I am a clone. That is, I am a colony of cells that developed from a single fertilized
egg cell. Most animals are clones like me. It is a slight oversimplification to say that
all of an animal's cells are genetically identical to each other. Some cells have
mutations. In mammals, some cells (red blood cells) lack a nuclear genome entirely. Some
cells have viruses—and when it's in a cell, a virus is basically a gene—that other cells
lack. But a typical animal is a clone in the sense that all its cells arise from that
single fertilized egg cell.
Not all animals, however, are clones. Sometimes two tiny embryos developing inside their
mother will fuse together into a single embryo and continue developing. The resulting
animal is not a clone, but a chimera: a conglomeration of two different cell lineages into
a single organism. Some species of monkeys (marmosets) typically have chimeric blood, from
having shared a blood supply with a twin in utero (Haig 1999), and rare cases of accidental
chimerism are known from many animal species (Tremblay and Caltagirone 1973; van Dijk et
al. 1996). In marine invertebrates, chimeric individuals often arise from the fusion of
individuals later in development (Buss 1987). Here I want to draw attention to a remarkable
form of chimerism found in armored scale insects. These insects (Figure 1) always develop
not from a single fertilized egg but from two genetically different cells. One of these
cells develops into a special organ (the bacteriome, which houses symbiotic bacteria) that
has a nuclear genome different from that found in the rest of the body.
Obligate chimerism—the presence of two genetically distinct cell lineages in every
individual at each life stage—is found in a few families of scale insects, but nowhere else
in nature. The avid naturalist wants to understand this sort of deep oddity for its own
sake, but such understanding might have broader implications as well. For instance,
although humans are not usually chimeras, we do have a quasi-chimeric phase in our life
cycle: pregnancy. Some diseases of pregnancy are apparently due to conflicts between the
genetically nonidentical tissues of mother and fetus (Haig 2002). And the main things that
humans eat are also quasi-chimeras: the seeds of flowering plants. In a grain of wheat, for
instance, the germ, the endosperm, and the bran have three different nuclear genomes, and
the conflicts between them may be similar in some ways to the conflicts seen in human
pregnancy (Alleman and Doctor 2000; Santiago and Goodrich 2000). Ultimately, we might learn
something about the general principles of conflict and cooperation between maternal and
embryonic tissues that govern these cases if we can understand the uniquely stable and
intimate chimerism of armored scale insects.
Two Different Cell Lineages
In all sexual animals and plants, production of an egg cell involves meiosis, the
complex cellular process (involving DNA replication, recombination, and two nuclear
divisions) whereby one diploid nucleus (with two copies of each chromosome) becomes four
genetically different haploid nuclei (each with one copy of each chromosome). Only one of
these four haploid nuclei becomes the egg cell (oocyte). In ordinary animals, the other
three nuclei (the polar bodies) degenerate—they never divide again and are lost or
destroyed—and the oocyte is the single maternal cell that (after fusion with a single
paternal cell, the spermatocyte) develops into the embryo. But in armored scales, the polar
bodies fuse together into a triploid cell (with three copies of each chromosome), and this
triploid cell also winds up in the embryo (Figure 2). The triploid cell derived from the
polar bodies fuses with one cell from the embryo to become a pentaploid cell (with five
copies of each chromosome). This pentaploid cell then proliferates to form the bacteriome
of the embryo (Brown 1965). Each cell in the bacteriome thus contains two copies of the
mother's complete genome, in addition to the same haploid paternal genome as the rest of
the embryo. In contrast, the rest of the embryo contains just one copy of half of the
mother's genome. The apparent function of the bacteriome is to house intracellular
bacteria. During embryonic development, bacteria move from the mother's bacteriome into the
cells of the embryo's bacteriome. The precise role of the bacteria is not known, but it is
thought that they synthesize essential nutrients (Tremblay 1990), as they do in scale
insects' close relatives, the aphids (Shigenobu et al. 2000).
Now the story gets even stranger. If the individual is a male, then the genetic
difference between his bacteriome and the rest of his tissues becomes even greater as he
develops. This is because most armored scale insects have an unusual genetic system called
embryonic paternal genome elimination (Herrick and Seger 1999). In males, the paternal
genome is completely eliminated from most tissues very early in development—but it is never
eliminated from the bacteriome. As a result, most of a male armored scale insect's tissues
(including his sperm) have one copy of half of the mother's genome (the same genome as the
oocyte from which he developed), but his bacteriome has two complete copies of the mother's
genome and also has a paternal genome. Thus, 60% (three of five) of the gene copies in the
male's bacteriome are absent from the rest of the male (Figure 2).
Chimerism and Sibling Rivalry
What could possibly be going on here? Why should scale insects, of all creatures, have
obligate chimerism involving activated polar bodies? Essentially, we have no idea, largely
because no one has even ventured a serious guess. When the phenomena were discovered, early
in the 20th century, the theoretical tools for making sense of them were unavailable. One
such tool is W. D. Hamilton's (1964a) theory of inclusive fitness, which holds that the
degree of cooperation between two organisms (or tissues) must depend upon their degree of
genetic relatedness. But the rise of Hamiltonian thinking coincided with the eclipse of
classical cytogenetics in favor of the molecular biology of model organisms, and these
remarkable little chimeras have languished in undeserved obscurity. Perhaps merely by
looking at them with a modern eye, we can turn up some plausible hypotheses.
Consider the special theoretical difficulty posed by chimerism between tissues derived
from the oocyte and those derived from the polar bodies ejected by it during meiosis. Two
siblings will typically exhibit some degree of sibling rivalry—their interests are not
identical. If an individual were a chimera comprising full-sibling tissues (identical
across approximately half of their genomes), there might be conflict between the two
nonidentical cell lineages, as there is between the tissues of a mother mammal and her
fetus (also identical across half of their genomes) during pregnancy (Haig 2002). This may
explain why obligate sibling chimerism never evolves (except perhaps in the very limited
case of blood cells between sibling marmosets). But the problem of cooperation between
tissues that derive from the oocyte and those that derive from the polar bodies is, if
anything, even greater. The oocyte and the polar bodies are
less closely related than two siblings would be, because the polar bodies
are enriched for chromosome regions
not present in the oocyte.
If there were no crossing over between homologous chromosomes during meiosis, then the
first meiotic division would consistently separate the chromosomes derived from the
mother's mother from the chromosomes derived from the mother's father, producing two cells
that are not related to each other
at all (or, more precisely, exactly as closely related to each other as
the mother's mother was to the mother's father). Crossing over prevents this, creating a
mosaic of related and unrelated chromosome regions between the products of the first
meiotic division and uncertain relationships between the final four meiotic products.
Nonetheless, the consistently depressed relatedness between the oocyte and the polar bodies
may help to explain why polar bodies are almost always eliminated—sibling rivalry might be
even greater if some siblings were derived from each other's polar bodies.
Towards an Explanation
So how and why did two families of scale insects tame and domesticate their potentially
fractious polar bodies, rather than killing them like normal animals do? There are at least
three lines of thinking that seem promising for unraveling this mystery.
Histological eusociality and relatedness.
There are interesting parallels between, on the one hand, the chimerism seen in
armored scale insects and, on the other hand, the eusociality (true sociality) seen in
ants and honeybees. In ants and honeybees, sterile individuals (workers) provide
nutrition to their potentially fertile siblings. In armored scale insects, a genetically
distinct but ultimately sterile cell lineage (the bacteriome) provides nutrition to its
potentially fertile “sibling” cell lineage (the rest of the scale insect)—though, of
course, polar body-derived cells are “sibling” in a strange special sense. Like ants and
bees, armored scale insects are effectively haplodiploid: males transmit only the
chromosomes they inherited from their mother, and all of a male's sperm are identical to
each other. This “clonality” of sperm boosts the relatedness between sisters, and
Hamilton (1964b) pointed out that this high relatedness can explain the high level of
cooperation between sisters seen in eusocial ants and honeybees. High levels of
cooperation between sisters have since been found in haplodiploid thrips as well (Crespi
1992). It is tempting to speculate that similar explanations can be applied to
“histological eusociality” seen in the cooperation between related tissues in scale
insects.
This temptation increases when we consider another case from the old cytogenetics
literature of apparent histological eusociality, though not of true permanent chimerism.
This occurs in a few families of parasitoid wasps (Tremblay and Caltagirone 1973; Strand
and Grbic 1997), in which cells derived from polar bodies form a membrane around the
yolkless egg that is deposited in the wasp's insect host (which is often a scale
insect!). Similar to the worker ant and the scale insect bacteriome, this membrane is
thought to mediate nutrition of the developing embryo, and, similar to ants, honeybees,
and scale insects, these wasps are haplodiploid.
But although it is tempting to conclude that haplodiploidy plays the same role in
promoting histological eusociality as it does in promoting organismal eusociality, the
temptation should probably be resisted. In the case of the parasitoid wasps, the polar
body-derived tissue has no paternal genome, so the clonality of sperm cannot boost its
relatedness to anything. In the case of armored scale insect chimerism, the bacteriome
does have a copy of the paternal genome, and that copy is identical to the paternal
genome in the rest of the embryo, so in that sense the two tissues do have a high
relatedness similar to the high relatedness of full siblings under haplodiploidy. But the
scale insect bacteriome gets its copy of the paternal genome directly from the embryo, so
the clonality of sperm (the source of elevated relatedness between haplodiploid sisters)
apparently has nothing to do with it. Some other explanation is probably needed.
Maternal interests.
Note that, whatever the relationship between the polar body-derived tissues and the
rest of the insect, the polar bodies contain the mother's complete genome. And while your
polar bodies may be
less related to you, on average, than your siblings are, they are
more related to your siblings (and, of course, to your mother) than
they are to you! Perhaps the polar bodies function to somehow enforce some maternal or
family interest, nipping in the bud some sibling rivalry that would otherwise suppress
the family's fitness. In haplodiploid groups, females are more closely related to their
full sisters (with whom they share three-quarters of their gene copies) than to their
brothers (with whom they share only one-quarter of their gene copies). So if there is
competition between siblings for resources, females are expected to behave more
antagonistically towards brothers and more cooperatively towards sisters. In contrast, a
female is equally related to a son as she is to a daughter (each carries half of her gene
copies). These asymmetries in relatedness lead to struggles in haplodiploid social
groups, with a mother seeking to direct more resources towards sons and with sisters
seeking to direct more resources away from their brothers and towards each other (Seger
and Stubblefield 2002).
It is difficult to see how such a struggle might play itself out in scale insects,
which are hardly social insects. The only motile stage in a female's life is the first
instar (“crawler”), after which she settles in one spot permanently. The male is slightly
more mobile, having a motile (usually winged) adult form. Nonetheless, (1) the low
motility of females, and the fact that they live mostly on long-lived woody plants, means
that maternal kin may interact over long timescales, as in social insects; (2) some scale
insects appear to make relatively sophisticated social decisions about where to settle,
settling nearer to (and thus possibly competing more closely with) non-kin than kin
(Kasuya 2000); (3) although most scale insects use phloem sap, an almost inexhaustible
resource, armored scales use parenchyma tissues (Rosen 1990), which may be locally
exhausted, and therefore may compete against neighbors for food. Thus, it is conceivable
that females may compete against brothers and sisters for resources, that they may make
decisions that affect the intensity of that competition, and that such decisions may have
different optima from the perspectives of maternal versus paternal genes. Possibly, the
presence of a massive contingent of maternal genes (a double dose of the complete
maternal genome) in a nutritionally significant tissue like the bacteriome might somehow
affect such decisions in ways favorable to maternal interests. Proximal mechanisms might
include effects on signals or perceptions related to relatedness, gender, site quality,
or satiety.
Similar manipulation of intersibling interaction might be going on in the case of the
parasitoid wasps that have polar body-derived membranes around their eggs. Sometimes
these wasps lay a single unfertilized (male) egg and a single fertilized (female) egg
into the same host. Both eggs divide to form embryos, which divide into a clone of many
embryos. Some of the embryos become sterile “precocious” larvae that can apparently
attack other larvae trying to use the same host—including, potentially, their own
siblings (Ode and Hunter 2002). Here is a situation in which the polar body genes (in the
membranes surrounding the proliferating embryos) might have very different selective
optima for levels of between-sibling aggressiveness—and even for rates of
development—than the genes in the embryos they surround, and (because they apparently
mediate the nutrition of the embryos) they might be able to influence how the embryos
develop.
Gender crypsis.
The endosymbiotic bacteria that dwell in the scale insects' bacteriomes are maternally
inherited. Thus, from the perspective of the bacteria, male insects are deadends. Many
maternally inherited bacteria have evolved to manipulate the hosts' genetic system for
their own advantage. Some bacterial lineages induce parthenogenesis or feminize males.
Bacteria may even evolve to suicidally kill male embryos that they find themselves in, if
the death of the male frees up resources that his sisters can use (Majerus 2003). In
order to do this, bacteria must respond to some cue that indicates the gender of the
individual they are in. Potentially, a host could evolve resistance to such manipulation
by maternally inherited bacteria by depriving those bacteria of cues indicating gender.
In armored scales, the bacteriome has exactly the same genome (two complete copies of the
mother's diploid genome and one complete copy of the father's genome) in all full
siblings, whether they are male or female, and the same is usually true in mealybugs.
This might explain why the bacteriome is the only tissue in which the father's genome
remains present and active in both males and females.
Prospects
Scale insects and their bacteriomes challenge our notion of what an individual is. Is a
scale insect's bacteriome a kind of sibling? Is it half sibling, half self? Is it a sterile
slave, under control? Is it an extension of the mother, exerting control? In all other
organisms, chimeras are temporary and unstable. How have scale insects suppressed the
conflicts that normally tear chimeras apart? To approach such questions, we'll have to
revive the empirical study of scale insect bacteriomes, combining approaches from recent
studies of aphid bacteriomes (Braendle et al. 2003) and of human pregnancy (Haig 2002). We
can better understand the nature of genetic conflicts in scale insects by studies of the
genetic structure of scale insect populations, together with studies of sex ratio variation
and the proximate mechanisms of sex determination. For simplicity, I have described only
the most common of the huge variety of very different scale insect genetic systems and
modes of bacteriome development (Tremblay 1977, 1990; Nur 1980). This diversity (greater
than for the comparable cases of mammalian placentas and flowering-plant endosperms) means
there is a huge scope for comparative ecological and genetic studies that could help
elucidate general principles. The study of truly strange creatures can tell us what kinds
of things are possible. That's why we will be so interested in any life found on another
planet and why, in the meantime, we should take a close look at scale insects.
