Planet of the Bugs: Evolution and the Rise of Insects (15 page)

Classic Fashions Never Go Out of Style

The most ancient wing style—a flat panel of skeletal material set into a membranous area at the top side of the thorax—was very simple but highly efficient, and some modern insects such as mayflies and dragonflies still sport it. The middle of the wing balances on a fulcrum formed from the pleuron. The wing itself acts as a lever, snapping up or down, because it is stable only in the most raised and the most lowered positions. Its upstroke is accomplished indirectly by muscles that connect the thorax’s top and bottom walls but do not attach to the wing. When these dorsoventral flight muscles contract, the thorax is flattened and distorted, causing the wing to snap into an upright position. In the paleopteran insects, the downstroke is accomplished by muscles connected to small plates below the wing, just near the front and back. These are sometimes called direct flight muscles, because they connect directly to the wing. They not only power a downstroke, but by differential contractions they can allow the wing to be tilted at different angles during flight, allowing directed navigation.

Although the mayflies and dragonflies are the only surviving insects with this ancient flight mechanism, when it first evolved it was the latest and greatest innovation in animal locomotion. Without any competition from birds, bats, or flying dinosaurs, the old-wing insects took to the air in prolific numbers, and by the Late Carboniferous, the earth’s wet tropical forests were populated by a startling array of flying insect species, almost all of which are now extinct. One of the most notable examples is the order Paleodictyoptera, the old net-winged insects. As the name implies, these insects had a netlike profusion of veins along their old-style wings, which they held out to their sides and were incapable of folding back over their body. But the old net
wings conquered the air more profusely than most other insects of the time. Over the Late Carboniferous and continuing through the Permian years there arose a dynasty of paleodictyopteran insects that diversified into at least seventy-one genera, classified into twenty-one families. Some of these species were quite enormous, the largest being about fifty-six centimeters in wingspan (about twenty inches across). They were positively gigantic compared to ancestral flightless insects, clearly indicating that the old net wings had successfully managed to escape the earthbound predators on the forest floor and specialize in tree dwelling, making them some of the first arboreal insects. In the future, most insect species would evolve to live in rain forest canopies.

Part of the old net wings’ success stemmed from their invention of a unique mouthpart style. The oldest known true herbivorous species, they were the first flying insects to evolve piercing and sucking mouthparts (beaks) capable of liquid feeding and tapping into the more nutritious plant parts in ways that no other animal group had done before. Species with long beaks and their nymphs could feed on plant tissues and fluids by piercing soft foliage or tapping directly into xylem and phloem. Other paleodictyopteran species with shorter, broader beaks fed by piercing the developing reproductive cones of ancient plants, and sucking out the liquid, spores, and ovules.

We know that the old net-winged insects fed on various plants, including pteridosperms, cordaitealeans, lycopods, and conifers, because we’ve found fossilized Paleodictyoptera with spores and pollen in their mouthparts and guts. We’ve also found fossil plant remains that show piercing-and-sucking feeding damage, no doubt paleodictyopteran handiwork. They were the only insects around with the right kind of equipment able to make those marks.
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The first plant galls, fossils of deformed plant growth of the kind usually caused by arthropod feeding, also date to the Late Carboniferous. We can’t be sure what insects made these galls—they could have been formed by mites—but they’re possibly the first evidence of insects concealing themselves while feeding inside plants. We also have fossil coprolites, literally fossil insect poop, which contains plant spores.
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Many of the paleodictyopteran insects had pigmented patterns on their wings. These species are preserved in detail in some fine sedimentary compression fossils, and although we don’t know the colors of the wings, we do know that they often had boldly contrasting
stripes or spots. What might these markings mean? The most likely explanation is that they provided visual cues for mate recognition, just as in modern dragonflies, grasshoppers, and butterflies. But insects evolve colors for several reasons. It’s possible that some of their pigments might have been cryptic. It’s difficult to know what sorts of leaf markings or color tones might have been prevalent in the foliage of Carboniferous rain forest canopies, but if paleodictyopteran wings were blends of greens, tans, and yellows, the insects may have been highly camouflaged when resting on tree trunks or in foliage. They may well have escaped entirely from the amphibians on the ground, but they may still have had to contend with the tree-climbing scorpions, spiders, and centipedes. Another possibility is aposematic warning coloration. Many modern insects gain toxic defenses by feeding on toxic plants and develop warning colors in their wings to advertise this to predators. Without any birds, this seems less likely to develop, but paleodictyopterans may still have faced an occasional amphibian on low vegetation, tree trunks, or mossy branches. So there might have been selection pressure to develop bright warning colors, even then.
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Another possibility is storage excretion metabolism: some insects shunt nitrogen wastes out of their body tissues by packing them into wing pigments (yellow butterflies are the best-known example). Paleodictyopterans might well have had bright yellow or orange colors in their wings, even in the absence of plant toxins or vertebrate predators. The point I wish to make is simply this: the Carboniferous world had pattern, color, and beauty. The orthodox reconstructions of that ancient period overlook this. I’ve seen several museum panoramas of coal-age swamps, and they always depict a cloudy, drab, green and brown world, usually with a spider, giant dragonfly, and maybe a roach. They never show you the paleodictyopteran insects. I prefer to think that above those swamps flew a shimmering fairyland of multicolored insects, many of which we would certainly consider to be beautiful.

FIGURE 5.2. Fossilized paranotal lobes and patterned front wings of an extinct upper Carboniferous paleopteran insect
Homoioptera gigantea
(order Paleodictyoptera). (Photo by Olivier Bethoux. © MNHN–Olivier Bethoux.)

My, What Big Wings You Have

The old net-winged insects may have succeeded magnificently by escaping most of the terrestrial predators in the forest understory, but they still had to contend with airborne insect predators, such as the
so-called giant dragonflies, or griffenflies, of the now-extinct insect order Protodonata. Among the most spectacular animals of the Late Carboniferous years, the griffenflies were not really true dragonflies but rather a group that resembled them. Members of one of the griffenfly families—of the tropical family Meganeuridae—are the largest insects that ever lived. During the Permian times,
Meganeuropsis permiana
developed wingspans of seventy-one centimeters (between two and three feet wide), while most other meganeurid species typically had wings four to thirteen inches long. These dragons of the air had sharp, powerful mandibles and spiny front legs for grasping prey. They may not have been really fast or adept fliers, but they were easily able to grab fluttering paleodictyopterans, swarming mayflies, and other flying insects out of the air. They probably also picked off paleodictyopteran nymphs and adults feeding on prominent canopy stems. In the absence of birds, bats, pterosaurs and other flying vertebrates, these Paleozoic giant griffenflies were the dominant predators of the skies, and they were likely the main source of predatory selection pressure shaping the evolution of wing patterns and colors in Carboniferous and Permian insects.

Some researchers have pointed out that the appearance of gigantic flying insects correlates with peaking atmospheric oxygen. Levels had remained around 15 percent from the Cambrian to the Devonian, rising significantly to around 35 percent in the Late Carboniferous. Then they dropped back to about 15 percent by the end of the Permian. Since the times of highest oxygen do correspond to the era of giant flying insects, it is tempting to relate the two. Scientists have suggested that such large insects needed heightened levels to operate their huge flight muscles, and there is some evidence that they had enlarged tracheal systems. Carbon dioxide was also elevated at the start of the Carboniferous but dropped dramatically over the Permian years to nearly modern levels. So it’s also been suggested that the air was thicker and more viscous then, making flight somewhat easier.

These physiological arguments may have some problems. They assume that since oxygen reaches insect cells by diffusing from their tracheal network, a respiratory constraint is placed on the insects’ upper size limit. But it’s important to note that insects can force air through their tracheal system and pump it to cells deep in their body, by contracting their abdominal segments. Also, we don’t know what the giant
griffenflies’ metabolic requirements really were. They were the top predators, and nothing else was chasing them. Prey like mayflies and paleodictyopterans probably fluttered along slowly, so there is no reason to assume that the giant meganeurids flew very fast. If they had a slow, lazy flight pattern, they may have required less oxygen than some large modern insects, like hawk moths. Another thing to consider is that modern dragonflies are very lightweight, and the giant meganeurids probably were as well. Most of a dragonfly’s body is very slender, and it has lots of gas-filled tracheae, which helps a dragonfly to both float on water while laying eggs and to fly more easily. Moreover, there are no modern insects quite so large in wingspan, but there are some massive ones. The heaviest adult insect, the goliath beetle of Africa, can weigh up to a hundred grams. Its thorax is thicker than that of a giant dragonfly, and one of these beetles probably weighs as
much or more than a meganeurid air dragon. And goliath beetles can fly just fine, even with the modern atmospheric oxygen level of around 21 percent.

FIGURE 5.3. A gigantic fossil wing of
Meganeuropsis permiana
(order Protodonata) from lower Permian rocks found in Oklahoma, about 280 million years old. The length of this wing is about thirteen inches. (Photo by Frank Carpenter. Museum of Comparative Zoology, Harvard University. © President and Fellows of Harvard College.)

Oxygen might have been a factor spurring the evolution of the air dragons’ large size, but it probably wasn’t the only one. It’s important to remember that insects develop by periodically molting their external skeleton. So for any insect to grow as large as a griffenfly, it would need to go through a series of progressive molts, and during each one it would be extremely vulnerable to predators. The growth of any giant insect therefore requires that the young live in a largely predator-free environment. Where, then, did young giant griffenflies grow up? We suspect that the immature forms were freshwater aquatic nymphs that breathed with gills (like those of modern dragonflies) and were predators who fed in marshes and ponds,
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where they would have found abundant food in the form of mayfly nymphs or insects that fell on the surface. Like modern dragonfly nymphs, they probably also fed on fish and amphibian eggs, small fish, and amphibian tadpoles. Consider the situation in the Carboniferous years: jawless freshwater fish were spreading to inland lakes and ponds, but the air dragons held the advantage. Because they could fly, the females were able to move inland more easily than fish and occupy temporary ponds and marshes that the fish could not as easily colonize. Griffenflies could also fly inland to unoccupied ponds, ahead of the fish, which, when they finally did arrive, would be attempting to lay eggs in ponds already full of vicious meganeurid nymphs. The large nymphs of many modern dragonflies are able to cover themselves in sediment and debris, and maybe the meganeurids could don similar disguises. Perhaps, as they grew ever larger, they burrowed into soft bottom sediments to complete their molts. If they lived in ponds, the liquid environment would have facilitated their multiple transitions. They would have emerged only to finally molt into fully-winged adults; then they could fly to the comparative safety of the forest canopy, where their main enemies might have been each other.