Planet of the Bugs: Evolution and the Rise of Insects

by Scott Richard Shaw

  While one can’t very well look at the Jurassic years without admiring the dinosaurs, I do have an ulterior motive in bringing them up: to compare those massive meals with some tiny ones in dead fallen trees—beetle larvae in rotting wood, to be precise—eaten by wood wasps. Remarkably, 180 million years ago, the dinners of these small burrowing insects became even more significant than the gigantic meals of the allosaurs, which enjoyed the grandest predator-prey relationship in the history of the planet. To understand this, we need to compare the descendants and fates of the allosaurs and the wood wasps.

  For all their grandeur, the allosaurs faded away. They may have been the forebears of the Cretaceous tyrannosaurs and velociraptors, but even these dinosaurs fell into decline, and around 65 million years ago the carnivorous theropods were snuffed out entirely. Such exceptionally large predators just didn’t have the staying power to last forever, but more importantly, their ecological niche requirements were massive; terrestrial ecosystems could only support a few such stupendous predators at the same time. There was no way they could possibly diversify into hundreds or thousands of descendant species.

  Consider, by way of contrast, the history of the Jurassic wood wasps. Sometime in the Early Jurassic years, a band of rebellious young wood wasps rejected the vegetarian diets of their ancestors and decided to eat beetle larvae. And so the dynasty of the parasitic Hymenoptera was born. Over the passing years these meat-eating wasps diversified and specialized to feed on a variety of multifarious insect species that had already evolved in the forests. By the end of the Jurassic there were hundreds of these parasitic wasp species, by the Late Cretaceous there were thousands, and currently there are hundreds of thousands, possibly millions, of descendant species.5

  We all have a pretty good intuitive grasp of what predators are: aggressive animals like Anomalocaris, scorpions, meganeurid air dragons, fin-backed reptiles, tyrannosaurs, and praying mantises that stalk and eat other (prey) animals. Easy enough to grasp—but there is an easy-to-overlook subtlety here: predators require multiple prey individuals and must keep hunting to survive. This approach worked fine for thousands of species over hundreds of millions of years, but in the Early Jurassic the wood wasps broke the mold and invented an entirely novel predatory behavior when they killed and ate only one other individual animal (called the host), that was large enough to feed them to adulthood.

  Although the term “parasitic” is loosely applied to a variety of unrelated insects such as lice, fleas, certain flies, and parasitic wasps, all of which live at the expense of one other animal, the parasitic wasps are different from lice and fleas because they feed extensively on the host animal, eventually killing it. This deadly behavior is so important ecologically that we use another term to describe organisms that do it: parasitoid. A parasitoid is any parasitic organism, more often than not a wasp or fly, which causes its host to die. The Jurassic parasitoids didn’t just find a new protein-rich meal, they narrowed their ecological niches to smaller dimensions than those of any previous predatory animals and in doing so allowed their descendants to live in a multitude of previously unoccupied microscopic niches. From that time onward, parasitoids dominated the diversity of terrestrial communities, and by their selective killing behaviors they shaped the richness and abundance of both the insect and plant communities. The scientific fact that the most successful bloodline of parasitoid animals is descended from a clan of log-chewing Jurassic wood wasps is well established. It’s broadly supported by independent evidence from the anatomy of living wasps, the ecology of their feeding behaviors, the fossils of Mesozoic wasps, and DNA evidence from modern wasps. But why did wood wasps in particular evolve parasitism?

  This is a good point to pick up a discussion thread from the last chapter, where we introduced the xyelid sawflies. Over the Late Triassic and Early Jurassic years, sawflies became among the most successful forest insects by diversifying into myriad vegetarian sawfly clans. As new plant species evolved, sawflies successfully colonized them, and new species coevolved with the forest plant community. The sawflies also subdivided the plants into multiple feeding niches. Some fed externally on leaves, while others learned to conceal themselves by tunneling and mining in leaf tissues or by hiding and feeding in leaf shelters constructed by tying together leaves with threads of silk. As sawflies were adapting to feed on different plant parts, so were other kinds of insects. As a result, competition for all edible plant parts increased, and sawflies responded by further varying their diets. Some specialized by tunneling into plant stems and others ultimately delved into the thicker woody tissues, evolving into the wood wasps. Their success in this endeavor was propelled by the same useful tool that promoted the first sawflies: the female ovipositor.

  The Story of the Sting

  We tend to think of wasps’ ovipositor, from which the stinger, or sting, evolved, as being a simple structure, like a hypodermic needle adapted for injecting eggs. It is actually far more complex. If you were to slice a wasp ovipositor in cross section and examine it microscopically, you would find that it is not one hollow tube but three or four separate interlocking shafts, each of which can be moved independently of the others.6 This allows the tip of the ovipositor to drill into hard substances, such as plant stems and wood, and be directed with great accuracy. To better understand this idea, try the following exercise. Clasp your hands together by interlocking your fingers and wrapping them tightly around your knuckles. Now extend the first two fingers of each hand, so that exactly four fingers are extended straight. This represents the form of a wasp ovipositor. Look at your fingers end-on and you will see that there is a little hollow space in the middle. This is like the tube through which the wasp egg passes. Now try moving some of your extended fingers, while holding the others in place. For example, try sliding your right fingers downward while keeping your left ones stiff. You will notice that the tip formed by the left fingers is turned to the right, even though they are not being flexed. This is how a female wasp is able to direct the tip of her ovipositor; by retracting the four shafts independently or together, she can move the tip with precision in various directions.

  The transport of eggs, hypodermic-fashion, across a microscopically thin tubular pathway required the evolution of microscopic eggs with highly flexible shells, eggs that could be distorted from an oval shape into a long, thin, sausage shape while being forced through this minute tubule. But more importantly, wasp eggs needed a mechanism that would transport them through the ovipositor. In this case, the mechanism was fluid pressure: the ovipositor is a hypodermic needle through which wasp eggs are literally squirted. Consequently, right from the start, wasp ovipositors evolved with a variety of associated liquids. These fluids initially came from female reproductive glands, and provided not only lubrication inside the ovipositor shaft, but also fluid pressure for physically transporting the eggs. They also allowed for the early evolution of wasp venoms.

  From sawflies to wood wasps to parasitic wasps, these venoms diversified to accomplish an array of useful functions that we still see today. Some sawflies inject venoms into plant tissues along with eggs, and these venoms induce unusual plant cell development, causing galls to grow. These growths form protective sites for egg development, as well as safe areas and nutritious tissues for larval feeding. In other cases the injected venoms may have antibiotic properties that protect the eggs from the ravages of microbial growth. Among wood wasps, gooey venoms were adapted to promote the growth of fungus. As I mentioned in previous chapters, wood, with its high amounts of nonnutritive lignin and cellulose, is the least digestible part of the plant for an insect. So, like the wood-boring beetles before them, wood wasps adapted to eat the fungus that grows inside decaying wood.

  The immature wood wasps were bound to bump into the juicy larvae of various wood-boring beetles from time to time, which were bound to be more delicious and nutritious than either rotting wood or fungi. The jump from chewing on fungi to chewing on the meat of other insects does not seem all t
hat great when one considers that on the tree of earthly life, animals are more closely related to fungi than we are related to plants. In other words, animal tissue is more like the tissue of a mushroom than that of a leafy green plant. Nutritionally and physiologically, the change was not that enormous.

  More challenging, perhaps, were the vital behavioral changes involved in switching from a vegetarian to a carnivorous life style. A wood wasp chewing on fungi in a rotting log didn’t have to contend with the fungi fighting back. Beetle grubs, however, were not totally defenseless. They could still wiggle around in their tunnels, and when attacked they could bite just as well as the wasps. Moreover, a wood wasp’s developing eggs would be defenseless against a beetle larva’s chewing mouthparts. Clearly the wood wasps needed a secret weapon to tip the scales in their favor.

  FIGURE 8.2. Megalyrid wasps (order Hymenoptera, family Megalyridae) are among the oldest living examples of parasitoid wasps; the family is thought to have evolved in the Jurassic period. Top, a female of an undescribed extinct megalyrid species in mid-Cretaceous amber from Myanmar with a long ovipositor, estimated to be about ninety-nine million years old. (Photo by Vincent Perrichot.) Bottom, the head (right) and ovipositor (left) of a modern, undescribed Dinapsis species from Madagascar, a rare surviving example of this ancient wasp group.

  The adult wasps, not their larvae, developed the trick that gave them the decisive advantage, and once again, the female ovipositor made all the difference. At about the same time that some wood wasp larvae were developing a taste for meat, some of their mothers were refining their egg-laying skills and trying out new kinds of venoms. These mother wasps would drill adroitly into the tunnels where large beetle larvae were feeding, then poke their ovipositors directly into the larvae and inject a new kind of venom that induced permanent paralysis. Then they would extract their ovipositor a bit and carefully place their eggs on the paralyzed beetle. Consider the advantage of venom that did not kill an insect, but rendered it motionless. If a beetle larva were killed by an adult wasp, it would begin to rot and decay, and the decomposition process would endanger the developing wasp egg. Paralyzing the host insect with venom instead is a cheap and efficient way to preserve the meat until the egg can hatch and the baby wasp can safely begin feeding. It’s pretty much like setting a full food dish next to a lazy dog: the wasp larva doesn’t have much to do other than sit there and chew on a big chunk of fresh meat.

  Which Way to Eat an Oreo: Two Kinds of Parasitism

  The sort of external parasitism that I’ve been describing has existed for about 150 million years. Termed “ectoparasitism,” which literally means “feeding as a parasite from the outside,” it became, over the intervening years, an important factor in the evolution and success of the wasps in particular. But the origin of parasitism is really just the beginning of a much bigger story. Although the first parasitoid species were very successful, diversifying and chewing on whatever young beetles they could find in the decaying wood for millions of years, they stayed restricted to that particular habitat until some entrepreneurial wasp came along with another new approach. Sometime in the Late Jurassic or Early Cretaceous the parasitoid wasps figured out how to feed inside other animals as an internal parasite. This more refined method of parasitism is what we term endoparasitism. It literally means “feeding as a parasite from the inside,” and looking at the modern insect world, the vast majority of parasitic species are of this second sort.

  Although ectoparasitoids’ early success in the Middle Jurassic was mainly due to their strategy of feeding externally on only one small organism, this approach had a major drawback. The host insect was permanently paralyzed and the immature wasp needed ample time to hatch from its egg, then devour the entire beetle grub. The process took many weeks, at least, and could work only in concealment. If exposed, the young wasp would be revealed to predators and subject to harsher environmental factors: desiccating sunlight, temperature extremes, wind, and storms. Therefore external parasitism was mostly limited to protected microhabitats inside plant tissue, which hindered what ectoparasitoids could ultimately achieve. Now, as then, the great majority of external-feeding parasitoids are associated with immature insects found inside plant tissues. The internal feeders, in contrast, were unfettered by these habitat constraints. The host became the endoparasitic wasp’s niche and its entire habitat during its youthful existence (endoparasitism was literally the discovery of niches within other insects). Once inside the host, the endoparasitic wasp larva became entirely portable, and it could exist in any habitat where the host might exist. As a result, endoparasitic wasps were able to diversify and feed inside virtually all kinds of Mesozoic insects. A Pandora’s box of feeding behaviors was opened for the wasps.

  Once again, an important event in the history of wasps was the refinement of egg-laying behavior and the female ovipositor. Some females quit laying their eggs on the outside of the host and started injecting them directly inside it. Stated succinctly like that, the transition to endoparasitism sounds simple, but it wasn’t. Remember that female wasps were already drilling and stinging host insects for millions of years, injecting paralyzing venoms with their ovipositors. They could have easily inserted their eggs inside other insects along with venom as soon as they developed parasitic behavior. But they didn’t. Instead, they pulled out their ovipositors from inside the hosts and laid their eggs on the outside, allowing their young wasp larvae to feed externally. The reason they didn’t initially place their eggs on the inside is that being there is a lot more challenging than being on the outside. Insects have an open circulatory system, so their inside is a sack full of organs bathed in a pool of blood. That blood, like our own, contains cells that defend insects against microscopic invasion. Early parasitic wasp venoms may have paralyzed a host’s muscular system, but they did not incapacitate the immune response of its blood cells. A small egg placed inside an insect’s body cavity would be swarmed and encapsulated by these cells and killed. Successful endoparasitism required that wasps evolve an array of special adaptations to the internal environment.

  The first step to successful internal parasitism was yet another refinement in precision egg laying: some wasps laid eggs directly into the host’s nerve or muscle tissue, thereby avoiding its blood—and immune system—entirely. This is a nice adaptation, as far as it goes, but sooner or later the egg needs to hatch and the young larva must move around and eat. It’s hard to avoid the blood entirely, and in fact, there is a very good reason to want to be there: insect blood is a pool of nutrient-rich fluids. So ultimately the most successful internal parasitoids were the ones that invented ways to compromise the host’s immune system. Once again the mother wasps helped their offspring. Along with eggs, they injected venoms, some of which were modified to help disable the immune system—but somewhere along the line an even more unexpected event occurred: a symbiotic relationship was forged between certain viruses and the wasps.

  We all have heard how dirty hypodermic needles can transfer viruses. Back in the very early days of internal parasitism, one of the wasps managed to soil its own hypodermic ovipositor with some virus particles. This happened fortuitously, but then those particles were injected, along with a wasp egg, into a hapless host insect. The virus replicated itself within the host, disabling its immune system but not harming the wasp larva. At the same time, the virus was able to imbed itself inside the developing wasp’s body and so was able to escape and eventually find its way to another potential host. It was a win-win situation for both the virus and the wasp.7

  Once host immune systems were disabled, wasp eggs and larvae could wallow safely in insect blood. An external parasite’s egg has a tough outer shell, which protects it from environmental factors, and a large protein-rich yolk, which feeds the developing embryo until it hatches into a larva. An egg placed in blood, on the other hand, does not have such a thick outer shell; it floats in a protein-rich liquid environment and, with a thin shell, absorbs nutrients directly from the host�
�s blood. Now the endoparasitic wasps only needed a mechanism for extracting nutrients, so that their eggs could survive with little, if any, yolk. If less yolk were needed, then females could produce eggs more easily and lay more of them. And so the endoparasitic wasps evolved a structure called a trophamnion, which works like a parasitic placenta. The trophamnion consists of a cluster of cells, closely connected to the embryo, that absorbs and transfers nutrients directly from the host’s blood. These cells feed the embryo it until it develops into a larva, which bursts from its egg and swims away. The trophamnion’s benefits do not end there. As the egg hatches, its cells disassociate and move independently into the host’s blood pool. These former trophamnion cells continue to extract nutrients from the insect’s blood and work to further disable its immune system. As they continue to feed, they grow and eventually morph into giant cells, called teratocytes, which the young wasp larva also consumes as it swims about and dines on the host’s blood and tissues.

  Wasp larvae adapted to life in their miniature aquatic environment by developing the ability to swim with long, taillike appendages, which they whip back and forth, and the ability to breathe with closed, gas-filled tracheal systems, which, since they have no open breathing holes, prevent water from flooding into them. The larvae also developed a thin cuticle without much hard skeletal material along their body wall. This allowed them to breathe directly through their body by a process known as cuticular respiration, just like many other aquatic insects that live in ponds and streams. Indeed, the wasps are actually the tiniest of aquatic insects and also the most diversified group of aquatic organisms.

  Although a larger aquatic insect living in a pond has a lot of room to move about, a parasitic wasp larva swimming in insect blood is limited to a small enclosed space. It literally lives inside a bowl of soup, its only food. This presents a special problem: anything that eats and grows must also produce waste, so how does the larva continue to develop without fouling its food and living environment? We can appreciate the importance of teaching kids not to pee and poop in the swimming pool and bath tub—all the more important when the pool is a food source as well. Young wasps solve this problem by simply accumulating waste inside their bodies and never defecating. They assimilate nutrients very efficiently with the middle part of the digestive system, but the hind part is closed, forcing waste into the rear end. When a wasp larva is done feeding, growing, and molting through several stages, it exits the host to spin its own silk cocoon, pupate, and finally transform into an adult. Upon emerging from its cocoon, the full-grown wasp voids its larval waste for the first and last time.