V. A. GEODAKIAN
Severtsov Institute of Ecology and Evolution, RAS, Moscow, Russia
Abstract—In order to understand the phenomenon of sex, it is not enough to know about its reproductive role and role in recombination. In addition, knowledge of its evolutionary role is required. Sexual differentiation allows testing evolutionary innovations in the male genome before they are transmitted into the female one. This is possible in the framework of dichronous evolution, when males evolve before females.
Dichronicity results from different reaction norm of the sexes. Consideration of males as an evolutionary “vanguard” of population and of sexual dimorphism as an evolutionary “distance” between sexes allows explanation from a single standpoint of many unclear phenomena, and discovery of new regularities relating sexual dimorphism with the evolution of the character (“phylogenetic rule of sexual dimorphism”), age dynamics of the character (“ontogenetic rule of sexual dimorphism”), dominance of the character in reciprocal hybrids (“paternal effect”), heterosis, and the effects of polygamy.
All biological theories, including main paradigms of classical genetics and Darwinism, are by default theories for unitary systems. When these theories attempt to explain behavior of binary systems (for example, unisexual population), they treat their subsystems as different forms, but not as phases, therefore they assume that the system evolves as a whole.
The Evolutionary Theory of Sex considers differentiation of a population into two subsystems (sexes) as a conservative and operative specialization. Increased variety and therefore more close contact of the operative subsystem with the environment transforms monomodal population into bimodal, direct “ecology” (environment → system) into indirect one (environment → operative → conservative subsystem) and synchronous evolution into dichronous one (first operative then conservative subsystems).
Sex riddle
The problem of sex is still unsolved primarily due to the lack of a clear understanding that the sexual process and sexual differentiation are opposite phenomena. Researchers attempt to understand the advantages of the sexual reproduction (hermaphrodite and unisexual forms) over the asexual one, although it is necessary to understand the advantages of unisexuals over hermaphrodites.
The purpose of the sexual process is described by many hypotheses. It is needed to comprehend the objective of the sexual differentiation. Although it is recognized that, because unisexual methods have no visible advantages over asexual and hermaphroditic ones, unisexual reproduction should provide us with significant evolutionary bonuses, the sex problem is commonly considered as a reproduction problem but not an evolutionary one.
Sexual dimorphism problem
Clearly pronounced sexual dimorphism exists in many animals and plants. Some cases of sexual dimorphism are manifested in the development of such characters, which are, evidently, detrimental to their owners decreasing their viability: e.g., decorations and bright coloration of many bird males, long tail feathers in bird of paradise or lyrebird males which inhibit their flight. Loud cries and singing, strong smells can also attract predators. Development of such characters is hard to explain in terms of natural selection. For their explanation in 1871 Darwin advanced the theory of sexual selection. It was the matter of controversy even then. Many authors thought it to be the weakest point of Darwin’s theory (see Sexual dimorphism. Geodakyan V. A. In: Evolution and morphogenesis. (Mlikovsky J., Novak V. J. A., eds.), Academia, Praha, 1985, p. 467–477.).
Conservative-operative specialization of sexes
Higher mortality and vulnerability of males to all harmful factors of the environment make one believe that it is the operative subsystem of the population. Compared to females, males (both XY and ZZ) experience more mutations, have narrower reaction norm, greater activity and mobility, higher aggressiveness and inquisitiveness, and riskier behavior. The second group of properties includes great superfluity of male gametes, their small size, the greater activity of males, their inclination towards polygamy and other ethological and psychological qualities. All these properties, moving the male sex to the frontline of the evolution, provide for receiving of ecological information.
Long periods of pregnancy, feeding and taking care of the descendants among the females increases the efficient concentration of the males, turning the male sex into superfluous, and thus cheap, while the female sex—into deficit and thus more expensive. As a result of such specialization of the sexes, asynchronous evolution takes place: new characters first appear in the operative subsystem (males), are tested there, and then are passed on to the conservative subsystem (females).
Transmission of genetic information to the progeny. Sexual dimorphism in one generation
Father and mother transfer approximately identical amount of the genetic information to the progeny, but the quantity of progeny that males can produce is much more compared to female. In a strictly monogamous population the number of mothers and fathers is equal. Contrary, in a polygamous population the number of mothers is always greater than the number of fathers. It means that the hereditary (“old”) information concerning the distribution of genotypes in panmictic population is better, more completely transmitted by the females. Broader reaction norm of females makes them more flexible, adaptive in ontogenesis so they can move from the zones of discomfort and elimination into the comfort zone.
Wide communication channel between males and their progeny makes possible better transmission of ecological (“new”) information. By leaving more offspring rare males can multiply their ecologically valuable genotypes. So, in changing environment, different reaction norm and channel to the progeny create genotypic sexual dimorphism in the first generation. This “new” information gets preserved from complete mixing by Y-chromosome which is transferred only from father to son.
Sexual dimorphism on different characters
In relation to sex the characters can be divided into three groups. The first group has no difference between sexes. Distribution of such characters in males and females in the population is similar. Among these are the majority of specific characters (number of organs, extremities plan and general structure of the body). There is no sexual dimorphism for these characters in the norm.
The second group of characters is those inherent only to one sex. It has an absolute pattern and distinguishes any male from any female. These include all primary and secondary sexual characters. Quantitative estimation of such character is possible for one sex only, for another one it equals zero. However they are genetically distributed in both sexes (e.g. information concerning egg yield of the breed lies in genotypes of hen and rooster as well). Because phenotype of one sex lucks the character, one can judge genotypic sexual dimorphism by reciprocal effects.
The third group of characters are those which are presented in both sexes but are differently pronounced or/and are met in the population with different frequency depending on sex. The pattern of sexual dimorphism for these characters is not an absolute, organismic, but the populational one (different distribution of the character in males and females). Populational sexual dimorphism can exist for such characters as stature, weight, size, proportions, and many morpho-physiological and ethologo-psychological characters.
“Phylogenetic rule of sexual dimorphism”
Males are the first to be affected by evolutionary transformations and therefore can be considered as evolutionary “vanguard” of population. Sexual dimorphism for a character can be considered as a “distance” between sexes, as a vector indicating the evolutionary trend of this character. It is directed from the female norm in the population for the given character to the male norm (“phylogenetic rule of sexual dimorphism”). Therefore the characters which more often appear and are more pronounced in females ought to be of the “atavistic” nature, and those more often manifested in males—of the “futuristic” one (search).
Sexual dimorphism and evolution of the characters
Sexual dimorphism must be closely related to the evolution of the character; it must be minimal for stable characters and maximal for the evolving characters (appearing, disappearing or altering). It could be expected that sexual dimorphism must be more pronounced for phylogenetically younger evolving characters. Sexual dimorphism also should be related to the population structure: in strictly monogamous populations it must be minimal, since they use sex specialization only at the organismic but not at the population level.
“Ontogenetic rule of sexual dimorphism”
In ontogenesis the character is changed, as a rule, from the female to male form. In other words, the female characters should be weakened with age, and the male ones—strengthened (“ontogenetic rule of sexual dimorphism”). About twenty anthropological characters for which the data on both sexual dimorphism and ontogenetic dynamics were obtained prove completely the regularity predicted by the theory. These characters are: relative length of legs, forearm, fingers, head index, tooth arch, epicantus, aquiline nose, erythrocyte concentration, pulse frequency, brain asymmetry, norm and time of reaction, olfaction, and perception of bitter taste of phenylthiourea.
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