The Sex Lives of Scales
Normark, Benjamin B., Natural History
Scale insects have evolved one bizarre genetic system after another. The author argues that they are caught in a game of cat and mouse with internal, symbiotic bacteria, which has unleashed genetic bedlam.
Bird-of-paradise flies-which are not really flies at all, but members of the sca/e-insect family Margarodidae-are a rarely seen kind of scale insect: mature males. Here are two of them on one enormous female. On reaching adulthood, the typical male scale insect lives just a few days. The genetic system of many margarodids, unlike that of most scale insects, is "conventional": both mother and father contribute half of their genome to each of their offspring.
Female scale insects of the family Ortheziidae have sunk their mouth parts into a leaf, where they will stay, feeding on the plant sap, for much of their sedentary, parasitic lives. The sap gives the insects access to a practically unlimited supply of sugars.
If you were in the backyard this summer, watering your lilacs or checking your apple trees for pests, you may have noticed that the plants were afflicted with little bumps on the leaves or bark, coming down with what looks like nothing so much as a case of botanical acne. Many people are surprised the first time they find out that each bump is actually an animal: a scale insect. Many scale insects look more like mollusks or turtles than like beetles or cicadas-the bodies aren't obviously segmented into head, thorax, and abdomen, and the six legs and four wings typical of most insects are nowhere to be seen. Yet those little bumps are indeed insects, related to aphids, whiteflies, and jumping plant lice.
All scale insects are parasites of plants, and the insects' habit of sucking the sap out of plants makes them generally disliked by farmers and gardeners. In a sense, scale insects have taken the parasitic lifestyle to the farthest extreme: the females of some lineages have evolved into legless, eyeless blobs that are permanently attached to their hosts.
Even among the most casual keepers of houseplants, most people's reactions to scale insects run from mere distaste to full-blown disgust. But if you take the trouble to look beneath the surface, scale insects turn out to be quite fascinating creatures. In particular, the laws of genetics-the rules that describe how the DNA of one generation is passed on to the next-seem to have gone totally haywire as the scale insects have evolved. The group encompasses more weird variations on the laws of genetics than does any other group of animals.
But surely, weirdness is in the eye of the beholder. Just because mammals don't have such varied genetic systems, is that grounds for calling scale insects strange? Well, consider this: From a genetic point of view, a typical multicellular animal is an assemblage of cells that are nearly all clones, or genetically identical to one another. Yet in most species of scale insects, not all the cells of an individual get the same genes from the insect's mother. Furthermore, scale-insect fathers vary widely in the genes they contribute (or, often, do not contribute) to their sons: In some species the males are the product of asexual reproduction and have no father at all. In other species the males have fathers, but all the chromosomes they get from the fathers are deactivated. In still other species the chromosomes from the fathers are present in some cells but not in others.
Much of this is not news. Thanks to the pioneering work of the American geneticist Sally HughesSchrader and others, many of these facts have been known since the 1920s. Only recently, however, has evolutionary theory begun to catch up with those facts, and to describe them with concepts powerful enough to explain the data in a satisfactory way. Only now do biologists have an inkling about what might be causing the apparently staid world of blobby little plant parasites to be convulsed by so many sexual revolutions.
It is not readily apparent why scale insects, of all life-forms, should exhibit such a diversity of genetic systems. After all, other, related groups of insects show nothing approaching the same degree of variation in their genetic machinery. Particularly puzzling is the scale insects' patrilineal inheritance. Why is it so frequently sabotaged? Those are unsolved mysteries, but quite recently, suspicion has fallen on some unusual suspects: bacteria.
The bacteria in question are not disease organisms; rather, they live symbiotically with their scale-insect hosts, a relationship that is vital to both organisms. The bacteria derive their very livelihoods from the insects, and the insects in turn depend on their resident bacteria for help surviving on a diet that is conspicuously lacking in protein. Yet despite the aid the bacteria render the insects, the bacteria may still interfere with the insects' genetics. To understand why, it is helpful to understand something about the lives of scale insects and the bacteria that live inside them.
Immature scale insects do not look much like the little bumps on plants that many of them are destined to become. During the first, or "crawler," stage in the life cycles of scale insects, the animal looks a bit like a small potato bug. The typical crawler, after hatching from its egg, walks a short distance on its natal plant, then inserts its mouthparts into the plant and becomes immobile. There the insect generally remains through subsequent immature stages, regardless of its sex.
The life and form of an adult scale insect, however, depends heavily on its sex. The males are not exceptionally strange-looking insects. Most people would probably mistake them for small flies, such as gnats or midges. Their strangeness becomes apparent only when you look more closely: they have only two wings (like true flies but unlike almost all other insects) and simple, rather than compound, eyes, and they always lack functional mouthparts; grown males never feed. Much more unusual looking are the adult females; they are the bumps you may have seen on your houseplants. Adult females never have wings, and they often lack legs and eyes as well; for antennae, many possess only the tiniest nubs.
All scale insects feed by sucking up plant juices, and most feed directly on the phloem sap of longlived trees and bushes. Phloem sap is typically rich in sugar, and most scale insects ingest far more sugar than they can use; they simply defecate the excess. The sugary excrement, called honeydew, is often consumed by ants. Sometimes it is even consumed by people, particularly in arid regions where evaporation of dripping honeydew can leave a solid sugary residue called manna. The manna referred to in the uible, in Exodus 16:14, seems to have been the dried excrement of Trabutina mannipara, a scale insect that feeds on tamarisk trees.
But even thuugh plant sap is rich in sugar, it is poor in other nutrients, particularly amino acids. Partly on the basis of studies of scale insects' better-known relatives, the aphids, one can infer that the symbiotic bacteria living inside scale insects manufacture essential amino acids lacking in the insects diet.
The essential bacteria in scale insects (and aphids) live inside the cells of an organ called the bacteriome. (The location and size of the organ varies, depending on the species of insect.) Each scale insect inherits the bacteria in its bacteriome from its mother. When the adult female scale insect is provisioning its eggs, cells from the mother's bacteriome discharge bacteria into the yolk. No scale insect gets bacteria from its father. Thus, the bacteria in the cells of male insects are effectively sterile; in an evolutionary sense, they are as good as dead.
John H. Werren, a biologist at the University of Rochester in New ^brk, has described how certain insects' maternally inherited bacteria rebel against the inglorious destiny of winding up in a male [see "Invation of the Gender benders February 2003]: they kill the male in which they live. Although that act is suicidal (the bacteria in the male they kill die along with the insect) and so might seem gratuitous, it is not pointless. Each bacterium in an embryo is practically identical to the bacteria that populate other individuals in the same insect brood. Moreover, if the goal of each bacterium is to pass its DNA on to future generations of bacteria, what is good for one bacterium is good for the rest. Thus a bacterium's suicide by killing its male host makes evolutionary sense, as long as such a killing helps the bacterium's kin to prosper.
It's easy to imagine how that circumstance could arise. For example, if female scale insects harboring bacteria were forced to compete with their brothers, the competition could very well be detrimental to the bacteria in the females. But from the perspective of the bacterial genome, the bacteria in the male insects are expendable, since they are guaranteed never to reproduce. Their suicidal killing of the males, though, gives the female insects (and their bacteria) freer run of available resources. That cold calculation holds particularly true among scale insects, partly because their host plants live so long, and partly because the insects move around so little. There is plenty of time in the life span of a longlived plant for the insects that live on it to produce enormous extended families. Moreover, the females' sedentary nature keeps close kin, and their closely related bacteria, ou a single host plant. Insects in such close proximity are particularly likely to compete with one another for hiding places or other resources, and the genes of their resident bacteria are so similar that the common bacterial genome is particularly likely to benefit if male insects are killed.
Thus one might expect a kind of struggle between scale insects and their bacteria. On the one hand, the scale insects are under pressure to keep their sons alive. On the other hand, the bacteria can benefit by killing males and only males. (Killing a female host insect is decidedly against the interests of the bacteria, since they cannot spread beyond their host except through her egg cells.) For the bacteria to kill males and not females, they must be able to distinguish male from female hosts, and it is possible they detect the sex of their host by interacting with their host's chromosomes. (Males often have a deactivated set of chromosomes or otherwise differ genetically from the females.) How could this struggle escalate? One way is that the scale insects might "fool" the bacteria into not killing males by keeping the bacteria inside cells that lack any clear sign about the sex of the host insect. Remarkably, that is exactly what many scale insects have evolved to do.
To understand how a scale insect might pull off that bit of legerdemain, it is helpful to start with some of the most ancient groups of scale insects. Their genetic characteristics are the most similar, among the scale insects living today, to those of the superfamily's long-dead ancestors. Each cell in each insect has a full set of functional chromosomes, one set from its father and one set from its mother. Such groups include the scale-insect fami lies Ortheziidae and Phenacoleachiidae, and many branches of the family Margarodidae (but not all branches; even within families, the scale insects have more genetic systems than I have space to discuss).
Many ortheziids, as they are known, live in soil or leaf litter and feed on fungi, lichens, mosses, and plant roots. Margarodids comprise a diverse group, found on all parts of plants; the family includes the largest and most striking scale insects, such as Australia's bird-of-paradise flies [see photograph at top left on page 38]. The phenacoleachiids comprise a "living fossil" group; today only two species exist, and they occur on the South Island of New Zealand and on adjacent islands. All three families include scale insects that are relatively "normal" insects-not very normal; they are scale insects, after all. But they have more in common with other insects than most scale insects do. Adult females have functional legs and eyes. The sex chromosomes are distributed in a reasonably ordinary way: as in aphids, males have one sex chromosome and females have two. And the entire insect has the same genome in every cell, including the cells of the insect's bacteriome.
But genetic simplicity is rare for the scale insects. Consider the family Putoidae. Putoids typically occur on the foliage or roots of woody plants in the southwestern United States. They, like their ancient relatives, look fairly "primitive": adult females retain their eyes and legs, and they can walk. Putoids also have the ancestral number of sex chromosomes: one for males, two for females. Yet according to the German biologist Paul Buchner, a microscopist and pioneer in the study of symbiosis, putoid bacteriomes are deeply strange.
The putoids, unlike other scale insects, are apparently not content to simply insert bacteria from the mother's bacteriome cells into the yolk of the fertilized egg. Instead, when the essential but potentially troublesome bacteria move from the mother putoid to her offspring, entire cells from the mother's bacteriome move with them, taking up residence to form the bacteriome of the embryo.
It is hard to overstate how weird that process seems to a geneticist. (It is so weird, in fact, that some biologists think Buchner must have gotten it wrong.) For the most part, we animals grow our own organs. Each of my organs is genetically "me." Putoids are the only animals I know of that appear to import one of their organs and then pass it down from mother to offspring much the way people pass along the family china or silverware. Normally an animal's germ line-the cells that give rise to gametes-is the only cell line that is, potentially, immortal: the only cell line inherited by offspring. But in putoids the cells of the bacteriome are equally immortal, yet they are independent of the germ line and not even closely related to it.
Biologists still do not really know what originally led to the evolution of such a wholesale migration of maternal cells (though those cells might play a role in provisioning the embryo). But one effect of the migration is that bacteriome cells in males are genetically identical to the bacteriome cells in their sisters. That may make it hard for the bacteria to identify the sex of their host insectand thus too risky to their own genetic well-being to kill their hosts at all.
Two other families of scale insects form their bacteriomes in bizarre ways. One is the family Pseudococcidae, another ancient, primitivelooking group whose females retain their legs. Pseudococcids are commonly known as mealybugs, a name referring to a coating of fine wax on their bodies that makes them look as though they had been rolled in flour. The other family with extraordinary bacteriomes is Diaspididae, the armored scale insects. Whereas mealybugs retain many of their ancestral characteristics-like legsthe armored scales lie at the opposite extreme in the morphological evolution of scale insects. Adult female armored scales lack legs and eyes, and they barely have antennae. Taken together, the mealybug and armored-scale families encompass more than 4,300 species, some 60 percent of all scaleinsect species. Yet despite their clearly visible differences, the two families have each evolved, apparently quite independently, similar yet highly exotic systems of bacteriome development.
Most animal cells, including the cells of the germ line, have two copies of each chromosome: one from the animal's mother, the other from the father. Egg and sperm cells, though, which are derived from germ-line cells, each have only one copy of each chromosome. In particular, to make an egg cell, a female animal must throw away one copy of each chromosome. That is accomplished, among other things, during a process called meiosis.
Meiosis actually starts with the duplication of every chromosome in the germ-line cell, followed by two divisions of the nucleus. Thus, one nucleus with two copies of each chromosome first gives rise to a nucleus with four copies of the chromosome. Then that nucleus splits into two nuclei, each with two copies of each chromosome; those nuclei in turn split into four nuclei, each with one copy of each chromosome. One of those four becomes the egg nucleus; the other three are called polar bodies.
In most organisms, the polar bodies are simply destroyed; only in a few cases do they avoid destruction. One such case is prominent and important: the nutritive tissue packaged into the seeds of flowering plants contains polar-body genomes. But even in that case, the polar bodies don't wind up in the embryo of the plant. The only case for which polar bodies from the mother are actually incorporated into the body of her offspring occurs in scale insects. And where the polar-body genomes wind up is, as you might have guessed, the bacteriome.
After a mealybug or an armored scale female forms her three polar bodies, the three fuse into a single nucleus; that nucleus thereby contains three full copies of the mothers genome, the three "extras" left over from meiosis. The nucleus is engulfed by the developing embryo, and then fuses with a cell from the embryo to form a cell with five copies of each chromosome. That cell proliferates to form the bacteriome [see illustration on page 41].
No one really knows why polar bodies survive destruction in those scale insects, why they fuse with a cell from the embryo, or why they then form the bacteriome. But one consequence is that the genomes of bacteriome cells of males are identical to those of their sisters. The participation of polar bodies in forming the bacteriome, like the inheritance of the maternal bacteriome in putoids, would seem to make it hard for the bacteria to selectively kill males.
Bacteriome formation is probably the strangest aspect of scale-insect genetics, and the one in which bacteria are most obviously involved. But a close runner-up for strangeness is the genetics of male scale insects. The male scale is originally endowed with two sets of chromosomes, but the ones from his father typically form an inactive clump in every cell. They never direct the synthesis of proteins, and they are discarded from the germ line when sperm are made. Hence each sperm a male produces has exactly the same genome-the genes he got from his mother. That, of course, is in marked contrast with most male organisms, including men, who each produce a diversity of genetically unique sperm. It also differs sharply from the genetics of the female scale, which has an active paternal genome and apparently produces genetically diverse eggs.
In some species of armored scale insects, the father's genes are not merely deactivated; rather, they are completely eliminated from cells early in embryonic development. In a few scale insect groups the father's genes have become reactivated, and there is one tissue in most scale insect speciesthose unusual bacteriomes of mealybugs and armored scale insects-that retains active paternal genes, though even there they are greatly outnumbered by maternal ones.
Geneticists have long wondered how genetic systems involving the deactivation or destruction of the paternal genome could ever have arisen, since the first males to completely lack a paternal genome probably did not survive. But the recent focus on the bacterial genome gives a possible answer to the puzzle. Symbiotic bacteria had both the motive and the opportunity to destroy the paternal genome in males, particularly if they could thereby kill the male. But the destruction of paternal genomes in sons could also be a phenomenon that the females have turned to their own advantage. In most genetic systems, such as the mammalian one, a typical male endows his offspring, on average, with half the genes he received from his mother and half the genes he received from his father. In contrast, a male armored scale or mealybug that manages to survive the depredations of the bacteria is twice as efficient as the typical mammalian male at transmitting his mother's genes. After all, the male scale insect's cells have basically jettisoned the genes the male received from his father. Thus the destruction of the paternal genome may have begun as a means of male-killing by bacteria. But over evolutionary time it may have been co-opted by females as a way to spread their own genes at the expense of the genes of their mates.
The ongoing partnership between scale insects and their bacteria is evidently a stormy one. Their conflict and its shifting tactics could well be what drive the dynamic evolution of the scale insects' genetic systems. But no one knows for sure. To find out, new generations of naturalists will need to explore the field, people who are subtle enough to resist the allure of prettier creatures and delve into the deep enigmas that are scale insects.
Female putoid scale insect depends, as do other scale insects, on symbiotic bacteria for nutritional aid. In putoids, the bacteriome cells, where the bacteria reside, appear to be passed down intact from mothers to offspring. That may make it more difficult for the bacteria to develop a male-killing habit, because they are always insulated from genetically male tissues and so may be unable to distinguish between male and female hosts.
Both male and female armored scale insects and mealybugs (a) host bacteria within the cells of an organ called the bacteriome. A male produces sperm (b) that carries only his mother's genome; a female produces an egg and three polar bodies (c) with a mixture of chromosomes from both her parents. The union of DNA from both egg and sperm form a zygotic nucleus within the egg cell, constituting a new genetic individual; the egg in these two groups of scale insects also hosts symbiotic bacteria in the yolk. The chromosomes from both sperm and egg in each new individual are "imprinted" as paternal (blue) or maternal (pink) in source (d). As the nucleus begins to divide and the embryo grows (e), the three polar bodies fuse with each other and then fuse with one of the cells of the embryo (f). The resulting cell has four copies of the maternal chromosome and one copy of the chromosome of the paternal grandmother. That cell becomes the parent cell of the new scale insect's bacteriome (g), to which the bacteria from the egg yolk then migrate.
Sex (or the lack of it) among scale insects gives rise to a bewildering variety of systems of genetic inheritance. Four of them are detailed at right, based on the same scheme as in the diagram on the preceding page. Parthenogenesis, or the virgin birth of females, takes several forms, but in automixis, the form pictured here, the female egg fuses with a polar body instead of with a sperm. In diplodiploidy, which is also the human genetic system, both the mother and the father contribute one copy of each of their chromosomes to each offspring, which can be either male or female. In paternal genome elimination, the most common method of genetic inheritance in scale insects, the male can pass along only those genes he received from his mother. In arrhenotoky, the male develops from unfertilized eggs. Those males mate with females, and every egg that gets fertilized develops into a female.
Tuliptree scale insects are members of the soft-scale family, but they do a remarkable imitation of a cluster of arboreal turtles. Many soft-scale species engage in paternal genome elimination: the genome of the father is disabled or eliminated in male progeny. Some species have done away with males altogether.
Black thread scales, here shown infesting a leaf, are members of the armored scale family. Although many armored scales reproduce sexually by paternal genome elimination, black thread scales have eliminated fathers-in fact, all males-completely.
Female margarodid scale insect…
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Publication information: Article title: The Sex Lives of Scales. Contributors: Normark, Benjamin B. - Author. Magazine title: Natural History. Volume: 113. Issue: 7 Publication date: September 2004. Page number: 38+. © American Museum of Natural History Dec 2008/Jan 2009. Provided by ProQuest LLC. All Rights Reserved.