Date Published: March 16, 2004
Publisher: Public Library of Science
Author(s): Benjamin B Normark
Abstract: Armored scale insects are unusual in that a part of their bodies is genetically distinct from the rest. This extraordinary phenomenon challenges the notion of identity.
Partial Text: 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.
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).
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.
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.
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.