Planet of the Bugs: Evolution and the Rise of Insects

by Scott Richard Shaw

  The centipedes are perhaps the most familiar myriapod group. There are more than three thousand species, mostly tropical, and they are active mainly at night. Centipedes have thirty or more legs, two per segment, and they really know how to use them: most can run very quickly. Unlike insects, centipedes do not have a waxy cuticle to prevent water loss. They can dry out rather easily, so they tend to stay in moist habitats near soil and avoid direct sunlight. All centipedes are predators, and they capture small animals with their fanglike front legs, which house venom glands. Most feed on other small arthropods, but some large tropical species, up to ten inches long, are capable of killing small vertebrates. Similar to the predatory scorpions, centipedes were certainly capable of surviving in the rocky intertidal zone and feeding on various other small animals long before plants colonized the land.

  The millipedes, the leggiest arthropods, are called “diplopods” because they have evolved a unique body type: each segment has two pairs of legs rather than one, and contains two pairs of nerve bundles and heart valves. This shows that their segments formed when two primitive segments, each with one pair of legs, fused together. There are more than seventy-five hundred millipede species, and although they live primarily in the tropics, they can be found all around the world.

  Millipedes are a lot nicer than centipedes. If you want a Silurian pet, I’d highly recommend one.1 They are friendly, they do not have venom or bite humans, and these days it’s not too unusual to find some of the giant African species for sale in pet shops. Like the centipedes, however, millipedes prefer to stay out of the sunlight, and so they hide in moss, tunnel in soil or under loose rocks, or live in caves. A few species are known to prey upon other soft-bodied arthropods and worms, but most are scavengers that eat decaying vegetation in addition to fungal or bacterial accumulations. It appears that the millipedes are yet another arthropod group that was perfectly capable of colonizing the beaches well before land plants evolved; these scavengers would have been able to feed on lots of non-plant-based organic material such as decaying green algae mats, fungi, and bacterial blooms in Silurian microbial soils.

  FIGURE 3.3. A white millipede (order Polydesmida) illustrates a unique characteristic of these leggy myriapods: each segment is equipped with four legs. Polydesmids are the largest order of millipedes, with over 2,700 species known. (Photo by Kenji Nishida.)

  The symphylans have escaped the notice of most people, but they are very important to the insects’ story because they most closely resemble the ancestral kind of myriapod from which insects evolved: namely, a short creature with fewer segments than millipedes and centipedes and only two unmodified legs per segment. The symphylans are quite small, only about 2 to 10 millimeters long (less than half an inch). There are about 120 known species, and they mostly inhabit the tropics. Like the millipedes, symphylans live secretively in soil, moss, and decaying vegetation and avoid the sunlight. Modern symphylans feed mainly on decaying vegetation, but like the millipedes, they were capable of living on organic materials in microbial soils before land plants appeared.

  These mysterious dwellers in the mosses have a very unusual method of reproduction. Male symphylans produce spermatophores, which they leave on top of long plant stalks. Females need to wander around and find them. Upon discovering a spermatophore, a female symphylan bites it, but instead of digesting it she stores the sperm cells inside her cheeks in special pouches. When she lays an egg, she reaches around and picks it up with her mouthparts, fertilizes it, and proceeds to glue the fertilized egg to a piece of moss.

  Green Tide: Plants Colonize the Shorelines

  Toward the end of the period, new, taller plants joined the myriapods in transforming the Silurian landscape. Two lines of evidence give us a good idea of what they were like. Preserved fossils from approximately 420-year-old Late Silurian sediments contain the archaic rhyniophyte plants, which are named after an early Devonian genus, Rhynia, discovered in Rhynie, Scotland. The oldest one, Cooksonia, was the very first vascular plant, and it grew only a few inches tall. Very simple and semiaquatic, the rhyniophytes lived along marginal habitats and had parts that could emerge out of the water. They did not have leaves, flowers, or deep roots, and the more advanced early Devonian species were also relatively short—about 50 or 60 centimeters long (mostly less than 2 feet). The rhyniophytes had creeping stems that ran sideways along the shore, probed tiny root hairs below into the soil, and sent shoots upward from multiple points along their top. Each vertical shoot forked once or twice, forming reproductive structures called “sporangia” at the upper tips. The rhyniophytes’ lateral stems allowed them to spread thickly over moist shorelines, since they contained vascular fluid-transporting tissues.

  The second line of evidence comes from plant DNA. Molecular studies support the long-held assumption that land plants evolved from photosynthetic green algae and that the nonvascular plants—liverworts and mosses—evolved first, around the Silurian, followed later by primitive vascular plants, such as ferns. Liverworts and mosses require a lot of moisture to survive and decompose rapidly when they die, so they did not fossilize well; however, we can be sure that the Late Silurian shorelines were full of them, as well as the rhyniophytes and a diversity of soil fungi.2

  If I haven’t said much about plants up to now, it’s because the terrestrial arthropods were able to thrive for millions of years before plants arrived and developed the capacity to survive. Arthropods had the initial advantage, because they developed their hard structural parts much earlier. More importantly, being mobile, these animals could pick and choose the time of their land expeditions. Because they’re nocturnally active and can easily avoid the sun’s harmful rays, the arthropods didn’t have to wait for the ozone layer to form before they colonized the land. They just did so under the cover of darkness.

  Plants, on the other hand, need sunlight. They didn’t have the option of moving ashore at night and hiding by day. This means that plants were not able to survive on land until two things happened: they had to wait for a sufficient ozone layer to develop so they could remain safely exposed all day, and following this they had to develop structural support mechanisms. By the Late Silurian they solved the problem of structural support by evolving the complex molecules lignin and cellulose, and arranging the tough stuff into fluid-transporting bundles. Some scientists have suggested that plants must have colonized land first because they create the oxygen that terrestrial animals require, but the cyanobacteria and green algae had been producing this gas for billions of years before the plants moved inland. Ironically, they—not animals—needed elevated oxygen levels, for the ozone layer’s ultraviolet filtering effect and to build lignin and cellulose.

  It’s fascinating to compare and contrast plants with insects, in terms of how they coped with the difficulties of life on land. Both faced the serious problem of potential water loss, so both evolved cuticles that resist water flow. Since a dense cuticle is impervious to oxygen and carbon dioxide, plants evolved breathing pores, called stomata, which allow gas transfer and can be opened or closed to prevent desiccation. These are directly analogous to insect spiracles. Plants needed to develop a water transport mechanism internally, so they hardened cell walls with water-resistant lignin and built internal pipelines, the tracheids. This is similar to the insects’ open circulatory system, a simple arrangement where the internal organs are awash in fluids. Just as insects developed a skeletal system for structural support, plants built woody tissues with lignin and toughened cell walls with cellulose. But because plants didn’t have the option of avoiding sunlight, they evolved complex molecules, the flavonoid compounds, which act as sunscreen and protect living cells from excess ultraviolet radiation. To protect their spores, which were exposed on the plants’ highest position, they also evolved another type of sunscreen, sporopollenin.

  Some of these plant adaptations influenced insect evolution. Because lignin and cellulose are tough and highly indigestible, they protected early plant stems from potent
ial herbivores. Tens of millions of years elapsed before arthropods figured out ways to consume woody tissues in bulk. The flavonoid sunscreens would have also deterred herbivores. Eventually insects would develop digestive mechanisms to cope with such compounds, and even to build them into their own body defenses, but again that would take tens of millions of years. Only the spores of early plants provided a nutritious, ready food source. The plants defended themselves, however, by placing the spore-forming structures up high, away from millipedes and the like hiding in the soil layer. They also used an herbivore-swamping strategy, producing spores to excess and flooding the environment with more than the plant-feeding arthropods could eat. Millions of years later, in the Devonian period, these nutritious spores may have stimulated the evolution of wings and flight by luring ancient insects high above the ground and giving them a reason to be there.

  For a long time, however, the first land animals and plants coexisted peacefully. None of the early terrestrial arthropods were true herbivores. Instead, like scorpions and centipedes, they were predators, or, like millipedes and symphylans, they were scavengers that ate accumulating organic materials in the microbial soils, and maybe some rhyniophyte spores. Modern millipedes and symphylans love to burrow in moss, so the ancient land animals undoubtedly moved into the moss as soon as it arrived. But no evidence suggests that they ate whole plants. My botanist colleagues might get agitated when they hear this, but I like to say that “plants provide a substrate for arthropods.” The mosses gave the myriapods a pleasant place to live in and shelter from the sun. The benefit was mutual because in the process of burrowing and feeding, the myriapods loosened and turned the soil, cycled nutrients through it, and conditioned it for the colonizing plants. Contrary to conventional wisdom, the animals may have moved ashore long before the plants, and in order to move inland, the plants needed the animal communities to prepare the soil.

  By the Late Silurian, 419 million years ago, the first terrestrial ecosystems had been established. To us they wouldn’t have looked like much: the inland areas were still windswept, dry, and barren of life, except for microbes in the soil, while along the shorelines mats of green algae and carpets of mosses and liverworts were studded with rhyniophyte stems rising a few feet up. Nevertheless, while the Silurian rhyniophyte marshlands were not tall by our standards, they provided a virtual miniature jungle for the scorpions, centipedes, millipedes, symphylans, and other arthropod residents. But after nearly 26 million years, the Silurian was coming to an end. The Devonian was approaching, and what changes that would bring. Finally, the plants swept across the lands and rose up tall, and the first forests were established. The planet turned green, and the first insect communities arose. And finally, tens of millions of years after those brave arthropods first stepped on land, our lazy ancestors, the tetrapod lungfishes, hardened their fins, took a deep breath, poked their heads out of the water, and wondered . . . “What’s going on up there?”

  4

  Six Feet under the Moss

  We live in a world of insects.

  STEPHEN MARSHALL, Insects, Their Natural History and Diversity

  It’s been years since I’ve lived in Michigan, but I still can’t look at the palm of my tetrapodan right hand without fondly remembering the state, and pleasant sunny afternoons spent lazily relaxing on sandy beaches along the shores of the Great Lakes. As any Michigan resident will tell you, your right hand, that modified fin of a Devonian lungfish, provides a convenient map of the lower part of the state. Michigan is, in fact, one of the few states with such a distinctive form that its boundaries can be easily recognized from outer space. It wasn’t always that way. The mitten-like form of Michigan’s Lower Peninsula was carved out by glaciers over the last 1.6 million years or so. As these ice sheets grew and retreated, they did more than excavate the basins of the Great Lakes. Along the way they gouged deeply into sedimentary layers, including lots of geological formations dating back to Devonian times, 419 to 359 million years ago. These rocks were ripped apart, and smaller pieces were dragged along with the glaciers. The softer stones were eroded and polished by grit and sand in the ice. As the ice melted and the glaciers retreated, pieces were dropped along the way and fell into the chilly waters of the Great Lakes. Over the millennia since then, waves have scoured the ancient rocks along the shorelines with sand. The result is that most of them are polished smooth and rounded and mix pleasantly with the beaches for human feet.

  Reflections on Petoskey Stones . . .

  My parents moved to northern Lower Michigan in the 1970s, so I’ve had many opportunities to visit such beaches near Boyne City, Charlevoix, and Petoskey. They are frequented simply for the beauty of their water and shorelines and for their soft sand. But these particular beaches are famous for another reason: they are the main sources of Petoskey stones, the state stone of Michigan. Petoskey stones are actually fossils. They are small bits of ancient coral, broken away and fossilized, from great coral reefs that once dominated the shallow seas that covered Michigan in the Late Devonian, about 360 million years ago. They are bound to be the favorite Devonian fossil of anyone who grew up in the state.

  The commonness of Petoskey stones gives some sense of how extensive the Devonian coral reef ecosystems must have been. The largest stone found so far, in the Sleeping Bear Dunes of western Michigan, weighs more than one ton. Most are much smaller than that. If you walk in the surf along the beaches near Charlevoix, you can easily spot them in the water. While the stones are wet, the distinctive form of the coral shows vividly. The living coral itself has been given the scientific name Hexagonaria, which reflects its six-sided shape. A wet cross section of stone looks like a melting chunk of a bee’s honeycomb. If you pick up a wet Petoskey stone, you’ll find that its surface is almost invariably smooth. The rocks are soft enough that they are easily eroded in the sandy surf, and with just some bits of sandpaper and a soft cloth you can buff them even smoother, revealing the intricate designs of their hexagonal coral architecture. A polished Petoskey stone feels almost greasy. At times I like to hold one, rub its reflective surface, and try to conjure images of the lost Devonian period.

  The Petoskey corals should remind us of the continuing importance of the Devonian coral reef ecosystems, but discussions of the period usually conjure other images. Vertebrate paleontologists, when telling the tale of life, have somewhat egotistically dubbed the Devonian the “age of amphibians.” It’s the time when our amphibious, four-finned lungfish ancestors first shambled out of the water. In their defense, I’ll note that the vertebrate paleontologists and geologists who came up with this name were trying to replace a dogmatic creationist framework with an evolutionary system. Out of necessity, they documented the transition of vertebrate forms over the geological ages, but in doing so unwittingly set up a new vertebrate-centered historical system that distracts from many important events in life’s history on earth. Other biologists might tell the story with different emphases. Botanists will proudly speak of the land plants’ expansion, the Devonian origins of the first plants with roots, bark, leaves, and seeds. It was the time of the first forests and the greening of the land, at least along the waterways. A bacteriologist or mycologist would doubtless tell of the proliferation of microbial soils, the development of bacterial and fungal soil processes that made the forests possible. But as an entomologist, I’ll speak for the small, hidden creatures—the very first insects—and their surprising roles in these processes.

  Despite the proliferation of life on land, which I’ll get back to shortly, the real peak of Devonian species richness remained in the oceans among those coral reefs. By the time low forests were first developing along the shorelines, the nearby coral reef ecosystems had developed high levels of diversity and structural complexity. The Devonian reefs were built of tabulate and horn corals, unlike any now living, on which speciose brachiopod lamp shells pasted their forms. During the Silurian and on through the Devonian, the menagerie of crustacean arthropods, ancient relatives of sh
rimp and lobsters, surpassed the assortment of trilobites. The ecological niches formerly occupied by the trilobites were also being filled by more modern types of arthropods, such as the monstrous eurypterid sea scorpions, which continued to be key Devonian reef predators. The diversity of fishes for the first time surpassed that of trilobites, but the predatory cephalopod “squids” were still more assorted than fishes and continued to exceed them in numbers of species through the entire Paleozoic era.

  Although the diversity of trilobites had declined to only about 25 percent of its peak in the Late Cambrian, the population seemed to establish a new equilibrium in the Middle Paleozoic seas. It actually leveled out for tens of millions of years over the Silurian and Devonian times. Then at the end of the Devonian it dropped again dramatically. Although the numbers of trilobite species had dropped enormously since the Cambrian, don’t get the idea that they weren’t important in the Devonian reef ecosystems. The trilobite species that remained were abundant, and they were well adapted for life in those times. A good example of a successful trilobite from the Devonian reefs is the “frog-eyed” trilobite, Phacops rana, a creature so abundant in the shallow seas that once covered eastern North America that it has since been declared the state fossil of Pennsylvania. This particular trilobite had exceptionally large eyes that bugged out on the sides, hence the common name. Presumably those eyes were an adaptation that helped them survive in the predator-rich seas. Like other trilobite survivors, Phacops rana had the defensive ability to roll its body into a ball when disturbed—and disturbances would have been increasingly common over the course of the Devonian as fish diversity increased. By the Late Devonian, twelve-foot-long predatory fish like Hyneria were common in the waterways. So when those first tetrapodan lungfish poked their eyes out of the water they may have wondered what lay ahead on the beaches, but you can bet that they had a pretty good idea of what lay behind in the deeper waters. Once again, our own relatives were among our worst enemies; predation pressure from larger fish may have driven the lungfish to the shorelines.