Animal Weapons

by Douglas J. Emlen

  Even when natural selection is directional, its effects often cancel so that the net effect is still stasis. When physical environments change, they tend to fluctuate back and forth. Winter gives way to summer, but reverts back again each year to winter. Wet years are offset later by dry years, and vice versa. Even glacial ice sheets advance and retreat in cycles, and ocean levels rise and fall. When animal populations evolve in response to these changes, they do so in an oscillatory fashion. Mice become lighter, then darker, and then lighter again. Many populations adapt continuously to changing patterns of natural selection, but the directions of these changes cancel so that the long-term trend is stasis.34

  This is not how sexual selection works. In battles for access to reproduction, males compete with rival males. The environment that matters for performance is a social one—other males with whom a male does battle—rather than temperature or sea level or other physical features of the landscape. And this social environment evolves in tandem with the weapons. As antlers or horns become bigger, so, too, does the standard against which a male must contend. Like a sliding scale, each increase in weapon size resets the baseline of the population, selecting, in turn, for yet another increase.

  Rhinoceros beetle horns

  Imagine a population of rhinoceros beetles where the average length of male horns is one-half inch. In this social environment, a few males stand out. A mutation increasing horn growth has given them three-fourths-inch horns. These males win battles the most frequently; they mate with the greatest proportion of female beetles; and they populate later generations with disproportionate numbers of their kind (including sons wielding three-fourths-inch horns). Over the next few dozen generations, the population shifts. It evolves in response to sexual selection so that now the average size of horns is three-fourths inches.

  The benefits of a three-fourths-inch horn aren’t so great anymore, because now everybody has horns this big. The evolutionary increase in horn length reset the standard for male competition. Into this new social milieu another mutation arises, this time leading to a one-inch horn. Males with these new alleles now have longer horns than their opponents, and they begin to win. So the new alleles sweep through the population as the largest horned males outcompete the earlier, three-fourths-inch rivals, until the population has evolved to this new weapon size. The scale has shifted once again. The population has ratcheted up to the new norm, and it stands poised and ready for the next mutation leading to still another increase in weapon size.

  Because social environments evolve in tandem with increases in weapon size, sexual selection can push populations along a path of unending directional change.35 Selection in this social context is not likely to oscillate. Measure selection in a beetle population now, measure it in a decade, measure it one thousand years in the future, and you’re likely to find the same thing: males with the biggest horns win. The particular weapon size performing best will change (one-half-inch horns give way to three-fourths-inch horns, and then to one-inch horns, and so on), but the direction of selection remains constant. All else being equal, this form of selection is going to generate a lot more change than selection oscillating back and forth or holding fast.

  Most of the truly gargantuan armaments in the animal world owe their excesses to this form of competition. Reproduction is the “other half” of success, in an evolutionary sense (we’ve already looked at survival). But it’s the half that really matters. When you strip the essence of life to its core, the only reason to survive is to have a shot at breeding, and, at the end of the day, it’s how many offspring you produce that determines success or failure on the evolutionary stage. Individuals reproducing the most win, plain and simple. They contribute more copies of their genome to subsequent generations of the population than other individuals do. Their alleles persist, while others gradually disappear.

  Battling beetles

  Sexual selection arises whenever individuals of one sex differ in their reproductive success. Some males sire three offspring while others sire four; the result is selection for traits that help an individual sire four. But selection in this case will be relatively weak, since the difference between winners and losers is small. When differences in reproductive success get larger, the intensity of selection increases. In extreme populations sexual selection is so severe that it eclipses all other forms of selection acting on these animals.36 Nothing else matters—not feeding, physiology, or immunity to parasites or disease—and males sacrifice everything for a chance to win the reproduction race.

  5. Economic Defensibility

  Structures of sexual selection are legendary for their extravagance. But not all of these traits are weapons. Sometimes there is nothing for males to guard; they cannot gain access to females through fighting, so weapons are useless. In these species males compete indirectly, scrambling for the attention of females by wooing them with dances, songs, or bright, gaudy displays. Male túngara frogs broadcast their location with eerie, incessant calls, ringing whines and chucks that are both energetically demanding and dangerous. Males sing for hours upon hours, night after night, even though their calls attract predatory bats.1 The odds that they will be eaten are high. But the price of failing to attract a female is even higher, so males take their chances and risk death.

  Male birds of paradise grow long and colorful tail feathers, which they spread in stunning displays to females.2 They, too, are risking death, since their elaborate trains make flying clumsy and, as they strut their stuff, they stand out from their backgrounds in full view of predators. Yet they dance recklessly, bobbing brightly colored plumes and shrieking loudly in a biological equivalent to flashing neon signs. Despite the immense risk, males pour everything they have into desperate attempts to outshine the next male. Reproduction is the currency that matters here, and getting picked by a female is the only shot males have at keeping their genetic heritage from vanishing into the abyss of history.

  This form of sexual selection is called “female choice” because females actively pick particular males based on the attractiveness of their displays,3 and it can be just as intense and unending as selection from male competition. Female choice also creates an evolving social backdrop because what is bigger or brighter or flashier depends on the displays of everyone else. Here, too, the baseline ratchets up as each new increase in trait size changes the social context and shifts the standard for what females find attractive. The difference is these extreme traits are ornaments, rather than weapons.

  In a sense, males compete with rival males regardless of whether sexual selection proceeds through female choice or male competition and, in many respects, the process—the intensity, consistency, and social nature of selection—is the same regardless. Why, then, do some species embark on a trajectory of overt competition leading to the evolution of weapons, while others end up dancing or singing with displays? Here is where the ingredients for arms races come into play, for these are the pieces that must fall into place if sexual selection is to trigger evolution of extreme weapons. The first ingredient is competition, the essence of all sexual selection. The second is economic defensibility.

  * * *

  Beetle horns are impressive things. They form during metamorphosis when parts of the body wall grow into rigid protrusions that stick out from the body proper. Horns can be curved, straight, broad, or branched, depending on the species. In many ways they resemble the antlers of moose or elk. Like antlers, beetle horns are typically a male trait. And, like antlers, horns in the largest males can reach enormous proportions. Sometimes a horn will comprise as much as 30 percent of the body weight of a male. If you were to scale these animals up to human dimensions, this would be the equivalent of producing a pair of arms or another leg and wearing it on your head.

  Horns have cropped up in all sorts of beetles, from knobby fungus beetles and weevils, to flower beetles, harlequin beetles, rhinoceros beetles, and dung beetles. Dung beetles, in particular, are noteworthy because only about half of the species
produce horns, raising the question of why just some species have weapons. There are entire dung beetle genera with hundreds of species that lack horns completely, and other genera that all have horns. I particularly like the genus Onthophagus because it contains both. Onthophagus turns out to be one of the most species-rich genera of any living thing anywhere, with almost two thousand species cataloged and another one thousand waiting to be described. What is most remarkable is the diversity of horns that they produce and, in this genus, even closely related species can differ so that one species has horns and the other does not.4

  The heart of dung beetle diversity resides in Africa, where eight hundred of the described Onthophagus species are native.5 In the Great Rift Valley, for example, gazelles, waterbuck, buffalo, giraffes, and elephants, as well as spectacular migrating herds of wildebeest and zebra, all contribute to the copious production of dung. Not surprisingly, dung beetle numbers in these areas can be very, very high.

  After weeks spent securing the necessary permits, I finally had a chance to look for dung beetles in Tanzania in 2002, while coteaching a field course through the University of Montana. With armed guards standing on the roof of our vehicle spotting for lions and angry Cape buffalo, I’d rushed from the truck with gloves and a spade to poke through manure as fast as I could. In this way, I was able to sample beetles from buffalo, gazelle, and giraffe dung. But the real find that day was a pile of fresh elephant droppings in the middle of the road. We must have just missed the elephant—the pile lay steaming between the rutted tire tracks. I promptly did what any field biologist would do. I scooped it into a plastic bin and brought it back to camp. That evening, I placed the dung onto moist soil away from our tents and sat back with a ring of students and headlamps to see what would happen next.

  Never in twenty years of traveling the world in search of beetles have I witnessed an abundance of insects like I did that night. When they first arrived I tried to catch them, count them, and place each in a separate vial, but soon they came too fast. Even with five helpers beside me all attempting to catch and record these animals we couldn’t keep up. Beetles began to spin into our headlamps and plonk onto clipboards and into our laps, and everywhere they fell like rain from the sky. They began dropping by dozens at once. Beetles were tumbling into our hair and down the backs of our necks, and the mass of beetles that landed on my notepad was so thick I had to sweep them aside to write. It was as if somebody was pouring beetles from a bucket over our heads and onto the dung. Our best (and admittedly rough) estimate was that more than one hundred thousand beetles converged on that single pile of dung that night.

  Tourists may flock to the Serengeti to see lions or elephants or gazelles with twisted horns, but it is the tiny dung beetles who display the most dazzling weapons here. Just in that one sample, we observed all sorts of impressive weapons: long, forked horns curling up from the head; a single horn rising from between the eyes and arching over the back a full body length beyond the end of the beetle; a long cylindrical horn protruding from the thorax and bending up at the end like a coat hook; and species with one, two, five, and even seven different horns simultaneously.

  There were also many species with no weapons at all. Same season, same habitat, even the same pile of dung, yet some species invested in large weapons while many others did not. Why is it that only a few species produce these elaborate structures, given that so many other species do not? It turns out that in essentially every animal species with extreme male weapons the explanation is the same, and it comes from the logic of economics.

  * * *

  Nature is the ultimate economizer, relentlessly culling individuals who allocate resources poorly. Over time, we expect that populations will evolve to become increasingly efficient in their use of resources, investing in the growth of large structures such as weapons only when the benefits of having them outweigh any associated costs—that is, when they are cost-effective. By any measure, weapons are costly. They are expensive to produce, and they are expensive to use. Males incur risks when they fight, and fighting requires time and energy that could be expended on feeding and other life tasks. However, males with the largest weapons may derive significant reproductive benefits if these weapons help them secure access to females and keep rival males away. When the reproductive rewards are high enough, even extravagant weapons can be cost-effective.

  But under what circumstances will the benefits of investing in weaponry outweigh the associated costs? And when will the net benefits (benefits minus costs) of a weapon be the most profound? For many animals the answer depends on the kinds of resources that they exploit, and how easy these resources are to defend.

  Imagine a food resource spread out uniformly across a landscape—grass, if you’re a grazer, extending as far as the eye can see. As a male, where would you stand guard? Even if it were absolutely necessary for females to visit places with grass to feed, and even if they were willing to mate with you if you happened to be there when they fed, where would that location be? For food resources broadly distributed in space, there is no obvious location that is better than any other. It would be impossible for a male to anticipate where females were likely to visit since they could find their food anywhere. A male could still invest in the production of weapons, and he could use his weapons to deflect rivals from a patch of turf. But why should he bother to guard one particular area if all of the surrounding areas are just as good? And why should he pay the price of producing a weapon and fighting, if other males without weapons or territories do just as well as he does? In the parlance of economists, such behavior would not be cost-effective.

  If, instead, those same food resources were sparse, and especially if they were clumped into rare but concentrated patches, then the male would face a very different set of payoffs for guarding a territory. He would still pay a price for producing the weapon, and for expending time and energy fighting to keep rival males out of his territory. But now these territories would matter, and the benefits he could glean from guarding them might be significant. Females would be much more likely to visit him, since the resources they needed were few and far between, and one of the only places where they could access them was inside his territory. Indeed, lots of females might visit his territory and, if the resources were localized enough to be readily defended from rival males, he might be able to mate with a disproportionate number of these females—more females than other males who were not able to guard a territory, and possibly even more than males who were guarding a territory, if his territory were bigger or better than theirs or contained more of the limiting resources.

  What this exercise in the logic of economics reveals is a central tenet of the field of animal behavior: animals benefit most from fighting to guard territories when those territories contain valuable and limiting resources. The more limiting they are, and the more economically defensible they are, the higher will be the payoffs for successful guarding behavior.6 But here is where things get interesting, because whether or not a particular resource is valuable enough, or sufficiently localized to make its defense cost-effective, depends entirely on the perspective of the animal in question. What is defensible and valuable to one species may not be to another, and understanding what is valuable to each species is essential in unlocking the mysteries of their weapons.

  * * *

  Harlequin beetles win my vote for the world’s most ungainly animal. They derive their name from angular streaks of orange, brown, and black on their wing covers and bodies, but their most distinguishing features are their weapons: a pair of massive, chopstick-like forelimbs which, in the largest males, can reach to a span of almost sixteen inches. These males are so awkward that when they fly, they have to pull their forelegs back over their heads to keep them out of the way, and their bodies hang vertically as they whirr through the air in slow motion. If crabs could fly, this is what they would look like.

  Harlequin beetles are active during the rainy season in lowland tropical forests of Central and So
uth America. David and Jeanne Zeh studied them in French Guiana and in Panama, where their life cycle is intertwined with that of the fig tree locally known as Higuerón. Figs are among the true giants of neotropical forests. Reaching heights of 130 feet or more, these pale trees are easily recognized by their sticky, milky-white latex sap, and by the dozen or more swirling root buttresses spiraling out from their base.

  Fighting harlequin beetles

  Female beetles drill their eggs into freshly fallen trees, and the larvae feed on the decaying wood as they grow. The problem is that larval development can take a long time—up to a year or more—and this means that only the largest, thickest tree trunks will suffice. Only a collapsed giant will persist on the forest floor long enough for a female’s larvae to grow to full size. Fig trees like this don’t fall every day.

  When such a giant collapses, the beetles flock to it fast—drawn from miles away by the pungent scent of sap released during the cataclysmic ripping of wood and bark as the trunk snaps from its roots and crashes to the ground. A treefall like this tears a gash in the canopy of the forest, letting direct sunlight stream in. As the beetles arrive, they avoid this glare and crowd instead onto the shaded underside of the trunk. A fallen tree still sits on its branches, so that much of its length is actually perched several feet above the ground. Here, on the cool underside of the trunk, sap oozes from slashes nicked in the bark during the fall. Harlequin beetles feed on this sap and, more important, females use these gashes to insert their eggs under the bark of the tree.

  Male beetles battle for ownership of these prized spots. There are generally only one or two good territories per tree, and the nearest other treefall can be miles away. From the perspective of a male beetle, sap flows on a fallen fig are rare and defensible—perfect real estate for a fight. Males battle viciously with one another for possession of these inverted territories and the consequent opportunities to mate. They butt heads and grapple with outstretched arms, trying to hook and flip their opponents off the trunk. They rear up on hind legs and smash into each other, twisting and prying with their ridiculous forelimbs in surprisingly athletic scrambles, and slice at flailing limbs and antennae with sharp mandibles. After as much as a half hour of thrashing, the loser eventually falls to the ground, though often not before losing a chunk of leg or antenna in the melee.