Frozen Evolution. Or, that’s not the way it is, Mr. Darwin. A Farewell to Selfish Gene.

 In unicellular organisms, cells are only rarely differentiated morphologically into microgametes and macrogametes. This is apparently a result of the fact that the unicellular organism and the unicellular gamete are exposed to very similar selection pressures in their environment, which does not permit them to differ much from the common structural plan in their morphologies. However, the situation is somewhat different for permanently attached (sessile) unicellular organisms. A different selection pressure acts on the gametes than on the sessile individual, as they must, at the very least, be capable of looking for one another. In this case, it can be expected that differentiation into microgametes and macrogametes will occur.

            Differentiation into microgametes and macrogametes is more or less a general rule in unicellular organisms forming colonies and in true multicellular organisms. The phase of a multicellular, frequently macroscopic organism regularly alternates in the life cycle of the species with a mostly unicellular gamete phase. It is evident that the selection pressures acting on a macroscopic organism and a microscopic gamete are different. Simultaneously, especially microgametes are frequently produced in an enormous excess compared to macrogametes, so that the intensity of their mutual competition to find and fertilize macrogametes can be extremely high.

            The aspect of intergamete selection warrants closer attention. At first glance, it may seem that its effectiveness must be incomparably greater than the effectiveness of selection at the level of an adult multicellular individual. One sperm from amongst millions participates in fertilization of an egg. However, it should be borne in mind that each gene occurs in the set of sperm derived from a single individual in only two variants, where 50 % of the sperm carry one variant and 50 % the other one. Thus, if the concepts of the theory of interallele competition are considered (see IV.9.1), it is apparent that, from the viewpoint of the individual alleles, this does not involve selection of one in a million but one of two. It is, of course, necessary to point out that new mutations formed during gametogenesis will be selected with an effectiveness of one in a million if they occur in the sperm population with this frequency.

            Gametes and their multicellular organism have a common gene pool for their evolution. However, because they are exposed to different selection pressures, situations must necessarily occur in which a certain gene is exposed to two opposing pressures. From the standpoint of the chance of a multicellular organism surviving to reproductive age, it could, for example, be advantageous if the Michaelis constant for a certain substrate is a reduced for a certain enzyme while, from the viewpoint of the chance of microgametes rapidly finding macrogametes, it could be, to the contrary, advantageous if this constant is increased. As the intensity of the selection pressure on the gamete can be greater than the intensity of the selection pressure on its multicellular organism, it could easily happen that the interests of the gamete would predominate over the interests of the organism and evolution would proceed towards an increase in the Michaelis constant and thus in an undesirable direction from the viewpoint of the multicellular organism.

            While the gamete can hardly affect the selection pressures to which the multicellular organism is exposed, the multicellular organism can very easily and very substantially alter the environment in which the gametes will live and thus the selection pressures to which they will be exposed. Some facts indicate that this targeted influencing of the gametes actually occurs.

            The most effective mechanism capable of limiting inter-gamete competition and thus also the subsequent autonomous evolution of gametes consists in inactivation of genes in the mature gametes. For example, it is known that most of the genes in the sperm of vertebrates are completely inactive and that neither transcription nor subsequent translation occurs on them (Ward 1994). Highly condensed nuclear material, i.e. an indirect indication of gene inactivity, is found in the microgametes of most animals, plants and protozoa. Thus, most of the properties of sperm are not determined by the set of genes borne by the particular sperm, but by the set of genes of the multicellular organism controlling the processes of spermatogenesis and spermiogenesis in the sex organs. However, recent results have indicated that, in spite of the condensation of chromatin, expression of a great many genes occurs in microgametes. In plants, possibly up to 20 thousand genes are expressed in pollen grains and it has even been observed in vertebrates that some of the expressed genes affect such an important trait from the viewpoint of intergamete selection as flagella mobility (Olsson & Madsen 2001).

            It is also known for a great many animals that the female does not leave the sperm to their fate in her reproductive organs following copulation (Pizzari & Birkhead 2000; Tschudirein & Benz 1990). Cases have been described in many species of animals, including human beings where the sperm in the reproductive organs are passively drawn in or rapidly moved by peristaltic motion to the sites where fertilization is to occur (Baker & Bellis 1993b). It cannot be excluded that the female thus prevents intergamete competition, here a race amongst the sperm for the fastest pathway to the egg.