Sex on Six Legs Read online

  Doug Tallamy and Thomas Wood from the University of Delaware took this one step further and pointed out that in addition, the species that evolve parental care have to have several preconditions. They have to reproduce only during a narrow window of time and during a brief period of the year, simply to make parenting cost-effective. They have to survive long enough to provide enough care to be meaningful, a tall order for animals as short-lived as most insects. And because insect eggs don't last well unprotected, particularly during long cold periods, the adults can't spend much of the summer or other favorable time of year growing up themselves. Instead, they have to be mature, or nearly so, at the start of clement weather so that the young ones get the full benefit of their care over the nicer times of the year. And last of all, some behavior patterns that could be adapted to parental care have to be present already in the species; Tallamy has seen the same kind of aggressive display used by mother lace bugs in defense of their brood when the females are discouraging overly ardent males during the mating season.

  These kinds of traits are sometimes called preadaptations, characteristics that happen to be present for some other reason and that can then be co-opted for a different use under different selective pressures. Natural selection can't use an empty palette; the raw material for parenting, or flight, or digesting a new food, or any other evolutionary innovation, has to be there already. Preadaptations aren't to be confused with evolutionary premonitions—you don't live in a climate with fleeting resources or bursts of cold because nature decided you should be a parent someday and thought those things would nudge you in that direction. They are more like the bits and pieces that happen to be lying around in your garage; if you want to build a bookshelf, and Home Depot doesn't exist, you are stuck using what you have available. So parenting used the lifestyles already out there and built upon them to make the patterns of care that we see today.

  Your Turn, or I Got Up Last Time

  Mothers are fonder than fathers of their children because they are more certain they are their own.

  —ARISTOTLE

  A MALE friend of mine says that when he used to take his son to day care, the other parents—all mothers—would stare at him like he was a child molester. Social progress of the last few decades notwithstanding, women in virtually all parts of the world do much more of the child care than men. It's also much more common for mothers than fathers to take care of the young in animals, insects included. Why is that?

  As with many basic truths, Aristotle was onto something when it came to parenting. The concept he alludes to above is what behavioral biologists call confidence of paternity. It implies nothing about a conscious awareness of one's likelihood of having been cuckolded. A male bird, say, that fetches mouthful after mouthful of painstakingly collected caterpillars to the chicks whose beaks gape insistently in his nest will not pass on his genes if it turns out that the female mated with another male during her fertile period several days or weeks earlier. Even worse, he has wasted time he could have spent trying to mate with other females himself. The female, on the other hand, either laid those eggs or didn't, and she was there at the time (aside from exceptions such as brood parasitism, which I'll discuss later). In mammals, where the events of mating and birth are even more widely separated, the problem of knowing which babies are sired by which male is even worse. There, of course, only the female can supply the offspring with milk, but males can perform other fatherly acts, for example, protecting everyone from predators or getting food for the mother.

  This disparity between the likely payoff to each sex that accrues from devoting oneself to one's offspring is often cited as the sole reason for males rarely being the sex that takes care of the young. It's evolutionary good sense to refuse to take on someone else's genetic investment, and males are generally thought to benefit more by competing for mates than by sticking with the offspring. But while certainty of paternity probably plays some role in the evolution of different reproductive behaviors, it is now emerging that it can't be the whole explanation. It's all very well and good to say that a male "should" go off and seek other females to mate with rather than stick around and care for the ones his current mate produces. But what are his chances of succeeding? Everyone likes to think he could have been a contender, but in reality, it's tough out there. Females may be scarce, they may be unwilling to mate with every philandering male that passes by, and the risk of being eaten by a predator before one is found may be high. Tip the balance of any one of these variables, and the parental care patter can skew toward mom, dad, or both. And insects are perfect test cases for ideas about "innate" parenting roles, because once the eggs are produced, either sex can easily protect or bring food to the babies, unlike mammals, where females have all the milk-producing apparatus.

  Single fathers are rare among insects, as they are elsewhere, but when they occur they do a bang-up job. Giant water bugs are true bugs, meaning they have strawlike mouthparts that they use to suck up their food. Some bugs, for example, aphids, merely sip sap, but the giant water bugs are fierce predators that ambush prey such as other invertebrates, fish, salamanders, and frogs. Once they grasp their victim, the bugs inject enzymes that liquefy the contents so that the interior can be extracted. About the size of an almond with the shell on, the bugs patrol lakes and streams around the world.

  When it is time to breed, males attract females by suggestively rippling the water's surface. Unlike most insects, after mating, instead of the female taking off with her store of sperm, giant water bug females from most species proceed to lay eggs on the back of the male, where they sit in neat pearly rows until it is time for them to hatch. Although the conspicuous bugs were noticed by early naturalists, the individuals bearing the eggs were assumed to be females. Even when the sex of the brooding individuals was known, scientists as late as 1935 declared that the females must be forcing the males to carry the eggs. The father, however, always mates with the female before allowing her to deposit her eggs, and the pair may go through several rounds of mating followed by egg laying, apparently at the male's behest. This probably ensures that at least a majority of the eggs carried are indeed the male's own. He then solicitously ensures the eggs are supplied with oxygen by periodically raising his back above the surface. Although more than one female can deposit her eggs on a given male, the space on his back may become limited, and the males do what they can to position females so that they lay eggs to fill in any gaps in the row. Carrying around the eggs is no easy task; their combined weight can be twice as heavy as the male himself. In one group of giant water bugs, the females lay egg masses that are attached to vegetation at the water's edge, and the males then guard the eggs while the female departs, perhaps to lay another batch fertilized and protected by another male. The male stays to guard the young bugs even after they have hatched, preventing both predation and cannibalism from occurring; a photograph of one such species shows the tiny striped nymphs clinging to a plant stem, as if to a pool toy, while their father bobs beneficently nearby.

  Biparental care, in which both parents cooperate to take care of the offspring, is at least as rare as male-only care among animals. It is seen in a few insects, however, including some that have the unfortunate attribute of being able to clear a room better than any other species. When I was doing my doctoral research at the University of Michigan Biological Station, the state-of-the-art Alfred H. Stockard Lakeside Laboratory had recently been completed. It was a lovely building, with excellent facilities for studying all kinds of local flora and fauna, from algae to woodpeckers. I was lucky enough to have a room to myself on the second floor, where I housed my crickets and recording equipment. Most days I worked happily at the microscope or with my experimental subjects, chatting with the other students and faculty, and generally having a grand time. But sometimes one of us would see David Sloan Wilson or one of his helpers walking toward the building with a white bucket, and we all knew to scatter. A multitalented evolutionary biologist, at the time Wilson was wor
king on burying beetles, and the stench was enough to make paint peel.

  As their name suggests, burying beetles locate recently dead animals by smell. If a male arrives at a carcass first, he sends out a chemical signal to attract a female. The pair then prepares the carcass as a nursery by stripping off any fur or feathers and shaping it into a ball. They cover their prize with specialized secretions that deter mold from growing (though this does nothing to deodorize the body, as we discovered to our regret). They then dig in the soil underneath the carcass, allowing it to sink into the forest floor. Once the carrion ball has been safely sequestered underground, the pair mates. The female then lays her eggs in the soil surrounding the carcass, and when the eggs hatch, the larvae beg for food from their parents by turning their heads toward mom or dad and waving their tiny arms. They are fed with either bits of carrion carved off the carcass like slices from a roast, or regurgitated meat that has been partially digested by a parent.

  Although this lifestyle has much to recommend it (a steady and nourishing food supply, protection from predators once the carcass is buried), burying beetles face a daunting problem: finding a suitable dead animal, and once it is found, defending it against rivals. Even avid hikers and wilderness lovers rarely come across a dead animal at all, much less one that is both small enough to handle and still fresh enough to provide the right environment for raising young. The beetles have extraordinarily sensitive odor detectors on their antennae, and can sniff out a carcass from miles away, but even so it is an extremely difficult undertaking. Recently acquired carcasses are therefore highly sought after, and if a burying beetle comes across a carcass that has already been colonized by another individual, pitched battles may result. Both parents participate in defense of their property, and if the male happens to be away from the carcass when a male intruder threatens, the invading male will kill the offspring and mate with the female. Female intruders are not as successful in taking over a carcass. If both parents are present, they can usually fend off the invaders and hang onto their prize. It is thought that this advantage of pair defense is what led to the evolution of parental care by both the mother and the father in this insect group. If the carcass is large enough, multiple females may stay and lay their eggs, although one of them is generally dominant over the others.

  Perhaps because of this difficulty in finding carcasses, one species of burying beetle has abandoned the role of "nature's undertakers," as one website refers to them, entirely. The substitute for dead birds and mammals that they chose, however, has to give one pause. They didn't switch to eating live insects, say, or any kind of vegetable matter. Instead, they are found in snake nests, eating the eggs and feeding them to the offspring. The beetles do not bury the eggs, since the snake takes care of that herself, and then leaves, so that the beetles do not have to face an irate mother snake. It seems to me that this was not the most sensible choice to have made—quick, which would you find easier to locate in a forest, a dead mouse or a snake egg?—but presumably it allows the beetles to exploit a resource that is less likely to be taken over by competitors.

  What Happy Families?

  I HAVE a Six Chix cartoon depicting two generic-looking insects sitting in armchairs; one is obviously bloated and looks a bit guilty, and is being reassured by the other, "It's natural to eat your young, Marilyn ... especially when they start running around the house like that—sometimes you just lose it."

  Insect mothers do indeed sometimes eat their young, but it's not annoyance that elicits the behavior. Infanticide and subsequent cannibalism are yet another manifestation of the rule that parenting is worthwhile only if it furthers the parent's interests. If investing in offspring now means losing out on future opportunities to reproduce, natural selection will not favor it. But a problem can arise if the world looked a certain way when a mother first produced her offspring and then changed once they were a little older. Because insects live their lives so quickly, often relying on transitory sources of food and shelter, and because they can replace a batch of eggs with relatively little trouble, simply offing one generation of young and starting from scratch is a more reasonable proposition for them than for at least some vertebrates, who need a lot of time to gin up another generation. This makes them excellent subjects for studying the circumstances under which infanticide is favored.

  Say a mother beetle lays a batch of eggs when the environment is benign and food abundant. She will benefit most by depleting her fat stores and turning them into eggs, since she can replenish those stores with the food around her. The eggs will survive best if she guards them on the plant, since predators would eat them if she were not around. But unexpectedly, the food supply dries up—maybe the gardener stops watering her food plant, or a cold snap makes it hard for her to move around and eat. What should she do? If she could read, she would be advised to take a look at an insightful paper by Hope Klug and Michael Bonsall pithily titled, "When to Care for, Abandon, or Eat Your Offspring." In it, the scientists outline the circumstances that favor each option. Cannibalism of offspring is particularly likely to evolve if parents can be selective about which young they eat, focusing on the lower-quality ones. Eating eggs is also expected to be common if doing so increases the parent's reproductive rate later on.

  These principles are nicely illustrated in a group of insects with the delightful name of assassin bugs. These often brightly colored bugs ambush prey from their perches on vegetation, and in many species one or another parent guards the eggs. One African species is unusual because the father, rather than the mother, is the caregiver. A male will guard the eggs laid by several females, so he does not lose future mating opportunities by running the bug equivalent of a day care center. Males frequently eat a portion of the eggs but tend to focus on those at the edges of the cluster. Interestingly, Lisa Thomas and Andrea Manica from the University of Cambridge in the United Kingdom found that those peripheral eggs were the most likely to have been parasitized by a tiny wasp and, hence, were going to yield baby wasps rather than miniature assassins. It doesn't appear that the males can tell which eggs are parasitized, because in the wasp-free laboratory they still eat eggs from the same position in the cluster as they do in the wild. In stead, natural selection presumably favored fathers that removed fewer of their future offspring from the gene pool. The eggs are an important food source; cannibalistic males didn't lose any weight while they were guarding, even though they couldn't go out and hunt.

  Infanticide and subsequent consumption of young was frequently observed in laboratory animals such as rats, and for many years the behavior was interpreted as abnormal and pathological, an artifact of captivity. Its documented occurrence in insects somehow didn't seem relevant to people, perhaps because we don't automatically see ourselves mirrored in their behavior. But then it began to be seen in wild animals such as lions as well, and now it is clear that at least some of the time it is probably adaptive in nature, because rearing young when life is harsh, or at the expense of the parent's well-being, may be too big a gamble for it to be continued. (Several kinds of animals, including lions, also commit infanticide without cannibalism, and of others' rather than their own offspring, for different but equally adaptive reasons.) If the going gets tough, the tough—and the smart—stop taking care of their children.

  Some insects even go so far as to produce infertile eggs, called trophic eggs, that they either eat themselves or use as extra provisions for the young that do hatch. Although in some cases this behavior may be opportunistic, with some eggs not developing because they are defective, in others the trophic eggs seem to have evolved as a food source. Ladybird beetles are particularly well known for the production of such extra meals and will lay more trophic eggs when prey are scarce, fewer if they are well fed. Starved female ladybird beetles may lay an egg and then immediately turn around and eat it, a much tidier solution to hunger than, say, gnawing off a limb. The trophic eggs often look different from those that develop normally. Putting extra provisions into addition
al eggs rather than simply making larger eggs that hatch into more robust offspring with the surplus may have evolved because mothers cannot manufacture larger eggs with more yolk reserves than they already do. Scientists suspect that trophic eggs may be cheaper to produce than the usual variety, although the details of this cost difference are still not clear. The trophic eggs can also deter earlier-hatching babies from eating the eggs of their tardier siblings, which means that the mother gets more offspring surviving to maturity.

  In addition to being excellent subjects for examining cannibalism, insects are perfect for exploring another stark reality of family life: parent-offspring conflict. In extremely influential work published in 1974, Bob Trivers, the same biologist who worked out some of the niceties of sex ratio theory discussed in an earlier chapter, pointed out that while parents and children have half their genes in common, they don't necessarily both benefit from the same things. Imagine that a mother beetle has a brood of twelve offspring. All else being equal, natural selection will favor her giving equal amounts of food to each of her children, because they are each equally related to her and equally likely to pass on her genes. But from an individual offspring's perspective, getting more care for itself at the expense of its siblings will also be favored, since it is 100 percent related to itself and only 50 percent related to its siblings. Thus there is a difference of opinion, evolutionarily speaking, in where the attention should go. Trivers called that difference of opinion parent-offspring conflict, and it is now thought to occur in a wide variety of animals and even plants. Trivers's theory explains many seemingly paradoxical family behaviors, including the grimmest: infanticide, discussed above, and its cousin, siblicide, the killing of one's siblings.