Evolutionary Theory of Sex Chromosomes

Explains the routes of gene movement along the chromosomes
during the gene’s life-span.

A new concept uses the idea of asynchronous evolution for the explanation of existence and functional roles of sex chromosomes.

In 1965 V. Geodakyan theoretically predicted that “In the chromosome set, the roles of sex chromosomes and autosomes (A) is in effect, respectively, the short-term and long-term memory; that is why sex chromosomes, primarily the Y-chromosome, serve as a gateway into heredity for variation”. Y-chromosome does it primarily for mutations induced and directed by the ecological differential rather than of spontaneous mutations.

The new genes first appear in the Y-chromosome and then, after many generations, become transmitted through the X-chromosome to autosomes.

Therefore, before appearing in autosomes, each new gene is tested twice in sex chromosomes, first in the Y- and then in the X-chromosome. The recessive X genes manifest themselves almost exclusively in males, and only males are under selection pressure. Such is the evolutionary significance of sex differentiation and the main advantage of sexual dimorphism.

Autosomes are long-term memory of the genome (analogous to the female sex in a population), and thereby serve for genome conservation. They store the working structural genes common for both sexes. They are the oldest chromosomes, found even in sexless organisms. Autosomes contain fundamental species-specific information, and implement the most ancient programs of reproduction and recombination. Stochastic transmission of autosomes ensures the maximum diversity of genotypes. Owing to that, autosomes perfectly fulfill the programs of the sexual process (fertilization), in which remarkable achievements are made by hermaphrodites. In this sense, autosomes can be regarded as “recombination” chromosomes.

Sex chromosomes are short-term memory structures, the experimental subsystem of the genome (a male sex analogue), and provide for genome modification. As a new character does not appear in the female genotype without prior testing in the male one, a new gene is not transferred to autosomes without testing in sex chromosomes.

The main role of sex chromosomes is not reproductive — determination of sex — as believed earlier, but evolutionary, i.e., the creation of dichronomorphism for economical evolution, even at the cost of reproduction. Sex chromosomes change and regulate the sex ratio rather than maintain it at 1:1 level.

Sex chromosomes are significantly “younger” than autosomes. By triggering and implementing the differentiation program, sex chromosomes form two subsystems in a population (conservative and operative). Because of this, the more monogamous and more polygamous sexes have respectively broader and narrower reaction norms, irrespective of the gametic type. Sex chromosomes contain mainly evolving genes, both newly acquired and bound to be lost. Their activity is directed against the recombination program, as they restrict the male-male and female-female combinations. Thus, the efficiency of the sexual process is reduced twofold. In this sense, they are more “antisex” rather than “sex” chromosomes. Therefore, according to their role, it’s more logical to name them the “evolutionary” chromosomes.

Several algorithms can be identified in the informational behavior of chromosomes.
Vertical mechanisms involve transmission of chromosomes from generation to generation.
Horizontal mechanisms describe reception of information from the environment; its transmission between chromosomes; and elimination in the form of genetic processes, such as mutagenesis, crossing-over, translocations, episomal transfer, transfer by viruses, plasmids, mobile elements, etc.

Behavior of the chromosomes is determined primarily by three vertical algorithms. (1) Stochastic, when chromosomes of the homologous pair come to the son or daughter in a purely random fashion. This algorithm is responsible for the transmission of autosomes and thought to be typical for X-chromosomes of the homogametic sex. (2) Ipsi-algorithm, when the chromosome is transmitted from the parent only to the offspring of the same sex. This is the transmission algorithm of the Y-chromosome. (3) Contra-algorithm is responsible for transmission from the parent to the offspring of opposite sex. This is the transmission algorithm of X-chromosome in the heterogamete sex.

The stochastic algorithm deals with the genetic information that is common for both sexes, and implies gene mixing during each fertilization, which homogenizes the population, and hence cannot provide a basis for genotypic sexual dimorphism. This algorithm is the oldest. It existed even before sex differentiation, and realizes only the reproduction and recombination programs.

Nonstochastic algorithms came into light after the appearance of different sexes, and deal with the information which differs in males and females, i.e., with genotypic sexual dimorphism; they hence produce, maintain, and regulate the dimorphism. Ipsi algorithms, pertaining to a single sex, transmit the genetic information via males, and hence can produce genotypic sexual dimorphism and increase or decrease it. Ipsi algorithms initiate the differentiation program. Contra algorithms, like the stochastic ones, involve information transmission from one sex to another, hence homogenizing the population, but contrastingly, they maintain the genotypic sexual dimorphism at a stable level rather than reduce it to zero. The combination of ipsi and contra algorithms thus allows producing and maintaining a certain difference between subsystems, and vary it in dependence on the environmental condition. In this connection, contra algorithms operate as stabilizers (negative feedback), while ipsi algorithms operate as regulators (positive feedback).

The Y-chromosome is a connecting link between the nucleus and cell environment (the cytoplasm, mitochondria, etc.), a kind of genomic gateway for information. This chromosome converts ecological information into a genomic format, i.e., it produces new genes (mutations), and can, therefore, be designated the ecological chromosome. It contains genes “of tomorrow”; triggers, accelerates, and controls the development of asynchronism or sexual dichronomorphism (evolutionary and morphological “distance” between sexes, including the difference with respect to the reaction norm); and serves as a primary “test range” and “quarantine” for new genes.

The contra-X chromosome (cX) is a gene carrier linking the Y-chromosome with the female genome (transport chromosome). Phylogenetically, it functions as a stabilizer, relaxer, and liquidator of sexual dichronomorphism. It also serves as the second test range for new genes (hemizygous in males and heterozygous in females) during ontogeny.

The ipsi-X chromosome (iX) is involved in determining the reaction norm in females, depending on the type of polygamy. It should contain a greater proportion of modifier genes and genes encoding quantitative traits. This chromosome transfers the new genes to autosomes and eliminates their old genes. Its certain region contains exclusively female genes “of yesterday,” i.e., carries atavistic information. Thus, sex chromosomes provide a means for both the storage and transmission of information.

environment

_______________ Chromosomes _______________

↓

│

cytoplasm

→

cX_m

→

cX_f

→

iX_f

→

cX_f

→

cX_m

Appearance of new genes —>

│

—> Death of unnecessary genes

m – male, f – female

In the process of partial conjugation of the X- and Y-chromosomes in animals, just as in plants, only a part of genes is present in the conjugating region (Fig). The "entry point" and the "exit point" of the Y-chromosome should be at some distance from each other. There should be some time necessary for the gene to move along Y-chromosome in order to get to the region, which conjugates with the X-chromosome.

Fig. The hypothetical schematic representation of the route of a new gene through
sex chromosomes during the divergent phase of trait evolution.
E—environment (cytoplasm). Chromosomal regions: a, c, e, g —entries of chromosomes do not participate in crossing-over; b, d, f —exits of chromosomes participating in non-equal crossing-over and translocation of genes to autosomes. Gene transitions: (1) from the environment to Y chromosome (mutagenesis); (2) along the Y chromosome from the nonconjugating (a) region into the conjugating one (b); (3) nonequal crossing over Y → cXm; (4) along the length of cX chromosome in male and female genome; (5) vertical cX algorithm (father → daughter); (6) unequal crossing over cXm → iX; (7) along the iX chromosome; (8) translocation (plasmids, viruses) and iX chromosome → autosomes; (9) along the length of autosomes.

The situation in the X-chromosome appears to be similar to that in the Y-chromosome. The entry point and the exit point are at some distance from each other, and, therefore, moving along the X-chromosome, the "young" gene in a hemizygous state is subjected to a second testing period in male genome (Fig.). Therefore, each new gene, before it moves into an autosome, passes a double check in sex chromosomes: first, in the Y-chromosome, then in the X-chromosome. But since recessive X-genes are expressed only in males, it is the male sex that is subjected to selection.

The classical chromosomal theory does not give an answer to this question. However, the very name of sex chromosomes (gonosomes) implicates that they carry genes for characters associated with sex and reproduction, and, consequently, autosomes carry genes for non-sexual, somatic characters; i.e., genes are localized in chromosomes according to the reproductive criterion. The new concept gives a definite answer to the above question: sex chromosomes must carry genes for evolving characters, and autosomes, genes for constant (stable) ones; i.e., the criterion is evolutionary. Thus, according to the classic theory, somatic mutations should be in autosomes, while genes coding for primary sexual characters should be in sex chromosomes; now, according to the new concept, all this should be the other way around: somatic mutations should be located in sex chromosomes, while genes coding for sexual characters should be in autosomes (Table).

Theory	Traits
	stable		evolving
	somatic	sexual	somatic	sexual
Classic	A	SC	A	SC
New	A	A	SC	SC

In the gene pool of a dioecious population, genes can be classified into the following three groups according to their evolutionary age and localization in chromosomes of males and females:
(1) Exclusively male Y- and X-chromosome genes. These are new, “young,” “tomorrow” genes determining future characters that appeared in males but were not yet tested, transmitted to autosomes, and shared.
(2) Shared (working, “today”) genes. These constitute the main part of the genome, are localized in autosomes, and are present simultaneously in both sexes.
(3) Female X-chromosome (old, having worked in autosomes, “yesterday”) genes. These genes were already lost by males but still preserved in females as atavistic prior to elimination. These genes are probably localized in a special region of the X chromosome (or maybe in autosomes) and are transferred to the male genome only for elimination.

The classic theory of sex chromosomes interprets the condensation of the X chromosome in the female genome (Barr's body), as the dose compensation of X-chromosome genes. If this interpretation were true, then the Barr bodies would normally always be present in homogametic sex. However, in birds, as in mammals, the female chromosome is condensed, although birds possess only one X chromosome. How can this be explained on the basis of dose compensation? Moreover, birds lack the conjugation of sex chromosomes. For some unknown reason, DNA replication of the single X chromosome in homogametic sex and the Y chromosome occurs after the termination of autosome replication.

According to the new concept the condensation of the X chromosome in the female genome irrespective of the gamety type, is interpreted as a barrier to the spreading of new, untested information in females.

From mothers we receive old genetical information, from fathers—latest evolution “news”

About two decades ago British scientists made an interesting discovery. They showed that development of the placenta (female organ) is controlled by father’s genes, while development of an embryo—by mother’s [Surani, 1984, McGrath, 1984]. This genetic process called genomic imprinting is challenging the classical view of human genetics that there are two functioning copies, one from each parent, of every gene. Imprinting means that one copy inherited from one parent is active, for some genes the maternal copy and for others the paternal, while the same gene from the other parent is inactive or silent.

Genomic imprinting confirms that there can be “male” and “female” forms (or phases) of the same gene. According to new view the main factor determining which form is expressed is phylogenetic age of a character, system or organ. Placenta is relatively new organ appeared in placental mammals. Embryo is very old system. So, genes for the placenta are still located in the male genome or were moved into female genome but are still closed. Control of embryonic development is very old information that we get from mothers.