily on their own. In spring, dominant males would establish lower-elevation territories, maintaining them continuously through the summer and throughout the mating season, or rut, during the month of November. Other males roamed the mountains year-round.
Territorial male chamois have high levels of testosterone and cortisol, and they can monopolize females that enter their territories. Starting in summer, the animals expend large amounts of energy defending their territories, however, and eat drastically less during the month-long rut. They also suffer immunosuppression, making them vulnerable to parasites. Nonterritorial males, on the other hand, continue to forage normally, making them better prepared to survive the winter, but they tend to secure fewer matings (Anim Behav, 84:1061-70, 2012).
Warmer and drier years appear to alter the hierarchy, however. When there is not much snow, Corlatti noticed, females tend to stay at higher altitudes where forage is better quality, and there they encounter the nonterritorial males that roam those parts. In such years, subordinate males may secure even more mates than their territorial counterparts, though long-term paternity studies would be required to know for sure, says Corlatti, now a researcher at the University of Natural Resources and Life Sciences in Vienna, Austria. The chamois’ alternative reproductive tactics are the result of “complex environmental and physiological parameters that can change from year to year. This changing of environmental and physiological situations most likely fosters variation in the fitness of these two male types, [allowing] these two tactics [to] be maintained.” —Jef Akst
MATING BY MOONLIGHT
BREESE GREG, US FISH AND WILDLIFE SERVICE/WIKIMEDIA COMMONSEach spring during the highest high tides on beaches along the US East Coast, horseshoe crabs (Limulus polyphemus) emerge from the sea to engage in an astounding mating frenzy. After the sun sets, thousands upon thousands of the ancient ocean-dwelling arthropods crawl out of the water to lay, fertilize, and bury millions of eggs in the sand.
To secure some of those fertilizations, males employ one of two strategies. A primary male, typically young and fit, will grasp onto a female’s carapace as she moves along the beach, while several older satellite males crowd around to get in on the action. Although the attached male is pretty much guaranteed the most direct access to spray his sperm over the eggs, satellite males, especially if there are only a few of them, are still able to successfully fertilize some proportion of the clutch. According to H. Jane Brockmann’s group at the University of Florida, attached males must sacrifice eating while they cling to the female, sometimes for weeks at a time, a hardship that may be too taxing for older males (Anim Behav, 85:165-73, 2013).
Brockmann has found that females, too, appear to have their own ARTs, an unusual characteristic in the animal kingdom. She observed that some females consistently mate with just one attached male, while others have a suite of satellites tagging along. When Brockmann’s team experimentally ushered satellite males over to a single-mate female, she would ditch all the males and head back to sea (Behav Ecol, 23:999-1008, 2012). Brockmann’s preliminary evidence suggests that polyandrous females actively attract satellite males, even though females with extra suitors seem to lay fewer eggs. To make up for this, “there must be something they’re gaining from satellite males,” Brockmann says. —Kerry Grens
ARJAN HAVERKAMP/WIKIMEDIA COMMONSThere is no mistaking the male ruff (Philomachus pugnax) from the female—or so birders had thought for about 50 years. During the mating season, territorial males (see photo at right) of the migratory shorebird species show off their dark neck feathers and head tufts to establish a mating court, to which they invite white-tufted satellite males to help recruit females. Both male morphs successfully reproduce, and although they compete, their cooperation presumably yields greater mating success for all. Which type of male a young ruff grows up to be is determined by a single gene, a rare instance of simple Mendelian inheritance of a reproductive strategy.
In 2006, bird banders in the Netherlands discovered a third type of male—a rare morph that can be mistaken for a large female (Biology Letters, 2:161-64, 2006). Although the mating strategy of the female mimic, called a faeder, is still unclear, David Lank of Simon Fraser University in Canada says he’s seen faeder males casually hanging around the females. Once a female squats to mate with an ornamented male, the faeder will jump in to form what amounts to a ruff sandwich.
To determine the genetic underpinnings of the new morph, Lank added them to his breeding flock and looked for patterns of inheritance. It turned out that the faeder morph results from a dominant allele at a second locus in the genome (Biology Letters, 9:20130653, 2013). If a bird is homozygous for the recessive non-faeder allele of that gene, then the second gene determines whether he develops into a satellite or a territorial bird. “In terms of alternative male mating strategies, this is the cleanest, simplest, genetically-based, one-gene-equals-one-morph kind of system,” says Lank. —Kerry Grens
JENNIFER O. REYNOLDSMale plainfin midshipman fish (Porichthys notatus) serenade for sex. By contracting a large sonic muscle around their air-filled swim bladders to generate low-frequency humming sounds, they woo females into their staked-out nest sites. But in about 10 percent of males, the sonic muscle is some 20 times smaller, allowing the production of only little buzzing sounds called grunts. Unable to sing, the smaller males, known as sneakers or type II males (photograph at right, bottom), swim about stealing fertilizations in the nests of the guarding, or type I, males (right, top).
In 2010, McMaster University graduate student Karen Cogliati set out to determine how the different male types fare with regard to reproduction. At low tide, Cogliati would walk along beaches in British Columbia, and occasionally Washington and California, flipping over rocks to reveal nearly dry nest sites, where she would find both male and female midshipman fish among clutches of eggs. She took brood samples from each nest and fin clips from the fish she found, then headed back to the lab to determine the paternity of the eggs she’d collected.
To her amazement, the guarding males fathered an average of just 52 percent of the eggs in their nest (Behav Ecol Sociobiol, 67:399-408, 2013). “Paternity was really low,” Cogliati says, “not at all what we expected given the past literature on species with alternative reproductive tactics.” This was particularly surprising given that midshipman fish guard the nest and eggs, a level of paternal care that had previously been associated with paternity levels of greater than 80 percent in other fish species, she notes.
By exhaustively sampling a single beach, Cogliati and her colleagues determined that while guarding males father on average slightly more than half of their own nest’s eggs, they also fathered more than 10 percent of eggs in other males’ nests (Behaviour, in press). “The guarding male tactic is behaviorally flexible,” Cogliati says. “They can also cuckold.” This may be an important aspect of the type I male’s reproductive strategy, she adds. Competition for nest sites is often high, and if a male fish fails to secure a spot, cuckoldry may be his only option. Of course, without a massive sonic muscle, type II males don’t have such flexibility. —Jef Akst
JENNIFER O. REYNOLDSEvery spring, the waters of Scotland’s Loch Lomond churn with randy lampreys. A male will grip a female by the head with his sucker-like mouth, loop his tail around her body, and rhythmically squeeze her with his body until ova burst from her cloaca. The male then ejaculates sperm, and external fertilization occurs. At the end of the erotic affair, other males that have been lurking nearby sometimes fertilize the expelled eggs on the sly, discovered John Hume, who studied lamprey sexual behavior as a PhD student at the University of Glasgow. “It’s a free-for-all,” he says.
Most lampreys hatch in freshwater, then journey out to sea to grow and mature, returning to natal streams or lakes to spawn the next generation before dying. But some members of lamprey populations develop into smaller forms that stay put in lakes, streams, or rivers for their entire lives. Researchers had long assumed that they were seeing the roots of lamprey speciation, because the act of fertilization just described requires the sexes to be close to the same size; a much smaller male lacks the strength to express eggs from the female. But Hume discovered that, in the populations inhabiting Loch Lomond and its surrounding streams, the migratory and smaller, nonmigratory morphs—as well as a third, medium-size freshwater morph that migrates from the lake into a nearby river to breed—were genetically the same species, and shared an abundance of gene flow. The larger males did the work, but the smaller males often cashed in.
And it wasn’t just the little guys that stole fertilizations from the larger males, Hume found. Rather, he observed all three male morphs jumping in at the end of courtship between lampreys of all sizes (J Fish Biol, 82:1093-100, 2013). “That was very, very unexpected,” says Hume, now a postdoc studying Great Lakes lampreys at Michigan State University. “They’re all sharing genes in all three directions,” and embryos were equally viable whether formed from the egg and sperm of like parents or of two different morphs. Hume suspects that epigenetic mechanisms, driven by resource availability, determine which form resulting offspring in such a mixed population will take. “But we can’t say that definitively,” he cautions. “No one’s done the work yet.” —Bob Grant
© FOUR OAKS/SHUTTERSTOCKSome male African flightless dung beetles (Circellium bacchus) are stereotypical dudes. Burly bachelors wrestle each other in intense sparring matches, and the winner gets the girl—plus the nutritious ball of dung she has rolled to serve as a nursery for her developing larva.
But lurking in the background are diminutive males—some of which are half the size of their more aggressive counterparts—with a different strategy for securing mates. While their competitors battle it out, they sneak copulations with females sitting on the sidelines. The smaller males will also dig clandestine tunnels to access and mate with females again after the fight is over.
Ecologist Chevonne Reynolds was the first to document this alternative reproductive tactic in the beetle species (regarded as vulnerable, though not yet officially listed). Other dung beetles—especially species with horned males that fight and hornless males that sneak copulations—are well known for using this devious strategy, and Reynolds suspected that African ball-rolling dung beetles might also be employing the sneaky tactic. In late October 2011, while teaching Duke University students studying abroad as part of the nonprofit consortium Organization for Tropical Studies, she watched C. bacchus flock to fresh dung heaps to fight and mate.
Reynolds observed smaller males, who would have no chance in an insect wrestling match against a large male, quickly copulate with females both before and after contests. She speculates that the evolutionary fitness of the two male phenotypes may be roughly equal, because the sneaker males have much larger testes, relative to body size. It may well be that the sneaker males boost their odds of fathering the female’s offspring by releasing more sperm per mating, says Reynolds, now a PhD student at the Percy FitzPatrick Institute of African Ornithology in Cape Town, South Africa. (See “The Hidden Side of Sex.”) “It’s sort of like a raffle: the more sperm you have in the lottery, the larger your chance of fertilizing the egg.” —Bob Grant
ROY L. CALDWELLSmall male algae octopuses (Abdopus aculeatus) looking to mate are often faced with much larger males guarding the most desirable females. So they have devised ways of sneaking in. Observing the behaviors of octopuses in waters near Sulawesi, Indonesia, more than a decade ago, Christine Huffard of the Monterey Bay Aquarium Research Institute and her colleagues saw dominant male octopuses defend and aggressively mate with females. But they also saw smaller males hover around the dominant males in attempts to cop copulations with their mates. Some sneaking males would simply wait to approach females until guarding males weren’t looking. Others would mask their distinctive male stripes—presumably using skin cells known as chromatophores, which other cephalopod species employ for color-changing displays and camouflage—to resemble females, and for good measure, flatten themselves against the seafloor and creep ever so slowly past the guarding male to extend a mating arm down into a female’s den. (See photograph; male is on left.)
“Size always determined [which male] won the fight,” says Huffard. “So smaller males didn’t have fighting as an option. But one option they did have was to access the females in their dens.” Female mimics could be so convincing that some alpha male octopuses even attempted to copulate with them.
But both sneaking strategies were uncommon, says Huffard. “Males adopting female camouflage were very rare,” she says. “In any mimicry situation, you don’t want the mimics to be so common that you lose that advantage and lose the ability to fool onlookers.” —Tracy Vence