A hummingbird sphinx moth, Hemaris sp., with its larva and pupa.
We identified it as a hummingbird moth, genus Hemaris, of which there are several species. This one had large eyes, a pale green back, and white fuzzy pile on its belly. Instead of a beak, it had a long proboscis, a tonguelike structure that when not in use is neatly curled up into a roll on its “chin.” The moth belonged to a worldwide family, the Sphingidae or sphinx moths, sometimes called hawk moths. But aside from their behavior, which seems to mimic that of hummingbirds, and their physiology, which is analogous to a hummingbird’s, one is struck by their beauty. The subtle color schemes of the sphingids are mesmerizing. Shades of gray mix with black and pure white, rich browns, yellows, purples, pink, ruby red, emerald green, in unimaginable combinations and designs due to their soft pelage of what appears to be hair but isn’t. In birds, bright colors are used in sexual displays, but for these moths the color patterning serves as camouflage on backgrounds of bark or leaf, or as a way to startle a predator with a sudden display of false eyes. Except for the Hemaris hummingbird moths, most sphingids are nocturnal, and they all communicate by scent.
No sphinx moth at rest could be confused with a bird, but the moment it takes flight it looks like a hummingbird (though never a hawk!). These moths overlap with birds in size, and the largest have a wingspread of eight inches. They resemble hummingbirds in exterior form to fit into the same role for feeding on nectar by hovering at flowers. But their structural design could hardly be more different from a bird’s. One has two legs with four toes on each, the other has six legs and no toes. One has a long bill and a long tongue, the other has a long proboscis, a sucking straw that can be rolled up or extended (in some it is more than twice the body length). One has a huge brain relative to its body size, the other hardly more than a little knot of neurons in its thorax and an even smaller one in its head. One powers two wings by an arrangement of muscles that pull directly on bones, the other has no bones but four wings. One has lungs that pump oxygen to its muscles by way of the blood, the other has no lungs and the blood does not transport oxygen. Hardly anything about them is the same, except that they look alike.
If we didn’t know about sphinx moths, they would seem to be creatures from another world, yet they would be easily recognizable as a familiar form. But that is true in only one stage of their life. The moth has another, entirely different life, one that—if we were not already familiar with it—we would never guess was associated with the same animal. And if we examine the details of its metamorphosis, perhaps it isn’t really all from the same genetic source. In this chapter I explore yet another way life transforms itself into another life, so that we can come to a more profound understanding of the concept and mechanisms of nature’s undertakers.
LIKE OTHER INSECTS, a sphinx moth experiences a deathlike intermission of weeks to nearly a year, and potentially several years, between its two “lives.” Had I wound the clock back about ten months, the hummingbird moth I captured that spring would have been a smooth-skinned, pea green animal with a huge gut, no proboscis, and no wings. It seldom moved except for its rapidly chomping, tiny, knifelike mandibles. It could crawl, but only slowly. As the moth’s power and speed of flight are an adaptation, so is its larva’s sedentary habit and slowness. The less it moves and the slower it crawls, the less likely it is to be seen by predators who hunt such prey relentlessly, cued by motion. Though of striking appearance when in your hand, in its natural habitat the larva is nearly invisible, blending in with the leaves it feeds on by subtle tricks of camouflage, including color matching, countershading, and a brown spot in its skin masquerading as leaf damage. The caterpillar remains firmly attached to a leafy twig, where it moves only a few inches each day to reach another leaf. It eats in such a way as to leave no leaf remnants, which would clue birds to its location; before it crawls to the next leaf, it chews off the remains of the first one at the petiole to obliterate its feeding tracks. If a predator, usually a bird, lands on the twig, the caterpillar rears back and assumes a stiff, lifeless pose like an Egyptian sphinx—hence the name “sphinx moth” caterpillar.
Of the many riddles of metamorphosis, one of the more speculative is why we have or need it. The default explanation is that metamorphosis is a necessary function of growth in reaching the adult stage, and that during this process the animal must develop through forms that trace the stages of its evolution. A tadpole is thus merely reliving its fish ancestry in order to reach the amphibian stage. Similarly, the gill slits and tail of the human fetal stage are also a retracing of that same early evolutionary path. These early developmental stages are useful guides to taxonomy because they are so conservative, whereas two totally different animals—the bird and the moth—show that convergence can lead to similarity.
On a practical level, consider a tuna and a whale: unlike a tuna, a whale fetus has fore- and hind limbs like those of other mammals, so we can deduce from its embryo that it is a mammal and not a fish, whose form it resembles. Similarly, a sphinx moth resembles a bird but is not a bird, and its larval stage, the caterpillar, resembles neither fish nor fowl nor amphibian. Larvae are, as Charles Darwin indicated, a good taxonomic tool. For a long time it was thought that barnacles, because of their hard calcium carbonate shells, were highly derived mollusks. However, Darwin showed that their larvae are free-swimming shrimplike creatures, so we now categorize barnacles as more closely affiliated with crabs and their allies than with snails.
The principle of developmental transformation that traces evolutionary change is called “ontogeny recapitulates phylogeny,” an insight credited to the German biologist Ernst Haeckel. It has often been harshly criticized, if not dismissed, because it does not apply universally. A phylogenic explanation might work well enough to distinguish insects from vertebrate animals, whose early embryos all look similar to each other but much different from other animals’. However, the early developmental forms of many marine invertebrates, such as sponges, starfish, and sea urchins, are wildly different from their adult forms. Octopi, on the other hand, which are derived from clams and their allies (earlier fossil forms had shells resembling those of snails), start life as plankton, but they have no metamorphosis with intermediary stages that look like snails. When octopi hatch out of their eggs, they look like octopi. Similarly, the principle of recapitulation of descent does not seem to apply very well to many other organisms, including insects, where the metamorphosis truly looks like transformation of one animal into an entirely different one.
Insects are an ancient group that arose in the Cambrian about 400 million years ago from aquatic crustacean-like ancestors. When they came onto land they brought along their protective armor, which also served as a skeleton and was modified into all sorts of forms. But in order to grow they needed to periodically shed this exoskeleton, which did not stretch unless it was soft. Every insect molts several times before it reaches the imago (adult) stage, and with each molt the body grows and may change shape slightly. That is, molting is the necessary step that permits transformation, but it does not necessarily result in metamorphosis. The most primitive insects make almost no change at all except in size; silverfish and springtails slip out of the egg as miniature adults. Similarly, very little change occurs from one molt to the next in grasshoppers (Orthoptera), true bugs (Hemiptera), and cockroaches and termites (Blattodea). Thus the question: why is there a radical, almost “catastrophic” body change in some orders of insects, such as the Lepidoptera (moths and butterflies), Diptera (true flies), and Coleoptera (beetles), all of which have grub- or wormlike larvae? As I will explain, the radical change that occurs during metamorphosis in these groups does indeed arguably involve death followed by reincarnation.
Whenever two sets of very different genetic instructions operate, as in the metamorphosis of some insects and some other animals, the resulting incarnation is like a new species; as the larva’s genetic instructions are turned off, those of the imago or adult turn on. But why are there two s
ets of instructions for two very different animals? The standard answer is that a caterpillar’s specialized needs require different genetic instructions from those for the adult moth, which has other needs. But how could two genomes arise in one species? The view most widely accepted until recently was that this situation came about through a gradual process of natural selection, with different selective pressures at the two stages of the life cycle: strong suppression of the adult genes during the early stage and their activation at the correct time. However, a new theory claims that because the metamorphosis from maggot to fly or caterpillar to moth is so radical, with no continuity from one to the next, that the adult forms of these insects are actually new organisms. According to this proposal, sometime in their ancient heritage, when these animals were still aquatic and when all fertilizations were external, they hybridized with another species. They thus harbored a second set of genes, which could, given the right environmental conditions, be activated. In effect, the animal is a chimera, an amalgam of two, where first one lives and dies and then the other emerges.
At first glance, the idea of such metamorphosis originating from two different organisms living sequentially through recycling seems wildly improbable, and when the marine biologist Donald Williamson first proposed it, he was, as might be expected, ridiculed. But in fact the idea of chimeras incorporating genomes of other organisms is part of mainstream biology. When I was a graduate student in the 1960s working with the protozoan Euglena gracilis, it was known that while the nucleus of this protozoan contains its own genetic instructions, its body contains another, separate set of instructions in the mitochondria and yet a third in its chloroplasts. I raised these animalcules in the dark, feeding them sugar, acetic acid, and other organic compounds; they were scavengers. When I shone light on them, they turned into plants; because they had chloroplasts, they no longer needed to scavenge carbon compounds other than carbon dioxide from the air. Euglena and some other protozoa are able to transform themselves because along with their own DNA, the DNA in their mitochondria, derived from bacteria, allows them to break down and use sugar, and the third set of DNA, derived from algae, allows them to be a plant. Chloroplasts are archetypal blue-green algae that have adapted to live in a new environment—namely, inside other cells—and even to reproduce there. They have adapted, as all organisms must, by accommodation and restraint and response to appropriate stimuli in their environment. The chloroplasts’ main adaptation was to not reproduce to the point of destroying their host.
In the above example only a part of another genome was incorporated to make the composite animalcule. But this process of DNA transfer happens all the time: when phage viruses infect bacteria, they often transfer genetic material from the infected cell into the genome of another, where it is incorporated and then multiplied ad infinitum as the cells divide and multiply. This process, called transduction, is a well-established experimental tool of molecular biologists. In the case of corals, mentioned earlier, whole cells from one organism live and multiply, but semi-independently, inside other cells. Similarly, the cells of some giant clams contain green algae, and like all green cells, these fix carbon dioxide into the carbon compounds that first build themselves and then also feed their clam host. And what applies to parts of cells living in other cells, and to whole cells inside cells of other organisms, applies also to whole organisms living in the bodies of other organisms, such as protozoa and bacteria living in the digestive tracts of termites, elephants, and numerous other members of the animal kingdom. Such symbioses also extend to the organization of ecosystems, and ultimately to the interdependence of millions of organisms—the whole biosphere of earth.
The idea that protozoans acquired useful genetic instructions from algae, and termites acquired other useful genetic instructions from protozoa, is a concept no wilder than that of humans incorporating domestic animals and plants into our society, giving us new genetic instructions for making McNuggets and French fries. What’s different is the level at which the new genetic instructions operate.
Regardless of how it came about, there are indeed two very different sets of genetic instructions at work in the metamorphosis of some insects and some other animals, and these are as different as different species, or even much more so. They thus represent a reincarnation, not just from one individual into another, but the equivalent of reincarnation from one species into another. How the two coexist in the same organism without creating a garbled creature that is “neither fish nor fowl” is a potential problem regardless of how those two genetic instructions originated. The solution is that most of one body dies and the new life is resurrected in a new body. It happens roughly this way in all insects. When my hummingbird sphinx moth caterpillar had grown to its full size, it left the cherry tree where it had fed all its life to wander about on the ground and then burrow into the soil. There it created a crypt for itself; lying there motionless in the dark, it eventually shrank, shed its dead skin, and turned into a mummylike shape with a hard covering. As its organs dissolved, its insides turned to mush, and most of its cells died. However, some groups of cells, named “imaginal disks” (from “imago”), remained. These, like the buds on a plant that can grow into a twig and the twig into an entirely new plant, are like seeds or eggs generating new organs. During this apparent “resting” or pupal stage, the disks secreted enzymes that destroyed the larval cells and incorporated the proteins and other nutrients from those cells into themselves. Eventually all of the larval cells were replaced, and the new cells assembled in an orderly way to produce the moth. As with most of life, this process followed specific instructions encoded on genes that directly affect physiology.
In us the process of transformation is the same, but something new is added. First, the process of change is gradual and extends throughout our lives. Second, it is not just the genes talking; it is also the brain that, in thoughts and ideas, can almost literally cause reincarnations, in others as well as in ourselves.
Beliefs, Burials, and Life Everlasting
I have no doubt that in reality the future will be vastly more surprising than anything I can imagine. Now my own suspicion is that the universe is not only queerer than we suppose but queerer than we can suppose.
—J.B.S. Haldane, Possible Worlds
In our family, there was no clear line between religion and fly fishing.
—Norman McLean, A River Runs Through It
WE MAY THINK OUR SPECIES GENETICALLY UNIQUE, AND INDEED it is, as every species is. But the mix of our DNAs is really an amalgam of all life’s DNA, and in many and varied ways that mix reaches back to a common origin in the dawn of life. One example of most recent common origin comes from our hunter ancestors, whose skill and knowledge were pivotal, as we’ve seen, in the recycling of animal carcasses. Since those carcasses were derived from formidable live animals, which the hunters had to get to know well in order to hunt them effectively, we became empathetic. We learned that the precious, mysterious gift that we call “life” may disappear suddenly when the animal is punctured with a spear or arrow. In no area did we know less and need to believe more than in that period after death, when a body is little changed and yet suddenly bereft of life. Where has “it” gone, and where did it come from and why? We invented stories about human creation to try to make sense of our life and our fate, stories that specified our relationships to each other and to the earth, which then nurtured our morality. The knowledge to create these stories was short then, but the belief anchoring that knowledge had to be long. Metaphors helped explain the unknown in terms of the known. For the metaphors to seem true, they had to touch truths of our existence, and if they made us feel good they were more readily accepted.
To the Egyptians, the dung scarab beetle (probably Scarabaeus sacer) represented Khepri, the sacred scarab that rolled Ra, the sun god, up into the sky in the morning. Ra, believed to be the creator of all life, created himself out of nothing every day and was rolled across the sky, then returned back to nothing in th
e underworld at night. Scarab models were made by the millions as amulets and were placed on the heart of a mummified corpse in its preparation to enter the afterlife. Further instructions for human afterlife appeared in what came to be called the “Books of the Dead” (which the ancient Egyptians called “Books of Coming Forth by Day”), vignettes in hieroglyphics on papyrus scrolls illustrated with pictures of people, animals, demons, and gods. These papyrus scrolls accompanied the mummified corpse with its scarab beetle on the heart and were intended to instruct the spirit for continuing the earthly pleasures.
The most famous vignette, preserved in exquisite detail, is of a man named Ani, who lived at the time of Rameses II, around 1275 BC. We see Ani and his wife bowing toward the gods as his heart, the presumed seat of intelligence and the soul, is weighed by the jackal-headed god Anubis. Ani’s soul is instructed to speak to his heart. The feather of truth is a counterweight on the other side of the scale. Toth, the ibis-headed god of wisdom, records the verdict. Ammit, “the Devourer” (a monstrous chimera that is part crocodile, lion, and hippopotamus), awaits the outcome of the weighing, which will determine whether Ha, Ani’s soul, will continue to experience earthly pleasures during its daily journeys out to Ra, the sun god. After making his daily rounds, Ha returns to the mummified body at night. If the weighing of Ani’s heart tips the verdict to indictment, Ammit will swallow his soul. The Egyptians believed they could influence the gods, and they had to adhere to rules, practices, and conventions to prepare for their afterlife. Those beliefs were strong enough to build the pyramids, whose purpose was to facilitate the afterlife of the powerful people who could afford the costs of construction. But the pyramids were also, as the ancient Greek historian Herodotus notes, emblematic of a time of horror for the masses, who were enslaved to build them to ensure others’ afterlives.
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