V.A. Geodakian
Severtsov Institute of Ecology and Evolution, RAS, Moscow, Russia
Dioecious reproduction includes two fundamental phenomena: crossing (fusion of genetic information) and differentiation of sexes (separation into males and females). The classical genetics and synthetic theory of evolution considers crossing, but not the differentiation products, which are delivered chiefly to the population level as a consequence of specialization of sexes. Therefore, the phenomena associated with differentiation, with the type of reproduction (hermaphroditic, dioecism), with the scheme of crossing or the structure of the population (mono- or polygamy, panmixia) find no treatment within the framework of classical genetics. It is suggested that certain premises of classical genetics need substantial supplementation and development in this sense.
In 1965 we proposed a new concept, treating dioecism as specialization according to two main alternative aspects of evolution: conservation and variation. Such an interpretation followed from the more general cybernetic idea, that division of any adaptive system, evolving in a variable environment, into two coupled subsystems, one of which is specialized for conservative and the other – for operative tendencies of evolution, increases the system stability as a whole. This approach allowed finding a number of new principles, relating the evolutionary characters of the population and the environment.
The central premise of the new theory is the conclusion of greater phenotypic diversity of males compared to females. The greater diversity implies that the first victims of any extreme environmental conditions are males (obtaining of ecological information). At the same time, the number of progeny that a male can leave in such population is incomparably greater than the number of progeny a female can leave (transmission of ecological information to progeny). This means that ecological information on changes that have occurred in the environment is received and transmitted to the progeny by males more effectively than by females. On the other hand, in a population the participation of different males in reproduction is unequal: some leave no progeny at all; others leave many, whereas the participation of females is more uniform: they almost all leave progeny, but a small number each. This means that the picture of genotypic distribution in the population is more representative, more fully rendered by females. Consequently, the flow of hereditary information (from previous generations) is realized more effectively by females, and the flow of ecological information s realized more effectively by males.
The greater phenotypic dispersion of males may, in the first place, be a consequence of the higher level of mutations in males (XY, ZZ). In the second place, it may be a consequence of the fact that female progeny inherit parental features more additive. Finally, it may be a consequence of the broader reaction norm of females.
The broad reaction norm makes females more adaptive and plastic in ontogenesis, which imparts greater stability of female in phylogenies. On the contrary, the narrow reaction norm of males makes them less plastic in ontogenesis, subjects them to greater elimination and as a result, makes the male more plastic in phylogenies. This implies that evolutionary transformations affect primarily the males. This means that males can be considered as an evolutionary “vanguard” of the population, while sexual dimorphism can be considered as a vector showing the direction of the evolution of the character. It is directed from the norm of females to the norm of males. Perhaps the features that more often appear in females should be of an “atavistic” nature, while those appearing in males should be of a “futuristic”. Sexual dimorphism, just like all the other basic characters of a dioecious population – dispersion and sex ratio – depends on the conditions of the environment and determines the evolutionary plasticity of a species. Under extreme conditions, when high evolutionary plasticity of the population is required, sexual dimorphism becomes more distinct. Consequently, in the range of a species, sexual dimorphism should be more pronounced at the boundaries of the range and less pronounced at its center. The hypothesis of “sexual dimorphism” has been successfully tested on a large group of lower Crustaceans, as well as on the distribution of congenital defects of the heart and large vessels in the males and females.
It should be noted that up to now sexual dimorphism has been considered only as a mutual adaptation of the sexes, which sometimes is significant for sexual selection, but it has never been associated with evolution of characters, i.e., sexual dimorphism has not carried any evolutionary meaning. Such a treatment could not explain many phenomena: for example, the existence of sexual dimorphism in plants, in which sexual preference and selection are excluded, and, on the contrary, the absence of appreciable sexual dimorphism in monogamous animals, in which sexual dimorphism (such as bright plumage or large size) could unquestionably give certain advantages in sexual selection (at least in the case of a shortage of females), or the presence of reciprocal effects in the homogametic sex.
The proposed treatment permits the detection of the evolutionary significance of sexual dimorphism. The genetic information that has already entered the male subsystem, but has not yet entered the female system, is manifested as sexual dimorphism. Consequently, sexual dimorphism is associated primarily with the structure of the population: in strict monogamy it should be minimal, since monogamists use specialization of the sexes only at the organism level. Furthermore, sexual dimorphism is closely associated with the evolution of characters: it is minimal for stable characters and is maximal for appearing, disappearing, or variable characters. This means that it might be expected that sexual dimorphism should have been more pronounced for phylogenetically recent (evolving) characters. Consequently, although in respect to the “old” characters, the genetic contribution of the father to the progeny is less than the contribution of the mother on account of the “maternal effect,” due to cytoplasm inheritance and uterine development, in respect to the “new” characters the contribution of the father should increase somewhat. This may lead to compensation of the “maternal effect” or even to the appearance of a “paternal effect.” In other words in the case of transmission of genetic information with respect to “new” characters, there should be some dominance of the paternal characters over the maternal ones. This explains modern riddles of dominance, “jumping” and “sleeping” genes, genomic imprinting and other epigenetic phenomena. Hence, considering the phenomenon of heterosis as a summation of the evolutionary achievements acquired divergently, it might be expected that the contribution of the father to heterosis should also exceed the contribution of the mother. The possibility emerges for a more complete explanation of the reciprocal effects, which are essentially nothing other than the sum of the “maternal” and “paternal” effects. We can also explain the different correlation of the progeny of one sex or the other with the mother and father. It is surprising that the characters exhibited only by the females (egg laying in hens, milk yield and amount of butterfat in cows and development of the placenta), which, it might seem, should have been transmitted by the mother, nonetheless are more transmitted by the father.
The predictions of the theory are easy to verify. For this it is necessary to select clearly “new” characters and to compare their inheritability among reciprocal hybrids in the crossing of different forms.
What characters can be considered as “new” characters or as characters “on the evolutionary path”? In agricultural, animals and plants, evidently all the economically valuable characters, for which they were artificially selected in the requisite direction, are such characters. In animals such characters are: early maturity, productivity of meat, milk, eggs, wool, etc. Consequently, it might be expected that for all economically valuable characters there should be a “paternal effect” – some dominance of the characters of the paternal line over that of the maternal line.
The pattern revealed casts light on the nature of heretofore uncomprehended reciprocal differences and permits the use of the vector of the “paternal effect” as a “compass”, showing the direction of evolution of a character. Moreover, in contrast to sexual dimorphism, the “paternal effect” permits a judgment of the evolution of all characters, including those that are manifested in only one sex, including primary and secondary sex characters. It becomes understandable why heterosis in agricultural animals and plants is always directed toward an increase in characters useful for man. In addition to its theoretical significance, this pattern is also of practical importance, since it permits a qualitative prediction of the results of hybridization and a correct selection of parental pairs in crosses.
The interpretation of sexual dimorphism as a phylogenetic “distance” between the sexes, as evolutionary “news” having already arrived to males, but not to females is applicable to all characters of humans, animals and plants for which sexual dimorphism is observed.
References, original articles and other supporting materials can be found at the theory’s web site http://www.geodakian.com