Animal Weapons

by Douglas J. Emlen

  We have to go back to the beginning for the answer: eggs and sperm. Both sexes offer a copy of their genome to every child, but the packages they come in differ. Eggs are nutrient-rich globs of protein, carbohydrates, and lipids, stuffed into protective membranous cases. Sperm are little more than wriggling, self-propelled packets of DNA. When sperm and egg fuse to launch a new life, it’s the resources provided by the mother that first feed it. Billions of cell divisions unfold in a precise cascade of cell-cell interactions as tissues and organs form, and appendages and skeletons grow. All of this takes fuel; proteins to build new cells and tissues, and nutrients and energy to power the literally trillions of chemical reactions. Development is expensive, and eggs provide the energy and nutrients sustaining this process.

  Females of all animal species produce larger reproductive cells (called “gametes”) than males. Eggs are bigger than sperm, and this difference in material investment is far more substantial than most of us appreciate. Humans are rather ordinary in this respect, but we’re a good place to start. The female egg is the largest cell in the human body. It measures almost a fifth of a millimeter across—about the size of a period (.) on this page—and it’s just visible to the naked eye. Sperm are the smallest cells in the body, and a hundred thousand could fit into the volume of a single egg.2

  In many animals differences in egg and sperm size are much more profound. A zebra finch mom fits nicely in the palm of your hand. She’s roughly four inches beak to tail, but she lays an egg that is over half an inch across. By weight, a finch egg is 7.5 percent of the weight of her body.3 That’s equivalent to a human female producing an egg weighing eleven pounds. Kiwis have the most gargantuan of all gametes, relative to their body size: brown kiwi moms lay eggs that are a fifth of their body weight.4 Our human mom would need to produce a thirty-pound egg to compare—the size of an eighteen-inch watermelon.

  Asymmetry in gamete size has consequences that ripple through the biology of animal species. For one thing, females can’t produce as many gametes as males do. With the same amount of resources, males produce trillions of sperm. And these numbers stack up fast, since each male produces similarly copious quantities of sperm. A human female produces roughly four hundred viable eggs over the course of her lifetime. A male, on the other hand, cranks out one hundred million sperm every day, easily four trillion over his lifetime.5 Scale that up to a population of a thousand people, and there are a quadrillion (that’s fifteen zeros) more sperm than there are eggs. Scale it to the current human population and there are a septillion (twenty-four zeros) more sperm than eggs. And humans aren’t even an extreme example. The simple fact is that in virtually every animal species there are nowhere near enough eggs to go around. The result is competition.

  The size of female gametes is important for another reason. Large, nutrient-rich eggs are expensive, and they take time to produce. Depending on the species, females may take days or even weeks to recover from producing one batch of eggs before they are ready to lay another. Males, on the other hand, tend to need only a few minutes. Thanks to their gametes, females generally take longer to “turn around” between breeding events than do males.

  Females also stand to lose more than males if a breeding attempt fails. Although each sex invests nutrients, energy, and time in producing gametes, the amounts they invest are different. Females spend more than males each time they reproduce and, because of this, the cost of abandoning a brood is much steeper for females than it is for males. As a result, whenever additional offspring care is required, it’s generally the females who provide it.6

  Females invest in offspring in all sorts of interesting ways beyond simply producing eggs. Cockroach moms hold fertilized eggs inside their bodies until they are ready to hatch, feeding and protecting them in an insect equivalent of a mammalian pregnancy.7 Scorpions wear bundles of babies on their backs for weeks after they hatch.8 Dung beetle moms excavate tunnels into the ground and provision their babies with balls of buried dung; a few species even lock themselves inside a crypt for a year so they can guard the young as they grow.9

  Preparing nests, pregnancy, guarding eggs, and feeding and protecting young all take time. These forms of maternal care can increase the latency between reproductive events still further, compounding the rift in relative investment between the sexes. Males can invest in offspring, too, as they clearly do in jacanas and humans, but it’s surprisingly rare in the animal world. In most animal species, males provide little more than sperm, and this means they recycle an awful lot faster than females.

  Turnaround times are tremendously important for explaining animal weapons, because whenever they differ between males and females the result is always competition. If you walk into a population of just about any animal species, and you count how many individuals of each sex are physiologically capable of breeding right now, you’ll find that all the males are able and willing, but many of the reproductive-age females are not. Some of the females are physiologically unavailable—out of commission, so to speak—in between broods. Female zebra in the midst of pregnancy cannot conceive new foals. Cow elk cannot start new pregnancies while they are nursing existing young. Females that are locked into a current breeding event are “out of the pool” since they are not available for conceiving new young. If all of the males are able to breed, but only a fraction of the females are, then there will not be enough females to go around.10

  Enter nature’s most pervasive and potent form of competition, what Darwin coined “sexual selection.”11 Individuals of one sex compete for access to the other. In principle, sexual selection can work both ways, with either males or females competing. In reality, except for rare cases such as the jacana, it almost always involves males competing for access to females.

  Female jacanas still produce the larger gametes (eggs are bigger than sperm), and it takes them a few weeks to recover between clutches. But this is where female investment stops. Male jacanas spend up to three months tending to eggs and chicks and, as a result, their turnaround time is longer than the females’ (seventy-eight days, on average, compared with twenty-four).12 At any point in time, roughly half of the males in a population are tied down with existing eggs or chicks, leaving just a few of them free to start new broods, while most of the females are yolked up and ready to go. They could lay eggs immediately if only they had access to a territory-holding, reproductively ready male. In jacanas, there simply are not enough receptive males to go around, and females battle it out for the chance to breed. Sexual selection, rather than selection from predators or prey, drove the evolution of blazing yellow spurs in jacana females.13

  * * *

  On the hanging scale of parental care (yes, the same one debated by so many busy couples today), the total time invested by jacana dads exceeds the time invested by moms, and the scale tips toward female competition. In some other species, including many birds, the time invested is similar for moms and dads—females lay eggs that are much larger than sperm, but both parents take turns incubating the eggs, and both parents bring food to the nest to feed the chicks. The scale in these cases hangs closer to level, and sexual selection is relatively weak. But these species, too, are relatively rare.

  For most animals, parental investment is weighted heavily on the side of females. In one pan sits a tiny sperm, in the other a monstrous egg. Add to that all the time spent preparing a nest; time spent incubating or protecting the egg; time spent nurturing, feeding, and in some cases teaching the young: all of this compounds the initial investment discrepancy arising from the gametes. In these species, the scale tilts sharply to one side, and the arrow points to male competition. The greater the tilt, the stiffer the resulting competition, and the more likely we are to find weapons.

  African elephants are a perfect example, and in many ways they represent the opposite end of the investment continuum from jacanas. Bulls invest nothing in the development or post-birth care of their young. All they provide to the females are sperm. Female elephants, on the
other hand, have a two-year gestation period and, after birth, they nurse and protect calves for an additional two years. When a female does become fertile, it’s only for the exceedingly brief period of five days.14 Female elephants are only receptive to fertilization for 5 out of every 1,460 days, less than one-half of 1 percent of their lifetime. As a result, there are very few females on the landscape able to breed at any point in time, and way too many males.

  Because of this scarcity of fertile females, bulls engage in intense battles with dangerous tusks for chances to mate. Competition among African elephant bulls is severe, vastly exceeding that found in female jacanas. In jacanas, females recycle roughly three times faster than males (24 days compared to 78 days), translating into almost three times as many reproductively ready females as males on floating territories. In African elephants, males recycle more than three thousand times faster than females (less than half a day compared to 1,460 days), and it’s not uncommon for many dozens of males to compete for each receptive female. Even at the worst “singles” bars, men don’t face odds this bad—possible exceptions being pubs in nineteenth-century mining camps of the American West and, until recently, the bowling alley at the McMurdo research outpost in Antarctica.

  Bulls can hear advertisement calls of females—subsonic rumblings carried through soil—at distances of more than six miles, bringing tons of feisty rivals into the fray. Bulls guard females through their brief estrus, but guarding requires consistent victories in the face of stiff challenges, and only the biggest and best-armed males stand a chance. Elephants continue to grow as they age, and elephant researcher Joyce Poole and her colleagues showed that males had to live for thirty years before they even got to play the game—before they were big enough to have any chance of winning fights at all. Most of the time, only males over forty-five actually managed to mate.15 (Contrast this with females, who generally begin calving by age thirteen). In one long-term study of elephants in Amboseli National Park, Kenya, fifty-three out of eighty-nine males failed to sire any offspring at all, and the overwhelming majority of calves were sired by just three males.16

  Victorious males wield the longest tusks and tower over their rivals, standing more than twice the height of smaller males. To the victor go the spoils and, in elephants, this means the oldest, largest, best-armed bulls sire the offspring.

  Battling bulls

  Today, there are just two species of elephant, African and Asian, but not all that long ago a great many species roamed the steppes and plains of Africa, Europe, Asia, and the Americas. More than 170 species have been described, and all but the very earliest had impressive weapons.17 Columbian mammoth tusks extended sixteen feet and weighed more than two hundred pounds apiece. Anancus was a “smaller” cousin to the mammoths, standing only ten feet tall, but the paired tusks of bulls reached thirteen feet apiece. Even African elephants were impressive in their day. In recent decades, poaching and the illegal ivory trade have drastically reduced the size of tusks, and it’s rare to see bulls with full weapons. But museums exhibit tusks that are eight feet long and one hundred pounds each, grim testament to the intensity of sexual selection resulting from male competition.

  * * *

  Weapon diversity in relatives of the African elephant

  Of course, surpluses of pugnacious young males compete for the attention of females in human societies, too (the reason automobile insurance costs so much more for adolescent men than it does for women), and nowhere was this more apparent than in the European knights of the eleventh and twelfth centuries,18 when there was a severe limitation of eligible, reproductively ready women, and an excess of battling rival males.

  European society during the eleventh and twelfth centuries revolved around locally powerful noble families clinging tenaciously to land and power, and surrounded by masses of tenant peasant workers and laborers.19 To prevent the dissolution of family wealth, all of the lands and monies passed in their entirety to the eldest son. Noble families tended to be large, with six or seven sons to a household, and any other form of allocation, it was believed, would erode family power.20

  Marriages, too, were all about the consolidation of wealth and power. Marriage outside of the aristocratic class was unthinkable. Within class, marriages were strictly arranged by heads of households.21 Eldest sons often had to wait years, until their fathers were old enough to cede power, before they could marry and start families of their own. But at least they had options. They stood to inherit the family wealth, and were therefore attractive suitors for the daughters of other noble families.

  For all of the rest of the noble sons—and there were a lot of them—the marital landscape was bleak. With no inheritance to claim, they were not considered attractive matches. A father permitting such a man to marry his daughter would be required to divide his wealth,22 and there were surprisingly few reproductive-age daughters to start with. The harsh reality of the time was that death during childbirth was commonplace, and heads of households often married three or four times in succession.23 Existing heads of households had first-priority access to marriageable daughters from other estates, followed, in turn, by eldest sons. Indeed, the need to “wait in line” for a wife was the main reason eldest sons had to delay so long before they could marry (the other reason was to prevent them from producing heirs that could threaten the power of the existing head of the house).24 By the time heads of houses and eldest sons were accounted for, very few “single ladies” remained.

  In fact, the only real option for younger sons of noble families was to marry an heiress—a woman who stood to inherit her family’s estate. The violent nature of the day did occasionally result in the total loss of male heirs to a family, in which case a daughter could inherit the wealth.25 Such a woman, if she chose, could afford to marry a man without an estate of his own, providing him with a chance to found a new dynasty. But noble heiresses were just about as rare as estrous female elephants, and competition for their favors intense.

  Noble sons began training for battle by the age of seven, when they signed on as vassals of other knights. They trained incessantly, shadowing their mentors into battle, and learning to run and ride with mail and armor. They could be knighted by the age of fourteen. From that point onward they traveled in bands, roaming the landscape in search of opportunities to demonstrate their valor.26 There is no question that the primary objective for these men was attracting a wife. Everything they did revolved around besting rival males and, in the process, wooing the favors of noblewomen. Unfortunately, most of the men failed. The few who did succeed in wooing an heiress generally did so after spending thirty to forty years battling rival males and ratcheting their way to the top of the pack.27

  Actual battle was the best test of a knight’s mettle, but it did not lend itself to the attention of women. There simply were not enough battles to go around,28 so the focus of male aggression turned to tournaments. Tournaments afforded knights with opportunities to demonstrate their strength and courage in front of noble women, and everything about these spectacles reeked of sexual selection.29 Men fought each other in ritualized battles of strength, often charging from opposing directions on horseback with leveled lances in high-speed clashes that shattered wood and knocked contestants to the ground.

  Judges and scribes meticulously recorded outcomes and consolidated results from tourneys across the land, ranking the knights accordingly, and noblewoman studied these standings.30 Knights emblazoned their armor with colorful plumes and tassels, and bore their family heralds on their shields and breastplates (coats of arms, incidentally, provided information on the genetic quality of a male—his bloodline—not unlike the colorful trains of peacocks).31 Women inspected the contestants beforehand, watched the battles from front-row seats, and awarded the prizes. And a knight who proved his worth in tournaments could occasionally earn the hand of an heiress.32

  * * *

  Sexual selection differs from most forms of natural selection in ways tailor-made for pushing traits to
their extreme. For one thing, sexual selection can be a lot stronger than natural selection. Whenever a small subset of males monopolizes access to large numbers of females, the disparity in reproductive success skyrockets. A few victorious males sire dozens or even hundreds of offspring, while the overwhelming majority of males sire none. When payoffs for success are high enough, weapons can evolve to really big sizes.

  Sexual selection also tends to be more consistent than other forms of selection, and this, too, can push traits along the path to extreme. When dark mice moved into coastal beaches, mismatched mice got hammered, and natural selection favored a shift from dark to light. Had we sampled beach populations shortly after the dark mice moved in, we would have measured strong selection acting in one direction, pushing the population toward lighter and lighter fur.

  But this pulse of evolution was brief. As soon as beach populations had lighter fur, the directional change ceased because mice now matched their surroundings—any lighter and they would be too white; any darker, and they’d stand out as they did before. Natural selection on fur color stabilized. It reached a balance, and populations now hovered around this new value for the trait.

  Such is the nature of most natural selection. Populations adapt to surrounding conditions until they reach a local optimum. Environments may change and, when they do, selection kicks in once again favoring new trait sizes or colors that work better in the new surroundings. But these shifts also are expected to stabilize. Ocean sticklebacks have sported three long spines and fifty-two armor plates for hundreds of thousands of years. When some of these fish found themselves dumped into freshwater habitats, natural selection in their new environment led to a rapid shift from three spines to one, and from many armor plates to few (fourteen plates).33 But once these populations reached their new optimum, the change in armor stopped.