Sex on Six Legs Read online

  Lamarck was quite interested in invertebrates, a subject not much studied by naturalists in the late eighteenth and early nineteenth centuries, and he was intrigued by the idea that they exhibited such fixed behaviors. It seemed reasonable to him and many of his contemporaries that doing something, whether following an odor trail or learning to count, could cause a permanent change in the body, and that such changes could be inherited. Of course, we now know that the genes cannot be influenced in exactly the way that Lamarck imagined. And it is likely that both learned and instinctive behaviors evolved together. Most behaviors, even in insects, are due to a combination of influences from the environment, and hence subject to learning, and influences from the genes, and hence instinctive, making the old argument somewhat moot.

  Dan Papaj, a biologist at the University of Arizona, doesn't believe Lamarck himself was correct, but he does wonder if there aren't new ways in which learned behavior could influence evolution. He works with a variety of species, from butterflies to parasitic wasps, to see just how learning operates in nature. He points out that the idea that fixed behaviors could have arisen from something an ancestral insect learned to do is not as far-fetched as it might seem. Researchers in the fields of robotics and artificial intelligence are particularly interested in how changes in stimuli—that is, the response a computer gets when it executes an action—could then make the computer's actions more sophisticated. It would be amusing if the behaviors so derided by Fabre and Cunningham turned out to pave the way for better, and more flexible, computers.

  Finally, social insects are well known for their genetically hard-wired altruism; honeybees can't help committing suicide when they sting an intruder in defense of the colony, because the stinging apparatus remains imbedded in the victim, tearing the innards of the bee asunder after the sting. But it has just come to light that ants, at least, can also choose to rescue their kin from harm even when the peril is novel. Elise Nowbahari and her colleagues in France and the United States took ants, partially submerged them in sand, and restrained them with a nylon filament so that their bindings were concealed under the surface. The scientists then re-leased either strangers or nest mates of the victim and watched the ants' behavior. If, and only if, the entrapped ant was from the same nest, the other ants hurried over, dug her out, and bit the snare away. Ants from foreign colonies, even though they were the same species, were left to struggle helplessly.

  Such a complex sequence of behaviors pushes the boundaries of what we thought an insect could learn. And if the same ability applies to species other than ants, we might want to rethink those sticky traps that attract cockroaches and trap them, alive and kicking, on the surface. If the roaches become able to rescue their fellows by nibbling through the glue, you have to start wondering if they might then be capable of plotting revenge.

  Chapter 2

  Six Legs and a Genome

  SOME of the most cutting-edge discoveries about insect molecular genetics, and therefore about how genes do and don't dictate complex behavior, have been made because Gene Robinson was tired of harvesting fruit. As a student worker on a kibbutz in Israel, he was asked to "help out with the bees temporarily, and since I was bored to tears picking grapefruits, I volunteered. I remember I was smitten that very first day."

  In his correspondence, he glosses over exactly why the bees were so appealing, but despite parental skepticism (he summarizes his mother's response as: "No doctor, no lawyer, where did we go wrong?"), Robinson went on to pursue a master's and later a Ph.D. in entomology. Now at the University of Illinois, he still professes an unabashed love of bees, which he has parlayed into one of the most compelling uses of genomics, the study of an organism's entire mass of DNA, anywhere in the world of biology. Robinson is interested in just how a complicated behavior such as the division of labor in a honeybee colony, where some bees go out and forage among the flowers while others stay home and nurture the young, is derived, first from the hormones coursing through the bee's body, then via the firing of nerve cells in the brain, and ultimately from the minuscule variations within a gene that directs the activity. He calls what he does sociogenomics, the molecular genetics of social behavior. It is where the genetic rubber meets the behavioral road, and it can best be understood using insects.

  Before explaining sociogenomics, a bit of background about the new age of genomics, and about what we mean by sequencing a genome or having a "genome project," is in order. The genome is the total set of DNA in an organism, arranged into the chromosomes that are characteristic of each species; humans have twenty-three pairs of chromosomes, while cats have nineteen pairs, cows have thirty, silkworms have twenty-seven or twenty-eight, and a species of ant has just one. Sequencing a genome means determining the order of the four chemical bases that are the building blocks of the helix of DNA. The bases are called adenine, thymine, guanine, and cytosine, usually abbreviated with their initials A, T, G, and C. The genes themselves are particular sequences of the bases that contain instructions on the manufacture of proteins that make up the structure of the body or instructions on regulating when and how other genes become activated. Not all of the DNA consists of genes; scientists knew going into the Human Genome Project, the first of such efforts, that some amount of the material on the chromosomes would be noncoding, meaning it does not contain information about either gene regulation or the making of a protein. The genome sequence therefore consists of a long—a very, very long—string of four letters, grouped together in a particular arrangement unique to each species.

  Once the Human Genome Project was completed in 2003, it was clear that more genomes needed sequencing. Many scientists wanted to put two animals next on the list. First would be the zebra fish, as a way to examine genes responsible for the development of a fertilized egg into an adult organism, and then the laboratory mouse, because as a mammal we could more easily compare its genes to those of people. Nobel laureate Sydney Brenner demurred, saying that "the mouse is too close. It hasn't had enough time to randomize, so you are confused by the commonness of origin."

  What he means is that because we so recently shared a common ancestor with mice, our genetic material is already very similar to theirs. But which genes are the essential ones, the ones retained through hundreds of millions of years? How have genes changed to perform different functions? To answer that, we need insects. It's been 250 million years since the mosquito Anopheles gambiae and the fruit fly Drosophila melanogaster shared a common ancestor. That's roughly the same evolutionary distance that exists between humans and fishes, a third more than the distance between humans and chickens.

  Of course, it's not an either-or situation. The zebra fish and mouse genomes have now been sequenced, along with those of the chicken, the African clawed frog, and a nematode called Caenorhabditis elegans. Genome projects are in progress for a whole host of others, including the European hedgehog, the green anole (a small lizard often sold in pet stores as a chameleon, although it is only distantly related to the true chameleons), and the gorilla, in addition to many invertebrates. Nevertheless, insects can reveal the process of evolution in ways that no other group of organisms can.

  As I already pointed out, insects are the most diverse group of organisms on the planet—there are more kinds of insects than any other organism, they live almost anywhere except deep in the ocean, and they vary enormously in size, shape, food habits, and virtually every other aspect of life. A queen ant can live for decades in her nest, while tiny midges that circle over fast-running Appalachian streams can dispatch a whole adult lifetime, complete with finding a partner, mating, and laying eggs, in a prompt 45 minutes. That diversity makes it much easier to answer questions about the genes responsible for traits such as life span or body size, because we have so many different types of animals to compare. Even if we had genomes for all the primates, say, or even all the mammals, it wouldn't be as useful as having genomes for as many types of insects, because compared with insects, one monkey is pretty much the same as
another when it comes to appearance and even behavior. A monkey is a lot more like a mouse than a grasshopper is like a flea. And of course insects are important vectors of diseases from malaria to typhus, as well as linchpins of our agriculture through pollination and pests because of their fondness for the same foods we eat. Without them, we cannot understand what makes life tick.

  What's more, because we shared a common ancestor with insects so long ago, we can use them as a way to explore how we arrived at similar-seeming destinations with such radically different modes of transportation. For example, we are social and spend time and energy taking care of our young. Honeybees are social and spend time and energy taking care of their young, too. We share a fair proportion of genes with honeybees—but are the genes associated with social behavior the same in both of us? If they are different, how do they get similar results? If they are the same, why did the genes persist through evolutionary time in us and them, but not in thousands of other species?

  Size, Junk, and Garbage

  BEFORE exploring which insects have had their genomes sequenced and what those sequences tell us, it is necessary to look at a different kind of large-scale genetic information we can get for living things: genome size. Before we knew much about the chemical bases that comprise the DNA inside a cell, we could at least determine the amount of DNA itself. Indeed, calculating an object's size is one of the first things we do with something new, whether that something is a previously undiscovered mountain, a recently incorporated township, or a newborn baby (why the vital statistics of weight and length are so often included on birth announcements is a mystery, at least to me, but it testifies to our obsession with measurement).

  Ever since the DNA molecule was discovered in the late 1800s, scientists were interested in the amount of it in different kinds of animals and plants. In the 1940s and early 1950s, the "DNA constancy" hypothesis, which stated that the nuclei of cells in various tissues contained about the same amount of DNA, and that this was roughly twice the amount contained in sperm cells, was used to test, and eventually support, the notion that DNA was indeed the source of genetic material.

  Once this idea was accepted, it seemed plausible that the more DNA a species had, the more genes it possessed, and therefore the more complex it could be. Intuitively, people looked at genes like money in the bank; the more you have, the more you can buy. Scientists thus expected that smaller, simpler organisms such as amoebas or flatworms would have less DNA per cell than hamsters or birds of paradise. Much to their surprise, this turns out not to be the case. The amount of DNA—weighed in picograms, or trillionths of a gram—is not related to the apparent complexity of the animal or plant in which it resides. Knowing genome size is useful in deciding which organisms should have their genomes sequenced, for the purely practical reason that sequencing smaller genomes is cheaper.

  Animals vary seven-thousand-fold in their genome size, and as you might expect, insects are champions of this variation. Among mammals, the smallest genome of 1.73 picograms resides in the Asian bent-winged bat, while the largest, in the red viscacha rat from South America, is really not all that much bigger, at 8.4 picograms. This size difference is dwarfed by insects, which vary 170-fold in genome size. Here the champion seems to be a mountain grasshopper, with the diminutive Hessian fly as its sparsely endowed counterpart. Humans, by the way, have genomes of a modest 3.5 picograms, which at least weighs in at more than the house fly, though less than that of the grasshopper.

  Aside from the kind of Trivial Pursuit cum Guinness Book of World Records appeal of this kind of information (though, alas, clues about genome sizes are unlikely to come up in crossword puzzles), what does the variation in genome size—and its lack of relationship to the complexity of the organism in which it resides—mean? Obviously, more isn't better. Bluntly put by Ryan Gregory, a biologist at the University of Guelph and one of the world's leading genome size researchers, this decoupling of DNA content and complexity puts paid "the expectation that genomes consist of the genes, all the genes, and nothing but the genes."

  So if the genome contains material other than genes, how did that happen? Furthermore, what exactly is that other material, and what is it doing in there? And why do some organisms seem to have so much more of it than others?

  The answers to these questions are intertwined. Some of the "extra" material consists of free-floating bits of DNA, sometimes called transposable elements or, more colorfully, selfish DNA. These arise when a sequence of DNA copies itself several times and then just lingers as part of the genome. It is selfish because, a la Richard Dawkins's selfish gene, the elements benefit by making more copies of themselves, but they do not contribute to the functioning of the organism in which they reside. If there is no disadvantage to the organism of harboring them, or even if there is a cost but no means of getting rid of them exists, they will persist, cluttering up the genome and giving us those oddball genome sizes in some species.

  Other noncoding DNA is often called junk DNA, which sometimes is used to mean all types of genetic material aside from the genes themselves, but more properly refers to copies of genes that used to be functional but are now obsolete. Like a manual lawnmower with a broken blade that you tuck away in the garage even after you've bought an electric model, the junk DNA clutters up the genome. In a distinction reminiscent of couples squabbling over organizing the closets, some scientists call DNA junk if it's not functional at the moment but could be useful at some hypothetical time, like that lawnmower, but garbage if it's not functional now and never will be, like—well, maybe it's best not to offer an example here. As with the transposable elements, junk DNA is thought to accumulate because DNA has an inherent tendency to copy itself unless otherwise halted.

  Genome size is often, though not always, a reflection of body size, particularly among insects and other invertebrates. And insects that take longer to develop from eggs into adults have larger genomes as well. Another restriction on insect genome size seems to be the way that the species develops—does it go through a metamorphosis with egg, caterpillar, cocoon, and adult stages, like a butterfly, or does each successive stage look like a slightly pumped-up version of the one before, like a grasshopper? The butterfly types seem to have far smaller genomes than the grasshoppers, for reasons that are unknown. Also perplexing is a link between sperm length, which as I discuss further in a later chapter varies enormously among insects, and genome size. And intriguingly, all insects that exhibit social behavior, including not just bees and wasps but termites, as well as cockroaches that take care of their young after hatching, have reduced genomes, despite the vast evolutionary distance between these groups.

  I look forward to the solutions to questions about genome variation, but what I like best about the measurements of genome size is the way they make our selves feel so literal, so concrete. Thinking about how many molecules can be crammed into a cell, imagining the adenines and thymines jostling for position, or the helices spooning like lovers in the nucleus, means that we can visualize who we are with startling clarity. Science writer Carl Zimmer titled his book tracing the history of our understanding of the brain and its relation to the mind Soul Made Flesh, in reference to the way that we can now see our essence in neurochemicals and gray matter. Thinking about the actual DNA, doled out in infinitesimal picograms in the genome, seems to make that translation even more tangible.

  The Sequential Fruit Fly (and Mosquito and Beetle)

  THE FIRST insect to have its genome sequenced was, as you might imagine, that sturdy workhorse Drosophila melanogaster. This was followed by the honeybee, a suite of other fruit fly species in the genus Drosophila, two mosquito species, the silkworm moth, and the tiny beetle that often inhabits the flour canister in your kitchen. More are on the way, and all are helping us understand the action of evolution on humans as well as our six-legged kin.

  Let us begin with the fruit flies. D. melanogaster is the model species for genetic research, but other species of Drosophila lead lives tha
t are both similar and different. Unlike the cosmopolitan D. melanogaster, D. sechellia, for example, lives only on the Seychelles Archipelago in the Indian Ocean, where it specializes on eating Morinda fruit, from a usually toxic plant. Drosophila grimshawi has elaborately patterned wings and is one of the extraordinarily diverse Hawaiian Drosophila, occurring only in a handful of remote locations. It is nearly a hundred times bigger than the puny D. melanogaster. A close relative of D. grimshawi, D. mojavensis is native to the Sonoran desert of the Southwestern United States and breeds on the spiky organ pipe cactus.

  The flies were chosen deliberately to cover a broad range of evolutionary history; the different species shared a common ancestor anywhere from half a million to sixty million years ago. This is approximately the same distance between humans and lizards, all within a group of flies in the same genus. Many of the genes are similar in all of the species, but others are surprisingly different. Journalist Heidi Ledford referred to the "turmoil" of the genome that is visible only when genes are compared across species; genes appear and disappear, the time and place for them to be switched on and off is altered. Even those stalwarts the sex chromosomes had some surprises; some genes were thought to be expressed only in males because of their position on the X chromosome, but different species with the same gene did not always express it in the same way. The genes used to code for molecules that fight microbes—part of the fruit fly immune system—are much more variable than others, which makes sense given the rapid rate of change of the disease-causing organisms. Genes for detecting odors, crucial to animals that make their living and find their mates on fermenting vegetation, are also diverse. And in some cases, although the regulation of a pathway for making a protein clearly changed, the protein itself was still being produced, suggesting that so-called transcriptional rewiring might be commonplace.