Planet of the Bugs: Evolution and the Rise of Insects

by Scott Richard Shaw

  ROBERT T. BAKKER, The Dinosaur Heresies

  The king is gone, but he’s not forgotten.

  NEIL YOUNG, “My My, Hey Hey”

  As I write these lines it is a frigid February in Wyoming. The landscape is about as cold and barren as can possibly be, and yet I am thinking of flowers. Valentine’s Day will not let me forget them. The television networks, radio stations, newspapers, and Internet all remind us to buy flowers for the ones we love, and for a few short days, in the bleakest of winter, the stores are saturated with bundles of roses and a lush variety of other blossoms in dozens of colors.

  Unless we have allergies, flowers generally make us feel good. We plant them in our yards and gardens around our homes and workplaces. We culture them in small containers and bring them indoors. We like their riotous colors and the extravagant forms of their petals, and so we create floral art, drapery, and wallpaper; grace our fabrics with floral images; and swaddle ourselves in flowery clothing and jewelry. Sometimes we even tattoo flowers onto ourselves. We especially like their smell. We harvest or duplicate their scents for aromatherapy and incorporate them into perfumes, soaps, oils, lotions, shampoos, deodorants, and candles.

  Perhaps our attraction to flowers might be another example of the phenomenon that Edward O. Wilson has termed biophilia, the innate love that humans have for nature and for other living things. Because we have evolved over millions of years in nature, maybe we possess a genetically programmed yearning to surround ourselves with its more pleasant aspects—flowers being one of its best-loved items. But we seem to like flowers more than we do other living creatures. We certainly don’t feel quite the same way about fungi, salamanders, frogs, spiders, or snakes, all of which can be colorful and interesting to look at. Some stink bugs have very pleasant odors, nicer indeed than some flowers, but we don’t give them to our wives or girlfriends on Valentine’s Day. Perhaps at a very basic level flowers attract us with the same characteristics that lure insects to them. Their vivid colors and curious shapes allow us to spot them from a long distance, just like a bee. At close range we react positively to their odors and sweet nectars, just like a butterfly. Flowers, bees, and butterflies are so commonplace today, it is easy to forget that the earth was not always filled with them.

  Rift, Shift, and Dinosaurs Adrift

  We tend to hear more about the Cretaceous’s catastrophic finale and not much about its long years. The period ended spectacularly with the colossal asteroid impact that (presumably) extinguished the Tyrannosaurus rex and its kind, and that (finally) allowed mammals to emerge from the carnivorous dinosaurs’ long shadow. We will hear more about that later, but for now let’s focus on what things were like during the Cretaceous, which lasted about seventy-nine million years—a long time, even by cosmological standards.

  With the end of the Jurassic and the onset of the Early Cretaceous, about 130 to 145 million years ago, the composition of this planet’s big animal communities noticeably changed. The Apatosaurus, Diplodocus, and their relatives faded to extinction, and the Cretaceous forests became filled with new communities of large herbivores, most notably the duck-billed hadrosaurs and the horned and frilled Triceratops and its multipronged relatives. Meanwhile, the southern supercontinent of Gondwana was violently fragmented, wrenching apart startled dinosaur herds. The land mass now known to us as South America began to split away from what is now Africa. With each massive earthquake, rifts formed from the south and north and ocean water rushed in, until eventually these areas were completely separated by a water gap and a narrow, infant South Atlantic Ocean was formed. The South Atlantic sea floor has continued to grow and widen since then, gradually but relentlessly pushing South America and Africa further and further apart, but it was in the Early Cretaceous that South America became a large island continent, at first just narrowly separated from Africa and already widely separated from North America (the Central American land bridge did not join South and North America together until just a few million years ago).

  If we were to view the Cretaceous continents from outer space, we could recognize at least the shapes of modern areas like South America, Africa, India, Antarctica, and Australia, but their positions were stunningly different than they are today. South America and Africa were separated by a narrow waterway that resembled a winding channel rather than a modern ocean; Antarctica was located further to the north, much closer to South America and Africa; and Australia, tilted on its side, was still very close to Antarctica, divided by only a thin gap. In the Early Cretaceous these southern continents had mild climates, and animals and plants were dispersed along the southern corridor from South America, across the northern coast of Antarctica, to Australia in the east. South America was not the Cretaceous’s only distinct island continent. The subcontinent of India had already fragmented from the eastern coast of Africa, and over the period a fully isolated India drifted north and east across what we now call the Indian Ocean.

  Although the shapes of Cretaceous India and South America might have looked familiar, their terrains would have been unrecognizable. Most notably, they were relatively flat; the modern mountain ranges that we know as the Andes and the Himalayas had not yet formed.1 Moreover, in the Early Cretaceous the Amazon and Ganges rivers did not exist. More ancient rivers drained across the lowland forests as duck-billed dinosaurs browsed in the misty twilight. Yet as strange as this scene might seem to us now, it also had a growing familiarity: in the Cretaceous forests the flowering plants first evolved and rapidly proliferated, and myriad flower-associated insect communities developed.

  Dance of the Sugar Plum Fairies: The Coevolution of Insects and Flowers

  The flowering plants, the blossom and fruit-producing organisms known to botanists as angiosperms, may have first evolved in the Jurassic period or earlier, but they were initially rare woody shrubs restricted to wet forest habitats. We have fossil flower pollen dating to the Early Cretaceous, 134 million years ago, and fossil leaves and flowers dating to 124 million years ago, and we know that by 120 million years ago the first angiosperms, including such recognizable species as water lilies and magnolias, quickly radiated and diversified. By the Middle Cretaceous (and on to the present day) angiosperms had become the dominant plant species.

  The early angiosperms’ method of reproduction is similar to that of the Carboniferous Gnetales, which predated the flowering plants by at least 160 million years and resembled the coniferous cycads, primitive seed plants with stout woody trunks, topped by crowns of stiff evergreen leaves, that had dominated the dinosaur-ridden forests since the Triassic. The Gnetales used pollen to reproduce and had two forms: some had pollen-producing structures and others pollen-collecting structures.2 Their female reproductive parts don’t look like anything we would call a flower, but they function in the same way—so although the gnetaleans are not classified as angiosperms, they might reasonably be considered the most ancient flowers. More importantly, it appears that the gnetaleans were insect-pollinated. Modern species, such as Ephedra antisyphilitica, are known to produce sticky droplets of pollination fluid at the tip of their flowering structure. This fluid grabs microscopic pollen grains but also attracts insect visitors with its sweetness.

  Sweet nectar and nutritious pollen allowed flowers—and insects—to overrun the planet. Plants produce them in sacrificial abundance, enough to feed ravenous hordes of flies, beetles, wasps, and moths, all of whom, in turn, scatter the protein-packed pollen that sticks to their hairs. The nutritional benefit to the insects is obvious, but how did the plants profit from this mutualism? Plants are rooted in place; they cannot get up and trot away in search of mates. Until the Cretaceous, their distribution was limited mostly by the constraints of wind pollination. But with the insects’ assistance—and thanks to the energetics of insect flight—plants at this time could spread their genetic material over long distances. Now they could exist as widely dispersed populations, scattered in forests with little wind movement.

  The benefit of pollination sy
stems to both plants and insects is clearly imprinted in the fossil record since the Middle Cretaceous. Fossils from this time are rich not just with diverse, new flowering plant species but with new species of flower-associated insects. Of particular note is the appearance and diversification of new flies with long, hollow, tubelike mouths modified for dipping into and sucking nectar from deep inside flowers. These long-beaked flies—the early bee flies, flower-loving flies, and tangle-winged flies (families Bombyliidae, Mydidae, and Nemestrinidae, respectively)—are among the earliest of the highly specialized flower-feeding insects. Moreover, by looking at remnant living Gnetales species such as Ephydra, as well as still-living primitive flowering plants like water lilies and magnolias, we can see that these ancient kinds of flowers achieved their success by attracting communities of assorted generalized insects—all with a taste for flowers. Close codependencies, like those between orchids and certain bee species, are the result of coevolution over the past hundred million years or more.

  The key groups of plant-eating insects—stick insects, katydids, plant bugs, leafhoppers, thrips, beetles, sawflies, flies, and moths—were already in place before the Cretaceous began. All enjoyed intense bursts of speciation that paralleled the plants’ rapid diversification. But of all these evolutionary explosions, none can rival the rise of the moths and butterflies during the Late Cretaceous. No other animal group since has more successfully colonized the flowering plants. What propelled them to evolutionary greatness was the feeding habits of their immature larval stages—caterpillars.

  Lepidoptera Domine

  Like the flowering plants they chew upon, leaf-feeding caterpillars are so common that it is hard to imagine earth without them. These externally feeding insects burst upon the Cretaceous scene only a mere ninety million years ago, along with the flowering plants’ early radiation. They evolved from more ancient, microscopic larvae that tunneled their way through plant tissues, which protected these larvae from predators, wind, and the sun’s drying effects. External-feeding caterpillars coped with their harsher environment by evolving thicker cuticles to prevent water loss, but a more serious challenge of life on the outside was simply staying on the plant. Unlike a leaf-tunneling insect, a caterpillar needs to cope with motion. Plants may not get up and run around like animals, but their leaves frequently rustle in the wind and their branches often sway in storms. Holding onto the plant is really crucial. If a caterpillar falls off, it will likely die before it can find the plant again, or it will waste great amounts of energy trying to regain its former position.

  The Lepidoptera in particular had a wonderful preadaptation for success in the outer world: silk.3 While most of us will recall the value of silk cocoons in protecting the transforming moth pupa, we tend to forget the importance of this material to the feeding caterpillar, for which it is a matter of utmost survival. That silk strand is literally a lifeline in the exposed world. As a caterpillar moves about a plant, it is constantly spinning a sticky silk thread, which adheres to the surface. If a caterpillar falls, it will release more silk, with which it can safely descend to another part of the plant, or up which it can return to its starting point. Upon the tips of its abdominal legs are microscopic spines and hooks, called crochets, which grab onto the silk threads while it walks, and keep the caterpillar firmly attached to the plant, even on windy days. The original inventors—and the most successful users—of Velcro, caterpillars also tie together leafs with silk and employ the bundles as feeding shelters to avoid the harsher outer environment and hide from predators and parasitoids.

  As the Cretaceous progressed, moth caterpillars and the very first butterflies became increasingly efficient at chewing on plant parts. If there was an edible portion, it seems that caterpillars managed to find it. They eat leaves whole, scrape leaf surfaces, and skeletonize leaf veins, and they also eat buds, flowers, fruits, seeds, stems, and even roots. All of this nibbling and crunching may sound like a total catastrophe for the early flowering plants, but they did not take the assault lightly. As insect feeding increased, the plants responded by evolving more efficient defenses. Some developed thicker cuticles or microscopic spines that are difficult to digest, others thick or gummy saps that bind to insect mouthparts and are impossible to chew. Many other plants evolved chemical defenses that make their leaves bitter, or even toxic.4 More than a hundred thousand such defensive compounds have been recognized so far, and new ones are constantly being discovered with the exploration of tropical plants. They seem to rival the diversity of the plant-feeding insect armies and include tannins, alkaloids, cyanogenic glycosides, coumarins, flavonoids, steroids, and terpenoids, to name only a few. While these names may seem foreign, the alkaloid compounds, for instance, include caffeine, nicotine, morphine, atropine, cocaine, strychnine, quinine, and curare. When we sip coffee or smoke a cigar, how many of us pause to reflect on the hundred million years of insect–plant coevolution that made these things possible?

  FIGURE 9. 1. This well-preserved fossil butterfly, Prodryas persephone (order Lepidoptera, family Nymphalidae), is from Eocene-age rocks of Florissant, Colorado, estimated to be at least thirty-four million years old. Butterflies first evolved during the Cretaceous but survived the end-Cretaceous extinctions to become important herbivores in the modern world. (Photo by Frank Carpenter. Museum of Comparative Zoology, Harvard University. © President and Fellows of Harvard College.)

  The angiosperms’ chemical arsenals did not doom the plant-feeding insects. If anything, they stimulated the evolution of even more creative feeding strategies. If an angiosperm evolves a totally new defensive chemical, this may prevent many generalist herbivores from continuing to eat that particular species. But there are always bound to be a few specialist insects that, because of their unique abilities, discover ways to keep eating the plant. Some insects simply avoid the chemicals. For example, a chewing insect might cut the large leaf veins, thus preventing defensive compounds from flowing into the area where it is feeding, or it might feed selectively on new growth with fewer toxins. Or an insect with piercing mouthparts might feed selectively by puncturing areas of the plant which lack the chemicals. Many insects evolve mechanisms for detoxifying plant poisons or, even better, find ways to incorporate them into their own body’s metabolism—thereby turning plant chemicals into their own defense against predators.

  Attack of the Bee Girls

  The Cretaceous surge of flowering plants and their associated insects also stimulated a parallel explosion of parasitic and predatory groups, since every new insect species that evolved to exploit a flowering plant was itself potential food for insect-eating species. The stinging wasps (Aculeata), for instance, descended from a group of Late Jurassic parasitic wasps that shifted their egg-laying duct from the ovipositor to just above the base of the ovipositor, which was itself modified into a hypodermic syringe used only to inject venoms. This allowed the sting to specialize as a venom-delivery device and ultimately as a purely defensive weapon—a transformation that in the Late Jurassic quickened the conquest of a new wasp group, the nest-provisioning wasps, and in the Cretaceous gave rise to several other new social insect groups: social wasps, bees, and ants.

  Probably not much changed for the Jurassic wasps with the new egg-laying duct. The females continued to sting and paralyze insect hosts and to lay eggs on them. However, once the sting evolved, females no longer had the option of drilling and injecting eggs deep into their hosts. They had to lay their eggs directly on easily exposed insects. But the same exposure that allowed the female wasps to easily find these insects also allowed other predators and parasites to discover them, which is why some females started moving their paralyzed hosts to a more secluded spot. With this move, the first nest-provisioning solitary wasps made their debut in the Late Jurassic.

  More often than not, a female nest-provisioning solitary wasp will dig a hole or tunnel in the ground or find a hollow plant stem. Then she goes hunting. She finds a suitable food item, such as a caterpillar, stings it, and
injects her paralyzing venom, just as her parasitoid wasp ancestors did for millions of years. Next she grasps the paralyzed insect with her mandibles or legs. Maybe she flies away with it, or maybe she just drags it along the ground. In any case, with determination and hard work, she takes that insect back to her nest, stuffs it into the hole, and lays a single egg upon it. Then she deftly seals up the nest entrance, and starts the process over again in another location.

  FIGURE 9.2. A female dryinid wasp (order Hymenoptera, family Dryinidae) fossilized in Dominican amber, estimated to be twenty to thirty million years old, with a visible sting. Modern dryinids are all ectoparasitoids of Homoptera adults or nymphs, which they catch with their chelate forelegs and sting to cause paralysis; then they lay a single egg between the host insect’s overlapping thoracic or abdominal segments. (Photo © George Poinar Jr.)

  As female wasps became better at searching for exposed insects during the Early Cretaceous, they refined their stinger into the supreme hunting tool, and many new nest-provisioning species evolved. As their hunting skills diversified, wasps also grew more creative at making nests. They began to tunnel into wood, hollow out the pithy centers of plant stems, and sculpt nests on vertical rock and cliff faces out of clay or mud. To further hide their nests, some modern wasps close it, fly over it, and scatter sand to erase all traces of the entrance. Other mother wasps pick up a small stone with their jaws and tamp down the soil over the nest entrance. Thus, wasps were the first stone tool users, probably tens of millions of years before any primate or human ever picked up a rock.