The Extended Phenotype: The Long Reach of the Gene (Popular Science) (46 page)

The first dimension of my classification has already been stressed. It concerns the degree of similarity or difference in the methods of egress from hosts, and propagation of host genes and parasite genes. At one extreme will be parasites that use the host’s propagules for their own reproduction. For such parasites an optimum host phenotype from the parasite’s point of view is likely to coincide with the optimum from the point of view of the host’s own genes. This is not to say that the host genes would not ‘prefer’ to be rid
of the parasite altogether. But both have an interest in mass-producing the same propagules, and both have an interest in developing a phenotype that is good for mass-producing those same propagules: the right beak length, wing shape, courtship behaviour, clutch size, etc., down to minute details of all aspects of the phenotype.

At the other extreme will be parasites whose genes are passed on not in the host’s reproductive propagules but, say, in the host’s exhaled breath, or in the host’s dead body. In these cases the optimum host phenotype from the parasite genes’ point of view is likely to be very different from the optimum host phenotype from the host genes’ point of view. The phenotype which emerges will be a compromise. This, then, is one dimension of classification of host–parasite relationships. I shall call it the dimension of ‘propagule overlap’.

A second dimension of classification concerns the time of action of parasite genes during host development. A gene, whether a host gene or a parasite gene, can exert a more fundamental influence on the final host phenotype if it acts early in the development of the host embryo than if it acts late. A radical change such as the development of two heads could be achieved by a single mutation (in host or parasite genome) provided the mutation acted sufficiently early in the embryonic development of the host. A late-acting mutant (again, in host or parasite genome)—a mutant that does not begin to act until the host body has reached adulthood—is likely to have only a small effect, since the general architecture of the body will, by then, have been laid down. Therefore a parasite that enters its host after the host has reached adulthood is less likely to have a radical effect on the host’s phenotype than a parasite that gets in early. There are notable exceptions, however, such as the parasitic castration of crustacea already mentioned.

My third dimension of classification of host–parasite relations concerns the continuum from what may be called close intimacy to action at a distance. All genes exert power primarily by serving as templates for the synthesis of proteins. The locus of primary gene power is, therefore, the cell, in particular the cytoplasm surrounding the nucleus in which the gene sits. Messenger RNA streams through the nuclear membrane and mediates genetic control over cytoplasmic biochemistry. The phenotypic expression of a gene is then, in the first place, its influence on cytoplasmic biochemistry. In its turn, this influences the form and structure of the whole cell, and the nature of its chemical and physical interactions with neighbouring cells. This affects the build-up of multicellular tissues, and in turn the differentiation of a variety of tissues in the developing body. Finally emerge the attributes of the whole organism that gross anatomists and ethologists identify at their level as phenotypic expressions of genes.

Where parasite genes exert shared power with host genes over the same host phenotypic characteristic, the confluence of the two powers may occur
at any stage in the chain just described. Snail genes, and the genes of the fluke that parasitizes the snail, exert their power separately from each other at the cellular and even the tissue level. They influence the cytoplasmic chemistry of their respective cells separately, because they do not share cells. They influence tissue formation separately, because snail tissues are not intimately infiltrated by fluke tissues in the way that, say, the algal and fungal tissues of a lichen are intimate. Snail genes and fluke genes influence the development of organ systems, indeed of whole organisms, separately, because all the fluke cells are gathered together in one mass rather than being interspersed among snail cells. If fluke genes influence snail shell thickness, they do so by first collaborating with other fluke genes to make a whole fluke.

Other parasites and symbionts more intimately infiltrate the systems of the host. At the extreme are the plasmids and other fragments of DNA which, as we saw in
Chapter 9
, literally insert themselves in the host chromosomes. It is impossible to imagine a more intimate parasite. ‘Selfish DNA’ itself is not more intimate, and indeed we may never know how many of our genes, whether junk’ or ‘useful’, originated as inserted plasmids. It seems to follow from the thesis of this book that there is no important distinction between our ‘own’ genes and parasitic or symbiotic insertion sequences. Whether they conflict or cooperate will depend not on their historical origins but on the circumstances from which they stand to gain now.

Viruses have their own protein jacket, but they insert their DNA into the host’s cell. They are therefore in a position to influence the cellular chemistry of the host at an intimate level, if not quite such an intimate level as an insertion sequence in the host chromosome. Intracellular parasites in the cytoplasm, too, may be presumed to be in a position to exert considerable power over host phenotypes.

Some parasites do not infiltrate the host at the cellular level, but at the tissue level. Examples are
Sacculina
, and many fungal and plant parasites, where parasite cells and host cells are distinct, but where the parasite invades the host’s tissues by means of an intricate and finely divided root system. The separate cells of parasitic bacteria and protozoa may infiltrate the host tissues with similarly comprehensive intimacy. To a slightly lesser extent than a cell parasite, such a ‘tissue parasite’ is in a strong position to influence organ development and gross phenotypic form and behaviour. Other internal parasites, such as the flukes we have been discussing, do not mix their tissues with those of the host, but keep their tissues to themselves and exert power only at the level of the whole organism.

But we have not yet reached the end of our continuum of proximity. Not all parasites live physically inside their hosts. They may even seldom come into contact with their hosts. A cuckoo is a parasite in very much the same way as a fluke. Both are whole-organism parasites rather than tissue parasites
or cell parasites. If fluke genes can be said to have phenotypic expression in a snail’s body, there is no sensible reason why cuckoo genes should not be said to have phenotypic expression in a reed warbler’s body. The difference is a practical one, and a rather smaller one than the difference between, say, a cellular parasite and a tissue parasite. The practical difference is that the cuckoo does not live inside the reed warbler’s body, so has less opportunity for manipulating the host’s internal biochemistry. It has to rely on other media for its manipulation, for instance sound waves and light waves. As discussed in
Chapter 4
, it uses a supernormally bright gape to inject its control into the reed warbler’s nervous system via the eyes. It uses an especially loud begging cry to control the reed warbler’s nervous system via the ears. Cuckoo genes, in exerting their developmental power over host phenotypes, have to rely on action at a distance.

The concept of genetic action at a distance pushes our idea of the extended phenotype out to its logical culmination. That is where we must go in the next chapter.

Snail shells coil either to the right or to the left. Usually all individuals in one species coil the same way, but a few polymorphic species are to be found. In the Pacific island land snail
Partula suturalis
some local populations are right-handed, others are left-handed, and others are mixed in various proportions. It is therefore possible to study the genetics of directionality of coiling (Murray & Clarke 1966). When snails from right-handed populations were crossed with snails from left-handed populations, every offspring coiled the same way as its ‘mother’ (the parent that provided the egg: the snails are hermaphrodites). This might be thought to indicate a non-genetic maternal influence. But when Murray and Clarke crossed F1 snails with each other they obtained a curious result. All the progeny were left-handed, regardless of the direction of coiling of either parent. Their interpretation of the results is that coiling is genetically determined, with left-handedness dominant to right-handedness, but that an animal’s phenotype is controlled not by its own genotype but by its mother’s genotype. Thus the F1 individuals displayed the phenotypes dictated by their mothers’ genotypes, although all contained the same heterozygous genotypes since they were produced by mating two pure strains. Similarly, the F2 progeny of F1 matings all displayed the phenotype appropriate to an F1 genotype—left-handed since that is dominant and the F1 genotype was heterozygous. The underlying genotypes of the F2 generation presumably segregated in classic 3:1 Mendelian fashion, but this did not show itself in their phenotypes. It would have shown itself in the phenotypes of their progeny.

Note that it is the mother’s genotype, not her phenotype, which controls her offspring’s phenotype. The F1 individuals themselves were left-handed or right-handed in equal proportion, yet all had the same heterozygous genotype, and all therefore produced left-handed offspring. A similar effect had been obtained earlier in the freshwater snail
Limnaea peregra
, though in that case right-handedness was dominant. Other such ‘maternal effects’ have
long been known to geneticists. As Ford (1975) put it, ‘We have here simple Mendelian inheritance the expression of which is constantly delayed one generation.’ The phenomenon perhaps arises when the embryological event determining the phenotypic trait occurs so early in development as to be influenced by maternal messenger RNA from the egg cytoplasm, before the zygote has begun to manufacture its own messenger RNA. The direction of coiling in snails is determined by the initial direction of spiral cleavage, which occurs before the embryo’s own DNA has begun to work (Cohen 1977).

This kind of effect provides a special opportunity for the kind of maternal manipulation of offspring that we discussed in
Chapter 4
. More generally, it is a special example of genetic ‘action at a distance’. It illustrates, in a particularly clear and simple manner, that the power of a gene may extend beyond the boundaries of the body in whose cells it sits (Haldane 1932b). We cannot hope that all genetic action at a distance will reveal itself in so elegant a Mendelian manner as in the case of the snails. Just as, in conventional genetics, the Mendelian major genes of the schoolroom are the tip of the iceberg of reality, so we may make conjectures about a polygenic ‘extended genetics’, a genetics in which action at a distance is rife but in which the effects of the genes are complex and interacting, and therefore difficult to sort out. Again as in conventional genetics, we do not necessarily have to do genetic experiments in order to infer the presence of genetic influence on variation. Once we have satisfied ourselves that a given characteristic is a Darwinian adaptation this, in itself, is tantamount to satisfying ourselves that variation in that character must at one time have had a genetic basis. If it had not, selection could not have preserved the advantageous adaptation in the population.

One phenomenon that looks like an adaptation and which, in some sense, involves action at a distance, is the ‘Bruce Effect’. A female mouse who has just been inseminated by one male has her pregnancy blocked by exposure to chemical influence from a second male. The effect seems also to occur in a variety of species of mice and voles in nature. Schwagmeyer (1980) considers three main hypotheses of the adaptive significance of the Bruce Effect, but for the sake of argument I shall not, here, advocate the hypothesis that Schwagmeyer attributes to me—that the Bruce Effect represents a kind of female adaptation. Instead I shall look at it from the male point of view, and simply assume that the second male benefits himself by preventing the female’s pregnancy, thereby eliminating the offspring of a male rival, while at the same time bringing the female quickly into oestrus so that he can mate with her himself.

I have expressed the hypothesis in the language of
Chapter 4
, the language of individual manipulation. But it can equally well be expressed in the language of the extended phenotype and genetic action at a distance. Genes
in male mice have phenotypic expression in female bodies, in just the same sense as genes in mother snails have phenotypic expression in the bodies of their children. In the snail case, the medium of the action at a distance was assumed to be maternal messenger RNA. In the mouse case it is apparently a male pheromone. My thesis is that the difference between the two cases is not a fundamental one.

Consider how an ‘extended geneticist’ might talk about the genetical evolution of the Bruce Effect. A mutant gene arose which, when present in the body of a male mouse, had phenotypic expression in the bodies of female mice with whom he came in contact. The route of action of the gene on its final phenotype was long and complex, but not noticeably more so than routes of genetic action within bodies customarily are. In conventional within-body genetics, the chain of causation leading from gene to observed phenotype may have many links. The first link is always RNA, the second is protein. A biochemist may detect the phenotype that interests him at this second link stage. Physiologists or anatomists will not pick up the phenotype that interests them until more stages have been passed. They will not concern themselves with the details of these earlier links in the chain, but will take them for granted. Whole-organism geneticists find it sufficient to do breeding experiments looking only at what, for them, is the final link in the chain, eye colour, crinkliness of hair, or whatever it is. The behaviour geneticist looks at an even more distant link—waltzing in mice, creeping-through mania in sticklebacks, hygiene in honeybees, etc. He arbitrarily chooses to regard a behaviour pattern as the end link in the chain, but he knows that the abnormal behaviour of a mutant is caused by, say, abnormal neuroanatomy, or abnormal endocrine physiology. He knows that he could have looked with a microscope at the nervous system in order to detect his mutants, but he preferred to look at behaviour instead (Brenner 1974). He made an arbitrary decision to regard observed behaviour as the end link in the chain of causation.