FIGURE 6.2. This very cryptic katydid from Ecuador (family Tettigoniidae) is a modern example of the highly successful insect order Orthoptera, which began their rise to prominence in the Permian. (Photo by Angela Ochsner.)
They haven’t diversified much over the years, but the icebugs show us that you don’t need to be highly diversified to survive global catastrophes. From Russian Permian fossils we know that the stem group of grylloblattids evolved more than 252 million years ago, and that ancient icebugs somehow survived the end-Permian and end-Cretaceous extinctions without mishap. They have been with us ever since.
Life Sucks: The Liquid Feeders Tap into Success
One of the greatest Permian innovations was the homopteran piercing-sucking mouthpart design. This adaptation consisted of hollow needlelike feeding tubes called stylets, and it made the Homoptera7—the ancestors of modern cicadas, planthoppers, leafhoppers, froghoppers, treehoppers, aphids, scale insects, and their relatives—one of the most successful clans of insect plant feeders. Their very refined stylets allowed the homopterans to drill deep into plant tissues, inject salivary enzymes through one set of tubes in order to predigest tissues and fluids, and extract liquids through the other set, often directly from the plant’s vascular transport system: the phloem. Just when the Permian climate was getting drier, these insects invented a way to feed on highly nutritious liquid food. It’s also an innovative way to avoid plant defenses. Homopterans don’t have to worry about highly indigestible molecules like lignin and cellulose; they just avoid eating them entirely. At the same time these insects are able to avoid the flavonoids and other secondary defensive chemicals that may accumulate in leafy photosynthetic tissues.
The homopteran insects might seem to have invented the perfect feeding system, but there was one problem: too much of a good thing. Liquid food is saturated with water. Dissolved food molecules needed to be concentrated and its excess water dealt with. The homopterans solved this problem too in an even more fascinating way: they evolved a filter chamber in their digestive tract that concentrates food and rapidly shunts away excess water. The filter chamber works like this: a homopteran’s digestive tract is very long, and its back part loops around over its front section. A membrane wraps around the place where the back portion overlaps the front, and at this point, two things happen: excess liquid water is transferred directly into the hind intestine for rapid excretion, and food molecules are concentrated for the ride into the middle gut, where they are absorbed into the body. The digestive mechanism is not perfect, the result being that homopteran insects are constantly excreting massive amounts of water with traces of sugars. If, in the summertime, you have ever parked your car under a tree infested with aphids, you may have experienced this phenomenon. The sticky drops on your windshield are aphid poop. In dry climates this stuff tends to crystalize into solid chunks on tree branches, which later fall to the ground; this is the origin of the term “manna from heaven.”
The homopterans diversified greatly over the Permian years, survived the end-Permian without any apparent mishap, and evolved rapidly over the Mesozoic era. All this occurred before flowering plants with nectar and sweet fruits evolved, so if the earliest dinosaurs ever craved a sugary snack, homopteran insects’ manna would have been the only sweet food around. The homopterans’ proliferation once again suggests that the end-Permian extinction event was not likely a singular catastrophe. Instead, their success is consistent with the global climate change hypothesis. Maybe the climate on land was getting hotter and drier, but homopterans succeeded by developing a liquid diet and modulating fluid uptake. Maybe plant communities were changing in ways that the ancient insects could not deal with, but homopterans succeeded by tapping directly into nutritious, undefended juices deep in the plants’ vascular transport tubes.
The order Thysanoptera, known as thrips, also evolved a liquid feeding strategy at about the same time. Their scientific name means “fringed wings” and refers to the thrips’ very narrow wings, which are fringed with long hairs. However, this feature is not unique to them. Feather-winged beetles and the microscopic wasps known as fairy-flies also have fringed wings. The really unusual thing about thrips is their asymmetrical mouth: the mandible is missing on the right side but is present on the left, which means that they have one left tooth, but nothing to oppose it. Thrips use that one tooth very creatively: they twist their head when they feed and use their tooth to scratch the cellular surfaces of tender plant parts. Once the plant is damaged, nourishing fluids ooze from its surface. Thrips then use their remaining mouthparts, formed into a short fluid-sucking beak, to tipple on the liquids. So the thrips evolved a way to tap into tasty plant juices without tapping into vascular tubes, thus allowing them to avoid the problem of intense fluid pressure faced by the homopteran insects. But their feeding style required them to evolve microscopically small body sizes; most species are only a few millimeters long or less. This combination of fluid feeding and minute body size turned out to be a real winner for the thrips, which apparently cruised through the end-Permian mass extinction without serious problems and have achieved moderate species diversity over the past 250 million years. Currently, there are at least 5,500 living species.
The Transformers: The Rise of Complete Metamorphosis
The proliferation of the orthopteroid crunching and munching protocricket brigades, along with the refinement of fluid feeding by the homopteran bugs, might seem to be the major insect accomplishments of the Permian, but another insect feat ultimately makes these things pale in comparison: the diversification of complex metamorphosis, which occurs among insects with larval stages. This innovation may arguably be the single most important factor in the insects’ long-term success, as more than 90 percent of modern species belong to groups with complex, or holometabolous, metamorphosis.8
At a fundamental level, the success of complex metamorphosis boils down to wing anatomy. The new-winged insects, with their flexible wings, had a great advantage over the old-wings. But they still had a disadvantage: young nymphs developed wings from buds exposed on the sides of their thorax, and as they gradually metamorphosed, they risked damaging their growing wings. The holometabolous insects solved this problem by internalizing the development of their wings, which, along with other adult features, stem from cell clusters called the imaginal discs. This allowed young holometabolans to lead active and even aggressive lives, and avoid damaging their growing wing parts. But internal wing development had other important implications. Holometabolan larvae could burrow into plant tissues, fungi, dead animals, or any other substrate, also without damaging their developing wings. They became highly efficient feeding machines, to the point where many adults did not need to eat (they simply relied on stored food reserves from the larval stage); such feeding specialization allowed larvae to eat entirely different foods, effectively taking adults out of competition with their own young for food or habitat space. Adults in turn became more highly specialized for the mature tasks of courtship, mating, egg laying, and dispersal.
To facilitate the change from feeding larva to reproductive adult, a transformational stage evolved: the pupa. Many people think that the pupa is a resting stage, but this is far from the truth. It may allow insects to hibernate over cold winter months or during prolonged dry seasons, but its purpose is far more important. Inside the pupa, remarkable cellular changes take place. Muscle systems are restructured and the massive thoracic muscles used for flight are constructed; the wings, reproductive organs, and adult sensory systems are built. The digestive system may be extensively modified and rearranged, especially when larvae and adults eat very different food. A good example of this is the transformation from a caterpillar, which feeds on solid plant materials, to an adult butterfly that feeds on liquid plant nectar. So the advantages of complex metamorphosis are many: it allows for the safe internal development of delicate wings, new feeding possibilities, the specialization and separation of immature and adult behaviors, and the development of divers
e resting stages for escaping difficult environmental conditions.
Who were the Permian Holometabola, and what can they tell us about the period’s events? Some were obscure, such as the extinct insect order Miomoptera, known from fossil wing fragments so difficult to interpret that some paleontologists do not even agree that they belong to the Holometabola. However, many others should seem familiar because they survived the end-Permian extinction and continue to thrive today. They include the scorpionflies, lacewings, beetles, flies, moths, and caddisflies.
Killers with Long Faces and a Lot of Nerve
The scorpionflies, insect order Mecoptera, are not at all closely related to true scorpions, and they do not sting. Their name comes from the fact that the males of certain species have large bulbous genitalia that resemble a scorpion’s stinger. Their greatly elongated lower head, which gives them a horselike appearance, distinguishes them from other insects. Most scorpionflies actively prey on other small insects or scavenge dead insect bodies. The tip of their narrow snout has well-developed mouthparts, which allow them to reach into narrow spaces and chew on small prey. During the Permian years, scorpionflies were the most abundant and diverse insects with complete metamorphosis, evolving rapidly in the Early Permian,9 and by the Late Permian developing into eleven scorpionfly families, almost double the number that exists today. In fact, the diversity of Permian scorpionflies was greater than at any time since then,10 and by the end of the period it must have greatly influenced other insect populations in the forest biome, since scorpionflies also commonly preyed on slow-moving insects and insect eggs.
The lacewings and their relatives, order Neuroptera, also appeared in the Early Permian, and by the Late Permian this voracious clan comprised at least six families. The scientific name means “nerve-winged” insects and refers to the abundance of very fine wing veins; hence their common name. Neuroptera actively prey on other small insects. The adults have chewing mouthparts, but the larvae are able to pierce insects with their sharp sicklelike jaws and suck blood though narrow channels in their mandibles. Most neuropterans are terrestrial, but their novel fluid-feeding ability allowed some of them to invade freshwater habitats. Lacewing larvae also evolved another curious and useful trick. All insects have excretory organs called Malpighian tubules that extract nitrogenous wastes from the blood and dump them into the hind intestine for removal, but the neuropteran larvae evolved the capacity to convert their waste products into a useful product: silk, from which they spun protective cocoons for the pupal stage. However, to get the silk out of their bodies, they need to excrete it. Neuropteran larvae are the only animals that spin silk from their anus.
Silk Spinners, Architects, and Geologists
At least one other new Permian insect order could spin silk: the Trichoptera, known as the caddisflies. The name “caddisfly” is thought to derive from the old English “caddice men,” vendors of material who pinned cloth samples to their jackets (as a caddisfly larva glues various materials to its portable case). Their larvae spin silk in a more familiar fashion: at the head end, from modified salivary glands located near their mouthparts. Caddisflies used their silk to colonize a new habitat: freshwater streams with rapidly moving water, an excellent place to find food particles washed downstream or other small insects and aquatic animals dislodged by currents. Plus, lots of small tasty mayflies and stoneflies were in the fast-moving streams, eating the algal mats on stones.
Caddisfly larvae used their silk not just as anchors, or safety lines, when moving downstream to capture prey; some learned to weave aquatic nets in the currents to collect organic debris. Others learned to gather small bits of rock, sand, wood, and other materials and weave them onto stones, into protective tents. Eventually some figured out how to make those shelters portable by tying silk and collecting items into movable houses. Observing the portable cases of modern caddisflies (they are among nature’s most adept architects) may tell us a lot about the behavior of ancient species. The modern cases are really impressive, coming in all manner of sizes and shapes. Some are long, others are short. Some are round, while others are square or spiral. Each species builds its own unique style of case and collects its own preferred set of building materials: sand, pebbles, large stones, small sticks, chunks of wood, pieces of shell, or pieces of leaves. Some preferentially collect heavy particles, however, and one is known to accumulate and weave gold grains into its cases, making caddisflies the first geologists as well as the first architects.
Aside from their obvious protective function, the cases serve other uses. Some caddisflies tie large ballast stones to their cases, allowing them to move along the bottom in fast currents without washing away. Most build a case with a hole at each end, which allows waste to be ejected from it and water to flow through it. Many have evolved the capacity to ventilate their tracheal gills by actively pumping water through the portable case, thereby increasing oxygen flow over their gills. This has allowed caddisflies to successfully radiate into slow-moving or still waters with much lower oxygen content.
In their classic paper, “Ecological Diversity in Trichoptera,” aquatic entomologists Rosemary Mackay and Glenn Wiggins observed that in modern aquatic insect communities, caddisfly species and genera greatly outnumber that of the mayflies, dragonflies, or stoneflies. They wondered why this should be so, and they came to a perceptive and surprisingly simple conclusion, neatly summarizing 250 million years of aquatic insect evolution with this simple statement: “We view much of trichopteran diversity as an expression of ecological opportunities made possible by the secretion of silk.”11 That wonderfully versatile substance allowed caddisflies to divide the aquatic habitat into hundreds of microhabitats inaccessible to other insects without silk. Even though many of the mayflies, damselflies, and stoneflies colonized the waters millions of years earlier, caddisflies were able to spin and weave their way to new lifestyles impossible for the more ancient aquatic insects.
The presence of caddisflies during the Permian suggests that primitive moths (order Lepidoptera) must also have been around, even though they do not appear in the fossil record until the Jurassic period, about fifty million years later. A lot of anatomical and behavioral evidence suggests that the Lepidoptera and Trichoptera are closely related to each other: they are what we call sister groups, which by definition originate at the same time because they share a common ancestor.12 So this is one of the better documented cases of a major gap in the insect fossil record. We know that moths—or at least protomoths—must have existed at least since the Permian, but clearly they did not fossilize well for another hundred million years. If the most primitive surviving Lepidoptera are any indication, there are obvious reasons for the gap. They are microscopically small species that mine and feed in plant tissue; the most archaic group, the mandibulate moths (family Micropterigidae) feed on fern tissue in extremely moist, nearly semiaquatic environments. Because microscopic soft-bodied insects living in moist, warm forests decompose rapidly when they die, the earliest moths did not fossilize much, if at all.
The insect order Diptera, the true flies, also originated in the Late Permian years, and although they were not very common then, they somehow managed to survive the Permian extinction and live on to become some of the most common and diverse insects in the modern world. Like caddisflies, ancient nematoceran flies had aquatic larvae that lived in cool, fresh, fast-moving water. These larvae developed various suction-cup holdfast structures for clinging to rocks in fast currents, where they fed on algae and organic debris. To this day, some of the more primitive aquatic fly larvae in existence can spin silk, which they use to anchor their bodies in a current or move safely downstream.
Why were streams so popular among Permian insects? During the period, the southern supercontinent, Gondwana, experienced extensive glaciations. Continental areas were colliding and inland areas were being raised up to greater heights. In areas were glaciers met temperate and tropical climates, melting ice and snow from upper elevations created several c
ascading waters, which offered a rich new frontier of streambed nutrients for insects that could adapt to the swiftly moving currents and eddies. Mayflies and stoneflies were the first colonists to follow the streams up to higher and higher elevations. Soon they were followed by species of caddisflies, nematoceran Diptera, and aquatic predatory Neuroptera. Whether the Permian was a grand disaster or a time of plenty just depends on your point of view. For insects that were able to find and colonize new niches it was a time of grand success. The aquatic mayflies, stoneflies, caddisflies, and nematoceran flies all successfully survived the Permian and have radiated extensively since then.
Planet of the Bugs: Evolution and the Rise of Insects Page 13
