Planet of the Bugs: Evolution and the Rise of Insects

by Scott Richard Shaw

  Bursting the Balloon: Deflating Our Vertebrate Egos

  Recently I came across an issue of National Geographic magazine from May 1999. On the cover was a list of articles, including the following: “The Rise of Life on Earth.” I thought this title was clear enough, so I turned to page 114, fully expecting an excellent story about the evolution of bacterial life over 3 billion years during the Precambrian. Imagine my surprise when I found the full title: “The Rise of Life on Earth, from Fins to Feet.” It was an article about the emergence of the first amphibians, some 365 million years ago. They were the first vertebrates to take a stroll1 through the mud, so I suppose that we shouldn’t be surprised. After all, we vertebrates are telling the stories. But there you have it. Here we are, at the start of the twenty-first century, and we continue to reflect on the ages of Paleozoic time in terms of degree of vertebrate development. Even in our enlightened times, life is sometimes equated with animal life, animals with vertebrates, and earth with dry land.

  Sometimes the “age of fishes” is extended from the Ordovician into the Devonian, when fishes diversified greatly. Sometimes the “age of amphibians” is extended from the Devonian, when amphibians first poked out of the water, into the Carboniferous times, when they radiated significantly in the ancient coal swamps. It doesn’t matter whether we call the Devonian period the “age of fishes” or the “age of first amphibians.” Either way, it’s a human-centrist bias that seeks to place our vertebrate ancestors in some kind of elevated position. Nothing could be further from the truth. During the Devonian, as in all periods since the Cambrian, the diversity of arthropod species greatly outnumbered that of vertebrate species, whether it was in the oceans or in the emerging terrestrial ecosystems. The terrestrial arthropod communities didn’t need the amphibians to crawl out of the water. On the contrary, the early amphibians needed the land arthropods for their survival and success. Large amphibians may well have fed on fish, and perhaps on each other, but immature and small amphibians, then as now, would certainly have depended upon small arthropods, such as abundant millipedes in the mossy shorelines, as an important food source.

  Because amphibians were capable of feeding on arthropods doesn’t mean that they somehow dominated over the arthropod communities. Plenty of already well-established predatory arthropods were perfectly capable of feeding on the amphibians. Small amphibian species, developing young amphibians, and amphibian eggs were all easy targets for aquatic and semiaquatic scorpions. In the mossy shoreline communities there were not only scorpions, but also large venomous centipedes, and now, newly emerging predatory arthropods resembling primitive spiders. The mossy Devonian shorelines were no Garden of Eden for the first amphibians, and once again we should feel very grateful, this time because by some stroke of luck, the Devonian scorpions and centipedes didn’t manage to hunt the first amphibians to extinction.

  If we could travel back in time and stroll along the Devonian beaches, I don’t think I could resist picking up a pocketful of broken corals from the shore. I’m sure that any avid readers of science fiction will tell me this isn’t wise, but if I were to see any lungfish or amphibians peeking out of the water, I wouldn’t be able to resist tossing some chunks of coral that way, each with a “sploosh,” until they went away. Let’s take a moment to close our eyes and imagine that scene. Let’s toss some broken pieces of coral at those pesky amphibians, and scare all the lungfish back into the water. I don’t want them interfering with the rest of this tale.

  Into the Woods

  The other lead story of the Devonian was the developing land plant communities. Recall that the first land plants did not have extensive root systems and that they needed a very moist environment to reproduce. So, the Devonian “land” plant communities rose up along the shorelines, in marshes and estuaries, along lakes and rivers, and other low areas that retained water, soil fungi, and sediments. Inland and upslope, most of the continental landscapes remained rocky, dry, sun-baked, windswept, and barren of life except in microbial soils.

  We can learn a lot about the Devonian plant communities by looking at a few kinds of plant fossils from the time. The state fossil of Maine, Pertica quadrifaria (an Early Devonian land plant), provides a nice place to start. This is a rare and distinctive state fossil, compared to others that we’ve discussed so far. About 390 million years ago, a volcano erupted, creating a shower of ash that buried a sizeable aggregation of Pertica plants. A sample of the Pertica “forest” was fossilized in the layers of volcanic ash and has since been rediscovered in the Trout Valley near Mount Katahdin, Maine. The Pertica plants of Maine in several ways resemble upscaled versions of their Late Silurian counterparts, the first vascular plants, Cooksonia. Like Cooksonia, the Pertica plants lacked leaves, flowers, and deep roots. But they branched more extensively and grew much taller. They were giants of the times, rising to heights of nine feet or more, and unlike modern plants, they didn’t have any leaves or flowers, just a lot of forked branches and stems. Photosynthesis took place in the exposed green cells of the upper stems’ outer layers, and the tips of the upper stems ended in reproductive sporangia. The main strategy of these early plant communities seems to be branching higher to expose more cells to the sun and placing the reproductive parts higher for better wind dispersal. It makes perfect sense that photosynthesizing organisms would evolve to become taller.

  Since plants without anchors would easily be blown over in storms, it should come as no surprise that the next round of plant innovations included the evolution of root systems. The Gilboa Fossil Forest of eastern New York provides some insights regarding mid-Devonian plants. The Gilboa shorelines comprised a complex plant community, complete with low plants covering the ground, small shrubby plants, and small- to medium-sized treelike plants that were fifteen to twenty-five feet tall, with leaves, bark, and roots. Still, the Gilboa vegetation was simple in a couple of ways. The plants had shallow root systems, restricting them to growth in marshlands near water. Also, their leaf arrangements were thinly scattered, producing not a dense forest but an open, sunny area. Finally, their sparse leaf structure suggests that production of leaf litter was minimal, so organic material accumulated more gradually than in subsequent forests.

  By the Late Devonian, forests of tall trees had developed. Perhaps the best known are those of tropical Archaeopteris trees, which were found on all continents, rose to heights of fifty to sixty feet, and had dense thickets of leaves, creating forests of deep shade and thick leaf litter accumulation. They also had deep penetrating roots, so they were able to spread widely over the Devonian tropical lowlands. By the end of the period, a true forest biome had evolved.

  On hearing the story I’ve just described, it’s easy to imagine that plants quickly conquered the land. Maybe you visualize mysterious but majestic trees severing the rocks with their roots and triumphantly marching inland. That’s not exactly the case. Keep in mind that the transition of plant communities just described occurred over the entire Devonian, a period of more than sixty million years. It’s also important to realize that the advancing plant communities didn’t just reach out with their roots and crush the rocks. They needed a substrate of microbial soils, which were created not just by plants building organic matter through photosynthesis, but also by the mycorrhizal fungi that grew in close association with vascular land plant roots, thereby increasing the plants’ ability to absorb nutrients from the soil, as well as by micro-arthropod conditioning of the soils. These mycorrhizal fungi broke down organic materials and rendered them into forms suitable for plant rootlet absorption. The complex communities of small soil-dwelling arthropods like millipedes fed on the fungi and decaying organic materials, breaking down decaying plant matter, aerating the soils, and moving nutrients by excavating pathways through the soil layers. Other animals, such as soft-bodied annelid worms, moved into the developing substrates, but the arthropods were crucial to the initial processes of creating those soils. In the shade of the first trees, under blankets of the first
leaf litter, in complex microbial soils teeming with life, a drama was playing out—and the very first insects were evolving.

  Adam Ant?

  One of the classic questions in biology is “Why are there no insects in the oceans?” At first glance it does seem puzzling that the most diverse group of land-dominant organisms should be virtually absent there. Many insects have colonized freshwater habitats, and some, such as the brine flies, have extreme degrees of salt tolerance. Only a few insects, such as water striders, have colonized the open seas. But there are no insects in coral reef ecosystems, or other ocean areas, except on the surface or seashore margins. Why? We are so conditioned to thinking about life having evolved in the oceans that we tend to forget that some important animal groups—like the insects—evolved later, on the land. By the time the insects evolved, the niches of marine ecosystems were already filled by other organisms. Various mass extinctions decimated marine communities, but never so completely that the surviving marine organisms couldn’t recolonize before the insects could adapt to enter the system. Insects didn’t need to move into the already highly competitive ocean environment. They succeeded simply by being the first to colonize each new and unoccupied terrestrial niche.

  How did the very first soil-dwelling insects evolve? Full of bacteria, fungi, and arthropod consumers, the Devonian soil microhabitat was not very conducive to fossilization. There are some very important Devonian fossils, which I’ll get to in a bit, but for now, let’s start by examining living insect species and comparing their anatomy to extinct ones. All insects, whether living or extinct, share a common body form. Through the process of tagmosis, primitive body segments were fused into three distinct body regions, or tagma: the head, the thorax, and the abdomen. An insect head contains the brain to coordinate sensory input, compound eyes for vision as well as simple eyes for detecting light and monitoring changes in day length, a pair of antennae that serve as feelers but allow chemical detection and a sense of smell, and the mouthparts. The insect mouthparts are formed from four primitive leg-bearing segments and are modified enormously across various insect groups for a diversity of feeding functions. The most ancient insects had chewing mandibulate mouthparts, not too different from that of the scavenging myriapods.

  The middle part of the insect body, the thorax, is composed of three segments modified for locomotion. All insects have six thoracic legs: one pair located on each thoracic segment. The wings of modern insects are also located here. Remember that the first insects didn’t have wings yet. That innovation came later, in the Carboniferous. The specialization of the insect thorax for locomotion requires that it be packed full of muscles. This is especially true for the winged insects, which require even more muscles for flying. Consequently, there is not so much room left inside that area, so most of the other organ systems are packed into the posterior.

  The third insect body region is the posterior multisegmented abdomen. Externally, it doesn’t look like much, but internally it is very complex and important. Functional parts of the digestive, excretory, circulatory, respiratory, reproductive, and nervous systems are located there. The heart valves are in the insect’s abdomen, and segmentation allows for contractions that increase blood pressure throughout the body. Most of the breathing holes, called spiracles, are located along the sides of the abdomen, whose contractions force air through the tracheal system. This is particularly important when insects molt, as it allows them to pump up their new body form by inflating with air. The systems of the abdomen, including the reproductive organs, are controlled by regional nerve bundles, so even a severed insect abdomen is sometimes able to survive long enough to reproduce. The insects’ external genitalia are thought to have evolved from primitive leg parts.

  Two Legs Bad, Six Legs Good

  Six-legged anatomy evolved during the Devonian, and insects have stuck with that plan ever since: all of the tens of millions of modern insect species are hexapods.2 Some minor exceptions can be noted. An insect can lose a leg or two in an accident but still walk. Some insects walk on only four legs; the front legs of brush-footed butterflies, for example, have been reduced to nonfunctional, brushlike structures, and they stand and walk on the back four legs. But they spend most of their time flying. Praying mantises’ front legs are modified for grasping prey and they walk on the back four, but they are ambush-predators and don’t need to walk or run very fast. Other insects, mostly immature forms like maggots, have lost their legs entirely; however, they live in their food, don’t need to move much, and eventually develop into adults with six legs. Some adult insects that don’t move at all, like scale insects, have lost their legs entirely. Many immature insects, like caterpillars, have evolved additional abdominal “prolegs,” which they use to hold tight to their food plants, but they still have the six thoracic legs. Also, no insects walk in a bipedal fashion, as we do, unless you count the brief moment when a jumping insect, like a grasshopper or cricket, stands on two legs as it launches itself in the air. The only bipedal insects are perhaps the fictional ones in animated movies. Cartoonists have humanized these creatures by giving them numerous people traits, bipedal posture being one of the more obvious. I once made a list of the traits of some of the characters from the movie A Bug’s Life and discovered that some of them have more human qualities than they have insect features.

  The fact that there really are no bipedal insects may reveal something important about the reasons for six-legged locomotion. At a fundamental level, it’s about balance and stability. I once saw a diaper commercial with a baby falling on his butt, pleasantly cushioned by a fat diaper. The narrator said, “You have to fall about two hundred times before you learn to walk.” I’m not sure if there are any data to back that up, but the commercial made a good point: bipedal locomotion is inherently unstable and such balance is not easy to learn. A six-legged insect nymph, however, upon hatching from its egg, is able to walk and run almost immediately. But the six-legged form is not just better for balance; it seems that it may be optimal. Everyone knows how inherently stable a tripod is; insects walk essentially by replacing one tripod with another, moving three legs while keeping the other three planted.3 The six-legged form is also good for running. Just look at some of the more common groups of primitive insects, like silverfish, bristletails, and cockroaches. They are all very fast on their feet, compared with your average millipede, which needs to coordinate motion across hundreds of legs.

  So the process of evolving six-legged bodies seems to be a question of optimizing balance and stability with the potential for rapid motion. Two-legged bipedal locomotion is so unstable and difficult to master that it seems highly improbable and almost pointless. Insects have had 360 million years to experiment with legs, but none has bothered to acquire bipedal form, or four-legged form for that matter, which is stable enough but has less potential for speed. The four-legged tetrapods were all sluggish and slow until they developed warm-blooded metabolism. Six-legged form is sublime. Fifty million insect species can’t possibly have it wrong. Eight-legged form isn’t so bad either. Just take a look at spiders, which make up thousands of species. But all in all, there doesn’t seem to be any real advantage to having eight legs; they’re nearly as good as six. And so on with ten legs, or twelve legs, or more. More legs just complicate the issue of coordinating movements, providing no real advantage in speed or stability. Plus, remember the trilobites’ downfall. Having more segments and appendages complicates the arthropods’ molting process.

  It’s tempting to think that tagmosis was the driving factor in the evolution of six legs. It seems likely that as with the trilobites, the hexapods would be more successful in part because having fewer segments and appendages would simplify molting. No doubt mastering the molting process and developing a simple body form were key factors in early insects’ success, but it can’t be as simple as that. Indeed, some myriapods mastered the molting process despite the difficulties of having numerous appendages. Just consider the millipedes’ long-term success
. They can have hundreds of legs, but they have survived for hundreds of millions of years. Some of the centipedes are fast on their feet as well. So although improving molting efficiency by reducing the number of body segments and legs could be an important factor in the origin of insect form, it can’t be the only one. It’s also important to consider that the evolution of six-legged form and speed was accompanied by the simultaneous evolution of very small body size. Some of the ancient Silurian and Devonian myriapods were quite large (some millipedes were up to fifty centimeters long). The most ancient hexapods, in contrast, were only a few millimeters long. Over the Devonian, arthropod body sizes underwent very serious downsizing.

  The reasons for this trend in reduced arthropod waistlines should be clear enough. The ancient myriapods faced some very serious predators: scorpions, centipedes, and spiders. Natural selection by such macro-arthropod predators would select for smaller arthropods and faster arthropods with fewer legs, since predators tend to hunt preferentially for larger prey, selecting them out of the environment. But being very small has several other advantages. It allowed insects to get deep down into the moss and right into the soil, into moist environments where they could hide and more safely complete their molts. Moreover, small body size also provides a breathing advantage. Smaller animals have more surface area relative to the volume of cells in the body. Therefore the very smallest insects can breathe directly through the cuticle, because they are so small and live in a very moist environment where a thick skeleton is no longer needed. But the ultimate advantage to microscopic body size is that fewer resources are needed for survival. Small animals can grow and reproduce more rapidly than large animals; therefore, they evolve faster, and they can occupy much smaller ecological niches.