Sex on Six Legs Page 6
In contrast to the desire to discover universal principles about the operation of genes from the workings of Drosophila, the scientists examining the two species of mosquito that have had their genomes sequenced had a much more practical motivation: they wanted to understand species that have such enormous effects on human health. The first species to be sequenced, Anopheles gambiae, is the principal vector of malaria in Africa. The second, Aedes aegypti, transmits yellow fever, dengue fever, and the less well known chikungunya virus; the latter was responsible for a recent outbreak in countries bordering the Indian Ocean that caused about 250,000 cases of illness and over two hundred deaths. Two U.S. Department of Agriculture entomologists, Jay Evans and Dawn Gundersen-Rindal, note that Anopheles was "the first animal to be sequenced, other than ourselves, whose actions have a strong direct impact on human lives." Although Aedes has a much larger genome than Anopheles, it doesn't encode many more genes, further supporting the idea that even closely related species can differ in the amount of noncoding DNA.
Once the sequence data can be used to identify functional genes, it should be possible to detect which genes are responsible for, say, successful transmission of the microorganisms that carry disease inside the mosquito's body, or for the mosquito's ability to use odor cues in sweat or exhaled breath to find a human to bite. The hope then is to tinker with these genes and breed a mosquito with a gut that is inhospitable to the malaria parasite, or one that cannot smell a delectably pungent victim nearby. Genes that are used to resist the effects of insecticides could similarly be altered to ensure that the mosquitoes remain vulnerable to certain chemicals.
If the fruit flies were sequenced to take advantage of the classic model system for genetics, and mosquitoes were sequenced in hopes of applying the knowledge to curing human disease, the flour beetle Tribolium castaneum could be said to have been sequenced because, well, no project in animal biology is complete without including a beetle. More kinds of beetles have been described than any other single group of animals—with over 350,000 species, one-quarter of all of the species of animals in the world is a type of beetle. The scientists who collaborated to sequence the flour beetle genome boast that beetles are "by far the most evolutionarily successful" multicelled organisms, and list, as if the insects were trying out for some kind of all-star reality television show, the many talents found in the group: "Beetles can luminesce, spit defensive liquids, visually and behaviorally mimic bees and wasps, or chemically mimic ants." I am not sure why these particular abilities are showcased, although there is a kind of "animals you might want with you on a desert island" kind of flavor to the selection. Interestingly, the beetles share with that other highly successful insect group, the ants, a lack of flight in day-to-day life; although most beetles can fly if necessary, their lives are mainly spent walking and tunneling on the ground. Whether this sacrifice of fragile wings is the key to their profligacy is not clear.
Tribolium itself is a good choice, among all those hard-shelled crawling candidates. Because it is easy to rear in large numbers in Petri dishes or other small containers, it has already been the subject of other types of genetic studies for many years. It is also an economically important pest in stored grains, which means that discoveries about its genome could reveal genetic Achilles heels to be exploited in its control, an urgent need since up to now it resists all kinds of insecticides that have been used against it.
Despite all the attention paid to the fruit fly Drosophila and its kin, it turns out that Tribolium is more of an "ur-insect," so to speak, than the fly—in other words, the flour beetle's genes seem to be less specialized and more like that of the ancestor of the entire class of insects than do the Drosophila genes. Over 125 groups of genes that the beetle has in common with humans, for example, don't occur in the other insects whose genomes had been sequenced as of 2009, suggesting that Tribolium has some pretty basic genetic material. In fact, nearly half of its genes are ancient, with counterpart genes occurring in vertebrates. This primordial nature means that it will be easier to determine how genes have changed through evolutionary time by comparing various groups to the Tribolium, and to determine which genes are responsible for general features of insect biology, such as metamorphosis or molting, and which are more idiosyncratic, say, those controlling the ability to make honey.
As is the case for genome size, and for that matter body shape and appearance, the genetic information from insect genome sequences is much more diverse than that obtained from vertebrates. A few constants appear, such as genes associated with detecting odors or those used to produce compounds that fight disease, but others are far more specialized. Silkworms possess about 1,800 genes that aren't seen in mosquitoes or fruit flies, including some used to make silk; although all insects and spiders use silk in some form or another, for spinning cocoons or dropping down from ceilings, the silkworms seem to have some additional genes exclusive to their lineage.
Of course, the first step after sequencing is to find genes with particular functions. Once that is accomplished, the opportunity arises for new, and sometimes diabolical, methods of pest control. Scientists are currently trying to use genetics to make insects pass on the instruments of their own destruction. A gene that is innocuous in the presence of, say, a particular antibiotic, but lethal otherwise, is inserted into an insect. The insect is then reared on a diet containing the antibiotic until it is an adult, when it no longer feeds, and is released into the wild. After the insects with the manipulated genes mate with normal members of the opposite sex, they produce offspring containing the gene—but those offspring are out in nature, where the lethal gene takes effect. Other even more clever methods are in the works.
As with genome size, studies of genome sequences confirm the presence of a hefty amount of noncoding DNA. One researcher refers to it as "dark matter," similar to the science fiction-like invisible stuff of outer space, which conveys both the mysterious nature of the substance and the almost peevish response that its discovery has elicited. We all seemed to have expected Mother Nature to be more thrifty in her allocation of genetic material, maybe saving that extra DNA, like leftovers at dinner. Shouldn't somebody have made another organism out of those bits and pieces of adenine and cytosine? Or maybe we just don't like the idea that it doesn't take many genes to make a whole complicated being; as Ryan Gregory says, "The strikingly low number of genes required to construct even the most complex organism represents one of the most surprising findings to emerge from the analysis of complete genome sequences." Somehow we seem to feel cheated by our own simplicity.
Of course, it's not that we are simple, per se. It's just that, once again, we are reminded that evolution is a tinkerer, using what's at hand to make its products. I like to think of the nuclei of our cells, not as perfectly tuned whirring machines, each gear essential, but as vast echoing warehouses of factories. Entire machines are outdated and useless, left rusted in a corner but never taken away and demolished. Others are jury-rigged out of pieces from older models and newer ones, rattling jerkily through their paces but ultimately manufacturing something useable.
The Social Genome
ALTHOUGH honeybees, like mosquitoes, are enormously important to human well-being, the sequencing of the honeybee genome was heralded not just because it might help us fight the mysterious decline of colonies throughout North America, but because bees are such extraordinarily social animals. Gene Robinson, who eschewed fruit-picking to devote himself to bees, thinks studying their genomes can show us how animals can become so integrated that they are often described as a single superorganism. According to the great biologist and ant lover E. O. Wilson, "If Earth's social organisms are scored by complexity of communication, division of labour, and intensity of group integration, three pinnacles of evolution stand out: humanity, the jellyfish-like siphonophores [creatures such as the Portuguese Man o' War], and a select assemblage of social insect species." Where does this high degree of interdependence come from?
One of th
e most surprising pieces of news from the honeybee genome project, published in 2006, was the relative paucity of genes associated with defense against diseases, compared with the other insects that have been examined. Given the crowded conditions of your average hive, one might imagine that pathogens would spread faster than colds at a preschool, which should select for highly vigilant immunity. One possible explanation is that the intense social behaviors of the bees, for example, the grooming and licking that individuals are always bestowing on each other, obviate the need for other defense mechanisms. It is also possible that honeybees, domesticated as they have been for thousands of years, will turn out to be an anomaly in this regard, a question that the sequencing of other social insect genomes should help settle. Two other startling results were the small total number of genes in the honeybee genome, and the apparent conservatism in the rate of the genome's evolution, compared with the mosquito Anopheles and Drosophila melanogaster, so that at least for some groups of genes, bees are more like vertebrates than those other insects. Contrary to what had been believed previously, in fact, bees seem to have arisen quite early in evolutionary history, branching off before the beetles.
Bees do have a lot of genes associated with producing and detecting pheromones, chemicals used to communicate with other individuals, which is not so surprising given their reliance on signaling within the colony, and they have some new genes that are associated with collecting nectar and pollen. But do they have special "sociality genes"? Several years before the honeybee genome sequence was completed, Gene Robinson noted that the difference between highly social insects such as the bees and solitary species such as Drosophila was likely to lie not in the creation of entirely new genes, but in changes in the way the same genes were turned on and off, or in the amount of product a given gene made. With some exceptions, this has turned out to be the case. Indeed, Robinson and his postdoc Amy Toth suggest that just as developmental biologists have discovered "modules" in body plans, with wings, legs, and arms produced from similar groups of genes in different animals, behavior can likewise be broken down into building blocks.
One of the most significant elements of insect sociality is the division of labor that Wilson cited above. Unlike other insects, or even virtually any other animal except for a few oddballs such as naked mole rats, in ants, bees, and termites queens do queenly things like produce eggs, males mate, and workers, well, work. Within the workers, different individuals often specialize on particular tasks, for example, going out and collecting food, or cleaning up the hive. This division, like the stratification of human industrialized societies, allows the colonies to be much more efficient. And the whole idea of sterile individuals that nonetheless labor for the group as a whole is a hallmark of sophisticated social organization. But what determines the destiny of any one individual?
It's arguable whether being a queen in a social insect colony is enviable or not, what with the continual egg laying and never getting outside, but the dogma used to be that queen honeybees were made, not born, via the feeding of royal jelly, a substance produced from glands in the heads of the workers that is given in lesser and greater amounts to different larval females. Adult bees, regardless of their social status, do not eat royal jelly. If you got a lot of royal jelly, the thinking went, you became a queen, while more modest amounts destined you for a short, chaste life among the colony proletariat. In the words of royalbeejelly.net, "Royal Jelly, the queen's food, makes the queen into a bigger animal with superhero powers," which I suppose is true if being capable of laying massive numbers of eggs is viewed as the insect equivalent of making yourself invisible. The association between upward mobility and royal jelly has given rise to a number of claims about the substance's ability to cure everything from asthma to wrinkles, though in a more sober moment surely someone has pointed out that bees suffer from neither.
But now it's turning out that at least for some social insects, you are not only what you eat, you are also the way you were born. In honeybees, different nutrients interact with the genome to switch some developmental pathways on and off, for a much more complex picture than had originally been supposed. In some ant species and at least one kind of termite, females bearing one version of a gene are more likely to be queens, while females with another version end up being workers. A particularly odd version of this genetic influence on caste occurs in harvester ants, in which two genetic lines coexist; queens belong to one line or the other, but workers are a cross between them. If a queen's eggs are fertilized by a male sharing her pedigree, the larvae become queens, but if the father is from the other line, the daughters become workers (recall that sons are produced only from unfertilized eggs, so they don't enter into the calculation). The difference between queens and workers can also be due not to a gene or genes being present or absent but to the regulation of those genes. A recent study of honeybees found at least two thousand genes that were present in both workers and queens were expressed differently in the brains of the two kinds of individuals, further supporting the idea that it's not just what you have but what you do with it—or what it does to you—that counts.
Queens may also specialize, with multiple reproductive females starting a nest together and then divvying up the duties like housemates, so that one goes out and collects food and the other stays home caring for the offspring. Alternatively, in the fire ant common to the southern United States and named for its painful sting, some colonies have one queen and others have two or more. The fatter queens go solo, whereas the burden is shared, literally and figuratively, in the nests ruled by multiple, lighter queens. Queen physiology, and the way the queens are treated by the workers, are both controlled by genes.
The role taken on by a worker had also been thought to be, if not diet related, at least environmentally determined, with all older worker bees, for example, doing more foraging and younger ones staying behind as "nurses." Now, however, the picture seems both more complex and more genetically determined. The age-related changes in tasks occur, to be sure, but altering the genes can change the workers' behavior, making them go out to forage at a younger age than they normally would. At the same time, foraging is influenced by social cues such as the age of other colony members and the type of pheromones given off in the hive, which in turn can feed back to the worker and change the hormones secreted inside the worker's body, further altering behavior. As in the queen-worker distinction, gene expression differs depending on the task the workers do. Hives with differences in genetic makeup also show different patterns of work. Most interesting, when a queen had mated with multiple males, the resulting blended family of workers was more efficient at making honeycomb, rearing the young, and flying off to collect pollen and nectar than were colonies started by a queen that had mated only once.
A group of scientists at the University of Sydney performed a clever experiment to examine the genetic regulation of reproduction in honeybees. Like humans, bees are affected by carbon dioxide gas, but unlike humans, queen honeybees respond to CO2 by increasing their ovary development, as if they had just mated and were getting ready to start a colony. In contrast, if a queen is removed from a hive, something the workers can detect immediately, the workers respond to the gas by suppressing their ovary development, just as if the queen were present and producing all the eggs (worker bees are able to lay eggs, although their sisters often prevent them from doing so).
The researchers, led by Graham Thompson, placed virgin queens and queenless workers in a chamber with CO2 for 10 minutes and then compared the gene expression in the bees' brains as well as their level of ovary development at intervals of several days. They examined twenty-five genes and found differences in expression in ten of them, suggesting that the bees are exquisitely sensitive to small changes in their environment and that the actions of their genes are altered accordingly.
Where did the extreme social behavior in these insects, with its self-sacrificial sterility, come from in the first place? The study of the honeybee genome, as
well as detailed information on the genes of social and nonsocial species, supports an idea that had been around for a while among entomologists: start with mothers sticking around to feed their young, and go from there, progressing from maternal care to the more generalized care of siblings. Many insects show a more modest amount of social behavior than the ants or honeybees, as I describe in the chapter on parental care; they may guard their eggs, bring food to the developing young, or join forces with other females to rear offspring collectively, and they provide good test cases for this idea. Toth, Robinson, and a group of colleagues used the common paper wasp to see if care of sisters and care of young were governed by the same genes. Although the genome for the wasps has not yet been sequenced, the scientists used an innovative technique to characterize short segments of DNA that were already known to be associated with social behavior in honeybees. Although the bees and wasps last shared a common ancestor 100 to 150 million years ago, the genetic material that was examined turns out to be amazingly unchanged.