Planet of the Bugs: Evolution and the Rise of Insects

by Scott Richard Shaw

  Perhaps the most curious thing about internal parasitic wasp larvae is their startling array of body forms.8 The demands of life inside another insect are different as the larva grows, so with each molt it has an opportunity to acquire a new form more perfectly adapted to the needs at a particular stage of life. One might guess that, after hatching from its egg, eating would be its main concern. Finding food is easy enough, however; the larva effortlessly imbibes its liquid meal. It has a bigger worry: sheer survival. The host’s immune system may be disabled, but another source of immediate danger might be present: competition from other parasitic larvae, either of another or the same species, residing inside that same host insect. Because these competitors might pose a mortal threat, young wasp larvae have become hyperspecialized for defense. Many are born with a large head, powerful sickle-like jaws, and as I already mentioned, a long, taillike appendage for rapid locomotion. Their first job in life outside the egg is to swim about and aggressively eliminate their rivals.

  FIGURE 8.3. The caterpillar of a papilionid butterfly from Costa Rica, which has been parasitized by an endoparasitoid braconid wasp, Meteorus papiliovorus. The larva of the parasitic wasp has recently consumed most of this caterpillar internally, chewed an exit hole (visible on the right), and spun its silk cocoon suspended by a short thread. (Photo by Kenji Nishida.)

  For the middle part of its life, the wasp larva exists as a featureless white maggot. It has eliminated its competition, so it no longer has large defensive jaws. Given that its food consists of liquids, small particles, and cells, and that it does not even need to chew, its head becomes greatly reduced. The larva doesn’t have to travel, so it loses its swimming appendage but does not grow legs. Because its cuticle is thin, gas can exchange across its body surface, and the larva can stretch, making rapid feeding and growth easy. The wasp larva keeps this simple body form for one or more molts, over the middle part of its life, when it has little to do other than float about, suck in food, and get bigger. Its hind digestive tract remains closed.

  As it gains the large body mass needed to transform into an adult, the wasp larva prepares to pupate and exit its host, whose inside is largely devoured and destroyed, and will soon begin to decay. For most larvae, this is now a good time to get out. During the last molt several major changes occur. The mature larva acquires open spiracles, and becomes capable of breathing gaseous air through tracheal respiration. It develops a more complete head with mandibles capable of chewing an exit hole, and spinnerettes capable of building a silk cocoon. Silk glands suddenly and rapidly develop.9 Last but perhaps not least, the mature larva grows a complete digestive tract, and is finally able to eliminate its stored body waste.

  Double Vision: Two Other Ways of Looking at Parasitism

  The evolution of endoparasitism led to an exceptional burst of species originations, as various wasps diverged and adapted to life inside other insects. But the wasps still had one important trick left, which sparked yet another explosive radiation of species. You will recall that parasitism began when wasps attacked large host insects in wood, insects paralyzed by female venoms. Parasitism of this sort, where the host is permanently paralyzed, is termed idiobiosis, and the wasps that display this behavior are called idiobionts. But the vast majority of modern wasps don’t do this anymore. The only real benefit to paralysis was in preventing the host from harming a young wasp. Once endoparasitism evolved, however, paralysis was not only not required, it may have become a real drawback. Consequently, the vast majority of endoparasitic wasp species have developed another behavior where the host insect is either not paralyzed at all, or is only temporarily paralyzed during the egg-laying process. Parasitism of this sort is termed koinobiosis, and the wasps are called koinobionts.

  At first blush, the difference between idiobiosis and koinobiosis may seem rather small, but the implications for wasp evolution were enormous. The key distinction is that while the idiobionts turn the host into a defenseless hunk of preserved meat, the koinobionts insidiously allow the parasitized insect to live on, continue feeding, grow, and even molt, after they have placed their parasitic egg. This allows the wasps to attack a greater diversity of life stages. While an idiobiont is restricted to hunting the biggest host it can find because its larva can feed only on the meat provided, a koinobiont has the option of attacking much smaller hosts. Many koinobiont species put their eggs into very young insects, which are always more numerous than older ones, at a time when the host is so small that it cannot provide the parasitoid offspring with enough food to grow into adulthood. But a koinobiont larva gets around this problem by developing slowly or delaying its own growth; the host insect is allowed to live until it attains enough biomass to properly feed the larva. By delaying development just a bit longer, a koinobiont wasp allows its host to begin pupating, which often involves seeking a safe hiding place, and perhaps forming a silk cocoon. The wasp is therefore able to take advantage of the host’s protective behavior.

  Idiobiosis is a great strategy for attacking concealed insects, but it’s a poor strategy for attacking exposed ones. If an exposed insect is permanently paralyzed, it easily becomes a target for scavengers and predators, and the young wasp is killed along with its host. So perhaps the greatest benefit of koinobiosis was that it enabled parasitic wasps to escape from dead wood and assail hosts which lived and fed externally on plants. With one fell swoop, koinobiosis broke the bonds of habitat confinement in the late Jurassic forests.

  Secretive Societies with an Anal Fixation

  While the wasps became supremely successful by inventing ways to escape the confinement of rotting forest logs, another emerging clan of Jurassic insects thrived by evolving a whole new way of living inside them. These entrepreneurial insects were the first termites, also known as isopterans, and they developed complex group-living behavior, making them the first truly social insects. When entomologists speak of social organisms, we don’t just mean that they gather together in groups. Way back in the Devonian and Carboniferous years, hexapods and insects aggregated—creatures such as springtails, bristletails, mayflies, and roaches may have lived together in large numbers—but we do not define them as social. Strictly speaking, social insects do reside in groups, but they also have three broad characteristics.

  The first requirement of social behavior is a longer adult lifetime, such that two or more generations of individuals coexist. In most nonsocial insects, the adult lays eggs and then dies; most parents do not live to see their children mature to adulthood. The social insects’ longer life span allows them to accomplish the second requirement of sociality: cooperatively caring for the young. Social insects provide the next generation with food, remove their waste, and protect them from predators and parasites until they can successfully mature and contribute to the colony labor themselves. Last but certainly not least, social insects show a division of colony labor; this has allowed specialized forms (castes), which perform particular roles in the colony, to evolve. The vast majority are sterile workers, individuals that do not produce their own children but instead help raise their mother’s offspring. These workers construct the nest, forage for food, and feed the growing young. They do not defend the colony, however; this special task is performed by the soldier caste, sterile individuals with massive heads and mouthparts so specialized for defense that they can’t feed themselves and must be nursed by the workers. Only a very few individuals in a termite colony actually have their own children: the reproductive kings and queens, the first royalty in the history of the planet. Once the king and queen have established a new colony and raised the first generation of workers, they just sit back and enjoy the fruits of their labor.

  Termites are often regarded as social cockroaches. The most primitive living species are indeed similar to the wood-eating cockroaches (Cryptocercidae), and it is generally agreed that termites evolved from roachlike ancestors.10 The key to termite behavior and existence is their ability to digest cellulose from woody plants. Like their near cousins
the wood roaches, they accomplish this difficult feat by housing symbiotic microorganisms in their digestive tracts. Like all other insects, they have an external skeleton, and their foregut and hindgut are lined with skeletal material. Therefore, when they periodically molt their skeletons, termites lose their symbionts as well, and they must acquire new ones or else they will starve to death. They get their symbiotic gut microorganisms by a process called anal trophallaxis—literally by eating the feces of other termites. As repulsive as this behavior may sound, it is crucial to their survival, and without it some of the world’s most impressive and influential societies might never have evolved.11

  FIGURE 8.4. Considered the most phylogenetically primitive of living termites, Mastotermes darwiniensis, from tropical northern Australia, is the only living termite species that lays eggs in pods, like cockroaches. Pictured are three social castes: a soldier (upper right), a dark-colored neotenic reproductive individual, and several pale-colored workers. (Photo © Barbara Thorne.)

  Anal trophallaxis, ironically, solves another serious problem of subsisting in large societies: sewage removal. When insects (or other animals) live together in groups, their accumulating feces can promote the spread of microbial pathogens, such as bacteria and fungi. It can also attract predators. When caterpillars feed in groups, for example, they are far more likely to suffer from diseases or be preyed upon than solitary caterpillars dispersed in the forest. The termites avoid all this not only by eating their own feces but also by using it to build tunnels and arches within their nests.

  The earliest termite families probably contained only dozens or hundreds of individuals, but they were so successful that from them emerged over 2,900 modern species, whose colonies can include upward of several million individuals. Each species has its own unique habits and life style, but each contributes powerfully to nutrient cycling and vertebrate food webs. Because of their diversity and abundance, termites are among the chief decomposers of wood and other plant materials, especially in the humid tropics. They help create and move soils, and they are voraciously consumed by other animals. Consider that a single towering mound of an African Macrotermes can be 20 feet tall and contain more than 2 million worker termites. Compared to the termites’ own body size, if scaled to human proportions, one of these mounds is taller than any skyscraper. Along with the mounds of other termite species, they are all the more impressive when you consider that they are single-family dwellings. A Macrotermes queen can live for 10 years, sometimes laying as many as 30,000 eggs in a single day; over her life she may lay as many as 100 million. How’s that for a family picnic?

  Of Lice and Hen

  We can’t go picnicking in Jurassic park without mentioning the feathered dinosaurs. Much has already been written about one of the oldest-known birds, Archaeopteryx, which had a scaly dinosaur-ish head, large feathered wings with claws, and a long feathered tail.12 How did Archaeopteryx, along with other early birds, learn to fly? One popular idea is the arboreal hypothesis of gliding flight, which suggests that birds evolved from small, feathered, tree-dwelling dinosaurs that first flew by gliding from tree to tree. This is easy enough to accept, as it simply proposes that the birds mimicked a successful strategy pioneered by the insects about 150 million years earlier. But the gliding-bird hypothesis has a couple of drawbacks. Why did the ancestral ground-dwelling dinosaurs bother to move up into the trees? And what factors might have caused them to develop large feathered front limbs, even before those appendages were capable of flight?

  The cursorial hypothesis gets around these problems by proposing that birds learned how to fly from the ground up. Although hotly debated, this idea remains close to my heart for a simple reason: it asserts the fundamental importance of insect feeding as a driving mechanism in bird evolution. The cursorial hypothesis suggests that birds started out by running along the ground chasing insects. It further suggests that these animals first evolved large feathers on the forelimbs not for flight, but as improved insect-catching devices. The idea of ancient feathery dinosaurs rapidly running along through the forests, using their front legs as fly swatters, is not far-fetched. We have already come to grips with the notion that many small ground-dwelling Triassic dinosaurs were omnivorous carnivores and therefore highly insectivorous. And birds clearly evolved from these very same dinosaurs, little ones, like Ornitholestes, that would most likely have fed extensively upon bugs. It makes perfect sense to suppose that the earliest protobirds would also have eaten insects, and that strong selection would have favored any behaviors that improved their ability to rapidly catch insect prey. The main drawback to this hypothesis is evidence suggesting that Archaeopteryx spent little or no time on the ground: their claws show very little wear. But the two ideas need not be mutually exclusive. While Archaeopteryx may have been a flier living in the treetops, its immediate ancestors might have been ground-dwelling insect chasers.13

  Whatever you think of this wing-swatter idea, the history of the birds’ emergence is intertwined and codependent with the insects’ history and success. The first birds could move into the air, and what better reason than to gobble up the highly nutritious swarms that were everywhere around them? What the birds lacked in size, they made up in numbers, evolving into more than eight thousand modern species, the majority of them insectivorous.14

  One might suppose that once the feathery dinosaurs burst into the skies, they spelled trouble for the insects and hunted some of them to extinction; however, there’s not much evidence to support this. One group did disappear about the same time that the early birds arose—the titan insects—but they were overly large and noisy. They might have been all too easily hunted. Other groups appear not to have been impacted and actually became more diverse. We can safely assume that, from the first, birds were powerful selective forces which drove insect evolution in several ways. Day-active feeders, they probably influenced the evolution of many insects’ night activity. And as visually searching predators, they helped stimulate the evolution of crypsis, aposematic coloration, and mimicry. So when dinosaurs finally feathered their way into the air, they didn’t hinder insect success. Bugs had been flying for 150 million years by the time birds finally came along; by then they were pretty good at it.

  As birds diversified, insects were probably quick to exploit them. A new group of parasitic insects, the biting and chewing lice, were likely early bird colonists, though they’re not to be confused with their more common cousins, the blood-sucking mammal lice, which evolved much later. Both the biting and the blood-sucking lice (order Phthiraptera) originated first as chewing lice that themselves probably evolved from bark lice feeding in the nests of early birds. Since the chewing lice have such a strong affinity for living among feathers—so strong that we often call them bird lice—we can’t rule out the possibility that even earlier, ground-dwelling, feathered dinosaurs might have already had lice prior to the birds’ emergence. However they came to be there, the bird lice grew very successful in that miniature feathery forest: today, there are more than 1,200 modern species.15 The potential fauna of parasitic lice was limited by the available vertebrate hosts; they could never attain the levels of hyperdiversity displayed by the wasps, which exploited the extreme species richness of other insects. Despite this constraint, the origin of the parasitic lice nevertheless remains another page in the saga of how insects successfully colonized our planet.

  During the Jurassic years, Laurasia and Gondwana continued to drift apart, creating more coastlines, changing continental climates from dry to wet, and transforming arid Triassic deserts into moist forests, whose towering redwood-like conifers soared above even the tallest Diplodocus. Although a multitude of new dinosaur species stalked through fern meadows and clamored among ginkgo branches in the real Jurassic Park, most of the period’s diversification occurred at a microscopic level, among the bugs, beetles, wasps, and flies. As the Jurassic drew to a close, legions of parasitoid wasps drilled into dead trees for beetle larvae, while termites chewed delicately a
midst the ground litter, and tenacious lice nestled among the feathers of small dinosaurs. But insect and plant evolution in the Mesozoic forests was about to become vastly more visible. During the dawn of the Cretaceous, a profusion of colors erupted as the forests bloomed with the hues and scents of the first flowers. The Cretaceous period also saw the first bees, flower flies, and butterflies. Nearly three hundred million years had passed since plants colonized the land. Why did the world take so long to blossom?

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  Cretaceous Bloom and Doom

  The evolution of the flower in all its complexity of form, color, and scent has gone hand in hand with the evolution of pollinating insects.

  V. H. HEYWOOD, Flowering Plants of the World

  Perfectly reasonable scientists, who pride themselves on their caution when dealing with their own specialty, indulge on the wildest flights of fancy when it comes to cracking the mystery of the Cretaceous killer.