1998 Evol Role Sex Chr Genetika Eng transl.doc
Russian journal of Genetics, Vol. 34. No. 8. 1998, pp. 986-998. Translated from Genetika, Vol. 34, No. 8, 1998, pp.
1171-1184.
Original Russian Text Copyright © 1998 by Geodakian.
DEBATABLE TOPICS
Evolutionary Role of Sex Chromosomes: A New Concept
V. A. Geodakian
Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow,
117071 Russia Received May 8, 1996; in final form, December 3, 1997
"It seems that the human mind should freely develop concepts prior
to the confirmation of their existence… Science cannot flourish on
pure empirical evidence. This flourishing is possible only when the
fictitious and the observed are compared."
Albert Einstein [1]
"One of the primary aims of a theoretical study in any
field of human knowledge is establishing the
viewpoint that reflects the studied object with
maximum simplicity."
Willard Gibbs [2]
Abstract—Sex differentiation provides for testing evolutionary innovations in the male genome
before they are transferred to the female one. This is possible with dichronous (asynchronous)
evolution, when evolution in males precedes that in females [3-7]. Hence, along with common
autosomal genes for stable characters, exclusively male and exclusively female genes must exist. The
male genes are already acquired by the male genome, but are not yet transferred to the female one.
The female genes are already lost by the male genome, but still remain in the female genome. They
constitute temporary evolutionary genotypic sexual dimorphism. Common genes cannot exhibit
genotypic sexual dimorphism; they show only constant phenotypic hormonal sexual dimorphism. On
the basis of the interpretation of genotypic sexual dimorphism as a consequence of sex dichronism,
the evolutionary role of sex chromosomes is clarified, and a new concept for them is suggested.
According to this concept, theY chromosome is the "conductor" of ecological information into the
genome, the "place of birth" and testing of new genes and the accelerator and regulator of genotypic
sexual dimorphism. By contrast, the X chromosome of the heterogametic sex provides the
transportation of new genes from the Y chromosome to autosomes. This chromosome stabilizes,
relaxes, and suppresses genotypic sexual dimorphism and accumulates genes that will be eliminated.
This concept sheds light on many problems: the chromosomal localization of genes and their transfer
to other chromosomes, the inactivation of chromosomes, mobile genes, mutation bursts, insertional
mutagenesis, the association of theY chromosome with stress, retroviruses, etc. In particular, it
explains why and where genes "jump," why transpositions of mobile elements depend on ecological
stress, why different genes mutate simultaneously, etc. [8].
INTRODUCTION
Since the discovery of sex chromosomes by McClung in 1901 [9], it is thought that their main role is
to determine sex and establish a 1:1 sex ratio. Is this true? Of course, sex chromosomes perform both
these functions, but is their role restricted to only this? Only one trigger gene is sufficient for sex
determination, and the 1:1 sex ratio automatically results from crossing a recessive homozygote to a
heterozygote. Sex existed before the appearance of sex chromosomes, and many modern dioecious
species lack them. Thus, the evolutionary significance of autosomal-gonosomal differentiation is
unclear. What principle underlies it? What is the significance of different algorithms of chromosome
behavior? Why are autosomes passed from parent to offspring in a random fashion, whereas sex
chromosomes have specific routes: the Y chromosome is transferred from the father to sons, and the X
chromosome to daughters? How are conjugation, crossing over, and sex-chromosome condensation
related to sex and gamete type? We have ample knowledge on the operation of genes on chromosomes
in ontogeny, but the evidence of their existence in the genome and of their genomic phylogeny is scarce.
It is unclear whether genes have a resident life mode: whether they are "born," "live," "work," and "die"
on one chromosome, or whether their "life" is nomadic disperse, i.e., whether they pass different stages
of their life on different chromosomes. Is there a regular route of genes in the genome, and if so, what is
this route?
1998 Evol Role Sex Chr Genetika Eng transl.doc
Many mysteries, contradictions, and new data that cannot be explained in the context of the classic
theory of sex chromosomes have been accumulated. For instance, the role of Barr bodies is traditionally
interpreted 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 [10].
TheY chromosome is enigmatic. This chromosome is most variable (especially in length) in the
genome. It is rich in repeats and heterochromatin in animals and in euchromatin, and is dispersed over
all chromosomes repeats in plants [11]. In humans, it is almost empty genetically, except for genes
determining hairy ears and webbed toes. In other species, the Y chromosome can contain numerous
active genes. For example, many genes in Drosophila are localized within the Y-chromosome
heterochromatin. In guppy Lebistes reticulatus, more than 30 Y-chromosome genes (and only one
autosomal gene) controlling color in males were found as early as in 1920s and 1930s. Some of these
genes participate in the unequal crossing over with the X chromosome, and the Y → X transfer occurs
four times more often than the X → Y transfer [12, 13]. Studies on dragonflies showed that the XY form
appeared in evolution later than XO. However, an opposite view exists, according to which sex
chromosomes originated from a normal autosomal pair carrying genes of sex determination. Because of
this, in more primitive species, the Y chromosome has the same size as the X chromosome, enters into
partial or complete conjugation with the latter, and participates in crossing over. In more evolutionarily
advanced species, the Y chromosome is small, binds with the X chromosome only in terminal parts, and
lacks crossing over. In the process of evolution, the Y chromosome loses active genes, degrades, and
disappears. Consequently, the XY form precedes XO [14]. The reason for this is unknown. However, the
opinion that the bright red spot on males of guppy previously was characteristic of females and later lost
by them seems to me dubious. I believe that females never had this spot. A Y chromosome of a larger
size was observed in different ethnic or social groups. There is evidence that this chromosome exhibits
greater variation in rodents inhabiting zones of high seismic activity [15], that it is associated with
retroviruses [16], new mutations [17, 18], and so on.
The results discussed above produce the impression that we do not have an essential understanding
of the role of sex chromosomes, particularly the Y chromosome. We do not understand why sex
chromosomes exist; what their functional, adaptive, and evolutionary significance is. There is no logical
explanation of their appearance. In the present study, I suggest a new concept of sex chromosomes that
provides answers to these questions. My model is based on the idea of dichronous evolution. However, a
more fundamental problem should first be considered: what is the purpose of sex?
THE PROBLEM OF SEX
For more than a century, sex has been a primary issue of evolutionary biology. The problem of sex
was investigated by prominent biologists of the 19th and 20th centuries: Darwin, Wallace, Weissmann,
Gold-schmidt. Fisher, and Muller. In spite of this, modem scientists still speak of a crisis in evolutionary
biology in relation to the problem of sex. In the past decade, interest in this problem has been revived. A
dozen monographs appeared bearing in the title words "sex" and "evolution" [19-28]. One of them [19]
begins with the phrase: "The prevalence of sexual reproduction in higher animals and plants is
incompatible with evolutionary theory." Another author [20] writes: "We do not have an adequate
explanation for the origin and preservation of sex." In the third monograph concerned with evolution and
the genetics of sex, the author states: "The problem of sex is the key challenge to the modem theory of
evolution .... This is the queen of problems .... Insights of Darwin and Mendel that shed light on a
multitude of problems could not overcome the enigma of sexual reproduction" [21]. Another prominent
authority argues: "It is amazing, but scientists do not know why sex exists" [29]. Numerous papers and
reviews appear on the problem of sexual reproduction. In 1993 and 1994, at least two leading genetic
journals devoted special issues to it [30, 31]. Thus, the key problem of evolutionary biology and
genetics—the problem of sex—remains unresolved, and the main question— what is the purpose and
adaptive significance of sex— still have no answer [32].
In the early 1960s, I realized that evolutionary theory has no answer to these fundamental questions.
The heuristic solution of the problem of sex was first published by me in 1965 in a mathematical journal
[3].
1998 Evol Role Sex Chr Genetika Eng transl.doc
What Is the Essence of the Problem, and Why Is It Still Unanswered?
The most important program of life is reproduction. It underlies such biological phenomena as replication,
reduplication, and asexual reproduction. Reproduction is the main criterion in distinguishing living and
nonliving systems. The main source of variation in this program is mutation. The second most important
program is the recombination underlying crossing over, fertilization, and syngamy. Creating a new variation
source independent of environment, recombination provided an ultimate solution to the problem of diversity.
On the basis of recombination, the sexual process appeared. The third most important program is
differentiation, which underlies meiosis, sexual, and other types of differentiation. As a result, dioecious
forms, castes in social insects, dwarf males in some fish species, and other forms of differentiation appeared.
In the process of evolution, these programs arose exactly in the order given above. This order reflects the
constitutive-facultative relationships between them, according to which the preceding basic programs are
obligatory for the formation of subsequent ones, whereas the opposite is not necessarily true.
The concept of sex includes two basic phenomena: the sexual process (the fusion of the genetic
information of two individuals) and sexual differentiation (the division of this information into two).
According to the presence (+) or absence (-) of this phenomena, numerous existing modes of
reproduction can be classified into three main groups: asexual (-, -), hermaphroditic (+, -), and bisexual
(dioecious) (+, +) (Table 1).
Table 1 Characteristics of three main reproduction types.
Program
(biological phenomenon)
Type of
reproduction
Efficiency
Source of
divercity*
Reproduction
Sexual
process
Sexual
differentia
tion
Asexual
+
–
–
max
mid
min
M
Hermaphroditic
+
+
–
mid
max
mid
M+R
Dioecious
+
+
+
min
mid
max
M+R+D
Quantitative
Assortative
Qualitative
* M—mutation, R—recombination, D—differentiation.
The sexual process and sex differentiation are two different and, in essence, opposite phenomena.
The evolutionary purpose of the sexual process is to create or increase genotypic diversity. By contrast,
sex differentiation causes a twofold decrease in this diversity, and nobody knows what the evolutionary
role of this is. For instance, in an asexual population of size N, the maximum theoretically possible
variability of offspring genotypes is N, given that the genotypes of all parents are different. Since the
offspring of each asexual individual is a clone with the same genotype, the variability of the offspring σ
is always lower than N.
In the sexual process, the variability of offspring is squared. In hermaphroditic organisms, each of N
individuals can mate with all individuals except itself, i.e., N - 1; but, as the cross of individual 1 with
individual 2 is the same as that of individual 2 with individual 1 (there is no reciprocal effect), at
N >> 1 , σ = N(N - 1)/2 ≈ N2/2; with the reciprocal effect, σ = N2. In dioecious forms, sex differentiation
that excludes one-sex (male-male, female-female) combinations, decreases the amount of diversity
possible in hermaphroditic organisms by at least two times: σ = N/2 x N/2 = N2/4 (each female with each
male, with the same number of males and females equal to N/2). The offspring diversity in a population
of dioecious organisms also depends on the sex ratio in the parental generation: it is the highest at a 1:1
sex ratio and decreases with any deviation from it.
Thus, with the same population size N, maximum possible offspring diversity levels in asexual,
hermaphroditic, and dioecious populations are in the ratio N : N2/2 : N2/4 ; i.e., dioecious populations
have two times less diversity than hermaphroditic populations! It is completely unclear, what the
advantage of sex differentiation is if it decreases the main benefit of sexual reproduction by twofold.
1998 Evol Role Sex Chr Genetika Eng transl.doc
Why do all evolutionarily advanced animal taxa (mammals, birds, insects) and dioecious plants
reproduce sexually if asexual reproduction is simpler and more effective and if hermaphroditic
reproduction yields more diverse progeny? This is the essence of the enigma of sex. It is still unresolved,
mainly because there is no clear understanding that the sexual process and sex differentiation are two
opposite phenomena. Biologists try to reveal the advantages of sexual (hermaphroditic and dioecious)
over asexual reproduction, but the main task is to understand what are the advantages of dioecious over
hermaphroditic reproduction (see Table 1)? The purpose of the sexual process is obvious: it generates
genetic diversity. But it is still unclear what the purpose of sex differentiation is. Although it is already
clear that, since sexual reproduction has no apparent advantages over asexual reproduction, it must be
evolutionarily advantageous [32], biologists continue to tackle the problem of sex as the problem of
reproduction rather than evolution.
THE CONCEPT OF ASYNCHRONOUS (DICHRONOUS) EVOLUTION
According to Darwin's theory, the evolution of a system follows environmental alteration and proceeds as
a trial-and-error process. Hence, it is more advantageous to test part of a system rather than the whole. For
this, the system should be divided into two parts: the first, more valuable part should be removed from
environmental influence in order to preserve its past characteristics, whereas the second, experimental part
should be exposed to the environment in order to assess what is needed at present and what changes may be
required for the future. This conservative-operative specialization is obtained by consecutive (cascade) or
dichronous (for binary systems) evolution: new characters first appear in the operative subsystem (in males),
are tested there, and then are passed on to the conservative subsystem (to females) [3].
In 1972, I extrapolated this concept to a number of binary evolutionary systems from the molecular to the
population and social levels of organization: DNA-proteins, autosomes-gonosomes, nucleus-cytoplasm,
female sex-male sex, cerebral subcortex-cerebral cortex, etc. I also advanced a hypothesis that all
differentiations of adaptive systems can be regarded as operative-conservative specializations that determine
information transfer from the environment to subsystems [33]. Based on this, isomorphic theories of the
dichronous evolution of sexes [4, 5] and of the asymmetry of organisms and the brain [34] were developed.
The explanatory and predictive potential of these theories is exceptional in biology (e.g., see [35]). Later, I
attempted to extrapolate this approach to the autosomal-gonosomal differentiation of the genome [8].
A population can be divided into males and females; bilateral organisms or organs (e.g., the brain) into the
left and the right halves; human society into right- and left-handers; the genome into autosomes and sexual
chromosomes; sexual chromosomes into X and Y chromosomes. All these classifications are based on the
same specialization principle that is primary for evolutionary systems: the preservation (P) and alteration (A)
of the system. First, the presence of preservation and alteration is the main prerequisite of evolution. The
absence of one of them precludes evolution: the system either disappears or remains constant. Second, the
ratio between preservation and alteration characterizes the evolutionary plasticity of the system; Third, these
conditions are alternative: an increase in alteration is associated with a decrease in preservation, as their sum
is unity (A + P = 1). Without the specialization of subsystems, the system reaches an intermediary optimum
of A/P, whereas with specialization, levels of both A and P can be increased. For instance, with isogamy,
each gamete simultaneously performs both conservative (providing the zygote with resources) and operative
(searching for a partner gamete) functions. As isogametes are of medium size, their performance of both
functions is mediocre. Differentiation in size allows small- and large-sized gametes optimize the search and
the resource supply, respectively. Hence, the large-small size combination is more advantageous than the
medium-medium one, which explains the evolutionary advantage of differentiation.
In each of the above examples, the first subsystem is conservative, main, and protected from the
environment, whereas the second subsystem is operative, "experimental," and more exposed to
environmental impact. Because of this, environmental information first enters into the operative subsystem
and then into the conservative one. Consequently, the evolution of any character in these systems occurs
dichronously (asynchronously): it starts and terminates earlier in the operative than in the conservative
subsystem.
Thus, according to this theory, new characters first appear in males, and then, after many generations, are
passed on to females [4, 5]; new functions become leading first on the right side of the body, then on the left
side; dominating operating centers first appear in the left cerebral hemisphere and then are transferred to the
1998 Evol Role Sex Chr Genetika Eng transl.doc
right one [34]. Similarly, new genes appear first in sex chromosomes, and then in autosomes [8].
The Theory ofDichronous Evolution of Sex:
The Appearance of Dichronism and Phases of Character Evolution
Sex differentiation is an economical form of the informational contact of a dioecious population with the
environment. Because of dichronous evolution, it allows the population to test all new characters in males
before transmitting them to females (Figs. 1, 2).
Figure 1
Evolution of trait (0 → 1) in the monoecious forms.
Abscissa: X—mean population genotype for a given trait,
(0)—preevolutionary, (1)—postevolutionary.
Ordinate: T—time of phylogeny, T1 beginning; T2—end
of trait evolution. E—stage of trait evolution;
s1—preevolutionary, s2—postevolutionary phase of the
trait
stable state. Dashed lines parallel to the tragectory and
small
distribution curves between them show the magnitude of
genotype variants in the population during different phases.
T
s2
T2
E
T1
s1
T0
0
Figure 2
Dichronous evolution of traits (0 → 1)
in males (♂♂) and females (♀♀).
T1–T3—beginning-end of trait evolution in ♂♂;
T2–T4—in ♀♀; Phases of evolution: d—
divergent, p—parallel, c—convergent; E♂♂ and
E♀♀—evolution of trait in ♂♂
and ♀♀. SD—sexual dimorphism, SDC—sexual
dichrony.For other designations, see Figure 1.
1
X
T
s2
T4
c
♀♀
E♀♀
T3
SDC
p
SD
T2
♂♂
d
E♂♂
T1
Males and females respond to
environmental changes, e.g., the ecological
s1
differential, in a different fashion. In 1974, I
advanced a hypothesis on a broader reaction
T0
1
0
X
norm in females than in males. Based on
this hypothesis, I successfully predicted a
higher concordance of male pairs of
monozygous and female pairs of dizygous twins [36]. The broader reaction norm of females allows them to
develop, on the basis of the old genotype, only via ontogenetic plasticity, a more adaptive phenotype, and
leave the area of selection. Because of the narrow reaction norm, males lack this possibility. Consequently,
1998 Evol Role Sex Chr Genetika Eng transl.doc
selection operates mainly in males, the number of males decreases, and evolution begins. Thus, the same
environmental information results in the modification of females and elimination of males. In other words,
sex differentiation for the reaction norm ensures the high phenotypic plasticity of females in ontogeny and
the high genotypic plasticity of males in phylogeny, i.e., the leading evolution of males [3, 4, 5, 36]. Females
transform ecological information into temporal phenotypic sexual dimorphism, whereas males transform it
into genotypic sexual dimorphism at the expense of their number. After testing, this information is passed to
females by an internal route. Thus, genotypic sexual dimorphism takes the place of the ecological differential
as a moving force for females. In this way, females receive new information from males, rather than from the
environment, and escape selection. This explains the evolutionary significance of sex differentiation and the
advantage of dioecy.
The evolution of any character in dioecious organisms consists of three phases.
In the first, divergent phase, only males evolve, because only males receive new information from the
environment. Genotypic sexual dimorphism appears and increases in subsequent generations (the stage of
increasing genotypic sexual dimorphism). The duration of the divergent phase and the level of asynchrony
(sexual dichronism) is equal to the evolutionary retardation of females or the acceleration of males (Fig. 2).
This temporal difference is required for the testing of new characters in males. But sexual divergence cannot
occur indefinitely, because it will ultimately lead to reproductive isolation.
Next, the mechanism of the transfer of information from males to females switches on. Females start to
change. This is a second phase of the evolution of a character. At this phase, both sexes evolve at the same
rate. Genotypic sexual dimorphism enters a stationary phase, which remains until the end of this phase.
The third phase of evolution is convergent. At this stage, only females evolve. It begins with the
termination of ecological pressure on males, while females are still subjected to the effect of genotypic
sexual dimorphism. Genotypic sexual dimorphism is reduced and disappears. The dimorphic character again
becomes monomorphic and constant. At this point, the evolution of the character is completed. This means
that dioecy, which is traditionally regarded as an efficient mode of reproduction, is in fact an efficient mode
of evolution [4,5]. This new interpretation of the key notion, sex differentiation, allows us to interpret its
derivatives (i.e., sexual dimorphism, sex ratio, sex chromosomes, sex hormones, etc) in a new evolutionary
context.
Sexual Dimorphism
Darwin's theory of sexual selection is virtually the sole explanation of the appearance of sexual
dimorphism [37]. However, Darwin committed a methodological error when he explained the general
phenomenon of sexual dimorphism as a consequence of a special mechanism of sexual selection. A theory
must always be more general than the phenomenon that it explains. In this lies the weakness of the theory of
sexual selection. This theory cannot explain sexual dimorphism in plants that lack sexual selection and in
animals for characters not connected with this type of selection. Moreover, no predictions can be made based
on this theory [7, 38]. According to my theory, genotypic sexual dimorphism is a consequence of the
dichronous evolution of sexes; hence, only evolving characters can display this dimorphism. It appears in the
evolution of any character as a "distance" between sexes and is characteristic of all types of selection
(natural, sexual, artificial). The direction of the evolution of the character is indicated by the direction of
genotypic sexual dimorphism (from the female to the male form of the character).
If new information (In) is already acquired by males but is still absent in females ("quarantine"), or if old
information (Io) is already lost by males but still retained by females ("archive"), the sum of these values
characterizes genotypic sexual dimorphism. The information contained in the male genome can be expressed
as Im = Is + In, and in the female genome as If = Is + Io, where Is is the information shared by both sexes. Is
includes information on the primary sexual traits of both sexes. When two populations (species, races,
ethoses) are mixed, the shared information is mixed in the first generation, whereas the new and old
information are retained in different sexes for the time that sex dichronism persists.
This concept easily explains the differences between interspecies, interracial, or interethnic reciprocal
hybrids related to the direction of crossing, because in these hybrids, only Is is identical, but In and Io they
receive from different forms. If the offspring received identical information from mothers and fathers, no
reciprocal effects would be observed.
1998 Evol Role Sex Chr Genetika Eng transl.doc
On the basis of the theory of the dichronous evolution of sexes, many easily verified predictions and
simple explanations of numerous unclear phenomena and facts can be made. For instance, the evolution of
most vertebrate species was accompanied by an increase in body size, while body size in many insect and
spider species became smaller in the process of their evolution. Hence, according to my theory, in large
vertebrates, males are larger than females, whereas in small insects and spiders, this relationship is reversed.
This is exactly what we observe in nature. The same trend is characteristic of mammals, in particular,
primates, and other taxa.
The theory of the dichronous evolution of sexes is confirmed by the better performance of males with
regard to all commercial traits in agricultural plants and animals. Compared to females, males produce more
meat of better quality, they have better fodder assimilation and growth dynamics. In the commercial breeding
of sheep, horses, reindeer, fur animals, silkworms, and hemp, males surpass females in all valuable traits.
For phenotypically sex-specific traits, the theory can be tested by reciprocal effects, since it predicts the
presence of the paternal effect (dominance of paternal traits) in reciprocal hybrids for all traits (including
those occurring only in females) with divergent evolution and the maternal effect for traits with convergent
evolution [4, 5, 7, 38, 39]. The paternal effect was reported for hatching ability, early maturity, egg
production, and live weight in poultry, in milk production and milkfat content in cattle [39], alcohol
addiction in humans [40], etc. These traits are new, as they resulted from selection or social causes. The
paternal effect for egg and milk production means that, genotypically, bulls have a higher "milk yield" than
cows and cocks "lay more eggs" than hens of the same breeds.
According to the theory of the dichronous evolution of sexes, in humans, the new and old information was
differentiated between sexes throughout many generations. Taking into account the historical processes of
ethnic admixture, e.g., migrations (participation of both sexes of both ethnic groups), conquests (participation
of males, and in the conquered ethnic group, of both sexes), the deportation of females of the conquered
ethnic group (participation of females from two and males from one ethnic group), a number of
anthropological phenomena can be explained.
Using the method of the generalized portrait, Pavlovsky [41] revealed a marked sexual dimorphism in the
Turkmeni population: portraits of females and males corresponded to one and two types, respectively. An
analogous phenomena was shown by Yusupov [42] for Bashkirs: female and male skulls followed
respectively unimodal and tetramodal distributions. In Udmurts and Bulgarians, Dolinova and Kavgazova
discovered sexual dimorphism for dermatoglyphic characters (females had the pattern of one neighboring
ethnos, and males, the pattern of another one [43]). No theory except that of dichronous evolution of sexes
can explain these facts.
AUTOSOMAL-GONOSOMAL DIFFERENTIATION OF THE GENOME
In 1965, when I first used the theory of dichronous evolution for solving the problem of sex, I realized
that this concept underlies the autosomal-gonosomal differentiation of the genome. In the conclusion of my
paper [3], I wrote: "In the chromosome set, sex chromosomes and autosomes play the role of operative and
conservative memory, respectively. Because of this, sex chromosomes, and primarily the Y chromosome,
mediate the accumulation of hereditary variation" [3]. At present, this theoretical prediction has been
convincingly confirmed by a series of experimental studies on the rate of nucleotide substitutions [17, 18].
When a system is divided into subsystems, the succession of systems receiving information from the
environment is of key importance. The information first enters the operative subsystem; next, it is transmitted
to the conservative one [33]. The succession is as follows: in sex differentiation, environment → males →
females; in the differentiation of the brain, environment → left hemisphere → right hemisphere. If
chromosomal and sex differentiations are in fact isomorphic, this isomorphism can be used to reveal cascade
evolution and to clarify the evolutionary significance of autosomes and sex chromosomes. To do this, one
should compare the different evolutionary roles of males and females (obtaining information from the
environment, transforming this information into phenotypic or genotypic one, and its transmission to
progeny) and the algorithms of chromosomal inheritance.
1998 Evol Role Sex Chr Genetika Eng transl.doc
Chromosomal Algorithms and Their Comparison with Phases of Evolution
Algorithms of the informational behavior of chromosomes can be classified into vertical (the transmission
of chromosomes in generations) and horizontal (the reception of information from the environment, the
distribution of information among chromosomes, and the loss of information—i.e., the genetic processes of
mutation, crossing over, translocations, transfer by episomes, viruses, plasmids, mobile elements, etc.). The
chromosome behavior is primarily determined by the following three vertical algorithms: (1) stochastic
algorithm (homologous chromosomes are randomly transmitted to sons and daughters), which is
characteristic of autosomes and X chromosomes of the homogametic sex; (2) ipsi-algorithm (the
chromosome is transmitted from a parent to the offspring of the same sex as the parent), which is typical for
the Y chromosome or of one of the X chromosomes of the homogametic sex (iX); and (3) contra-algorithm
(the chromosome is transmitted from a parent to the offspring of the opposite sex), which characterizes X
chromosomes of the heterogametic sex and the second X chromosome of the homogametic sex. The
stochastic algorithm controls only the information shared by both sexes. Mixing genes in each fertilization, it
maximizes unimodal genetic 'diversity and homogenizes and levels off all drastic changes. Consequently, it
cannot generate genotypic sexual dimorphism. This algorithm, which realizes only programs of reproduction
and recombination, is the most ancient, and existed prior to sexual differentiation.
Nonstochastic algorithms appeared later than dioecy and deal with genetic information that is different in
males and females, i.e., genotypic sexual dimorphism. They create, maintain, and regulate this type of
dimorphism. The ipsi-algorithm initiates the program of differentiation, transmits information within one sex,
creates the information potential between sexes (genotypic sexual dimorphism)—increases or-decreases it.
The contra-algorithm, as the stochastic one, transmits information from one sex to the other, arid thus levels
potentials, but, in contrast to the latter, it maintains genotypic sexual dimorphism rather than annihilating it.
The combination of ipsi-algorithms develops and maintains a specific level of genotypic sexual dimorphism
among subsystems and regulates it according to environmental conditions. The contra-algorithm acts as a
stabilizer of genotypic sexual dimorphism (negative feedback), and the ipsi-algorithm, as a regulator
(positive feedback) [44]. The combination of ipsi-contra associations is of general significance in all cases in
which a "distance" between subsystems should be established and maintained. The same system of control
underlies an unexplained fundamental phenomenon of neurobiology, the control by cerebral hemispheres of
opposite parts of the body [34]. The same principle governs the regulation of sex hormones in males and
females.
To ensure the dichronous evolution of the sexes, the above algorithms operate in the following succession.
(1) As, at the divergent phase only males evolve and genotypic sexual dimorphism arises and increases, new
information should be transmitted only via the ipsi-algorithm. Evidently, as this phase is aimed at
transporting information to the male genome and accumulating it there in the form of genotypic sexual
dimorphism for subsequent testing, these aims can be realized only by the Y chromosome. (2) At the parallel
phase, both sexes evolve, and the level of genotypic sexual dimorphism is constant. Consequently, new
information must be transferred from the Y, chromosome to the female genome. This can be performed only
by the contra-X chromosome. (3) At the convergent phase, females evolve and genotypic sexual dimorphism
decreases and disappears. For this, the reception of new information from the environment by the Y
chromosome must stop, and the transmission of this information to the female genome Via X chromosomes
must continue.
Evolutionary Routes of Genes in Chromosomes
As many generations are required to test a gene on the Y chromosome, a new gene must remain there for
this time period. Both in plants and animals (Lebistes, Melandrium), only some genes of the Y chromosome
are located in the conjugating region in the partial conjugation of the X and Y chromosomes [11-13]. If new
genes directly entered this region, they would immediately be transmitted to the female genome. However,
this contradicts the rationale of the theory of dichronous evolution of sexes. Consequently, the "input" and
"output" of the Y chromosome must be localized at a distance. The time required for a gene to move along
the Y chromosome to the region conjugating with the X chromosome corresponds to sexual dichrohism.
Because of this, only genes that passed the "quarantine" in the Y chromosome enter the conjugating region
and are transmitted via unequal crossing over between the Y and X chromosomes to the female genome.
1998 Evol Role Sex Chr Genetika Eng transl.doc
Apparently, in the X chromosome, the input and output are remote from each other. Moving along the X
chromosome, "young" genes are tested in the hemizygous state in the male genome (Fig. 3). Thus, prior to
entering autosomes, each new gene is tested twice in the sex chromosomes: first at the divergent phase in the
Y chromosome, and then, at the parallel phase, in the contra X chromosome. As recessive genes are
expressed only in males, selection acts exclusively on this sex.
In general, the hypothetic scenario of gene transfer in cascade (sequential) chromosome evolution can be
visualized as follows. When a new gene appears, environment → cytoplasm → Y → cXm → cXf → (iX?)
→ A; when a used gene is lost, A → iX → cXf → cXm. As in sexual differentiation, there is a
dichronomorphism of characters, autosomal-gonosomal differentiation must produce the oligochronomorphism of genes, i.e., three out of four times of appearance and the same number of localization types (Y, cX,
A, iX) of one gene. The direction of evolution of chromosomal oligomorphism (iX → A → cX → Y) and
sexual dimorphism (females → males) is always opposite to that of the information flow (Y → cX → A →
iX, males → females) and can serve as an evolutionary "compass" (Fig. 2). If the route of genes is known,
the principle of their localization in chromosomes can be determined.
Fig. 3. The hypothetical scheme of the route of a gene in sex
chromosomes at the evolutionary stages. E, environment
(cytoplasm). Chromosome regions: a, the input of the Y
chromosome not participating in crossing over with the cXm
chromosome; b, the output of the Y chromosome participating in the
unequal crossing over with the cXm chromosome; c, the input of the
cXf chromosome participating in the unequal crossing over with the
Y chromosome; d, the output of the cXm participating in the unequal
crossing over with the cXf chromosome; e, the input of the iX
chromosome participating in the unequal crossing over with the cXf
chromosome; f, the output of the iX chromosome, translocations of
genes on autosomes; g, the input of autosomes receiving
translocations. Gene transfer: (1) from the environment to the Y
chromosome (mutation); (2) along the Y chromosome from the
nonconjugating (a) to the conjugating (b) region; (3) unequal
crossing over Y → cXm; (4) along the cX chromosome in the male
and female genomes; (5) vertical cX algorithm (father → daughter);
(6) unequal crossing over cXm → iX; (7) along the iX chromosome;
(8) translocations (plasmids, viruses) iX chromosome → autosomes;
(9) along autosomes.
What Genes Are Localized in Sex Chromosomes and in Autosomes ?
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 (Table 2). What are facts?
It is evident that 29 out of 30 genes determining color in guppy (with the exception of one autosomal
gene) [12, 13] and Y-chromosome genes determining hairy ears and webbed feet in humans are
evolutionarily new somatic mutations that are n6t directly associated with reproduction. At the same time,
genes controlling "the most reproductive" characters, i.e., primary sexual traits (gametes, gonads, and
genitalia), are localized in autosomes. These facts contradict traditional views and confirm the new concept,
according to which the main difference between genes located in autosomes and sex chromosomes concern^
evolution rather than reproduction.
1998 Evol Role Sex Chr Genetika Eng transl.doc
Table 2. Which genes are localized on autosomes and which on sex chromosomes?
Combination of characters*
S, C
Localization of genes
according to the classical theory
according to the new concept
Sexual dimorphism
The basis of sexual dimorphism
A
A
—
—
R, C
A
SC
RSD
Phenotypic
S, E
A
SC
ESD
Genotypic
R, E
SC
SC
SD+ESD
Phen + gen
* S, somatic; C, constant; R, reproductive; E, evolving; SC, sex chromosomes; SD, sexual dimorphism; RSD,
reproductive sexual dimorphism; BSD, evolutionary sexual dimorphism.
Dichronous evolution means that, 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. The existence of group 3 is proved by the theory and follows from known facts
and phenomena that cannot be otherwise explained [41, 43, p. 13]. These genes are probably localised in a
special region of the X chromosome (or maybe in autosomes) and are transferred to the male genome only
for elimination.
As gonosomal genes evolve and autosomal genes are stable, the ratio of gonosomal to autosomal genes
(G/A) reflects the evolutionary plasticity of the population. Populations continuously living in a constant
environment lack gonosomal genes (G/A = 0); the more variable the environment, the higher the G/A ratio.
Consequently, there must be an equilibrium [A] ↔ [G] similar to that of the sex ratio [females] ↔ [males].
This equilibrium depends on the environment and shifts to the right and to the left in extreme and optimal
environments, respectively. When populations mix, autosomal genes become mixed in the first-generation
progeny, whereas gonosomal genes remain differentiated between sexes during the period of sex dichronism
(see Fig. 4).
According to the chromosomal and sexual localization of underlying genes, sexual dimorphism can be
classified into three types. (1) After appearance of any character, male genes form a dichronous (gonosomic)
temporary evolutionary genotypic sexual dimorphism of a "futuristic" nature. As these genes reach
autosomes and become shared by sexes, genotypic sexual dimorphism disappears. (2) However, for
characters that have different selective values in males and females, genotypic sexual dimorphism is
maintained by sex hormones and is transformed into autosomal (constant phenotypic sexual dimorphism. For
these (primary and secondary sexual) characters, genotypic sexual dimorphism is absent, whereas the
presence and level of the expression of phenotypic sexual dimorphism determines the hormonal sex of the
individual. (3) In the loss of any character, female genes also form a dichronous temporary evolutionary
genotypic sexual dimorphism that is of an atavistic nature. This dimorphism appears when a shared gene is
transformed into a female one and disappears when this genes is eliminated in the contra-X chromosome.
Constant phenotypic sexual dimorphism is constitutive (basic), and evolutionary genotypic sexual
dimorphism is facultative and can develop only on the basis of the constitutive one. An evolving
reproductive character can have a double (constant and evolutionary) genotypic sexual dimorphism.
1998 Evol Role Sex Chr Genetika Eng transl.doc
Fig. 4. Autosomal (A) and gonosomal (G) genes. Abscissa: genotypes X for the given character; ordinate: their
frequency v in the population. GPD, genotypic sexual dimorphism. In populations continuously living in the
constant environment, all genes are localized in autosomes; consequently, distributions of male and female
genotypes coincide: G/A = 0, GSD = 0, phenotypic sexual dimorphisms 0, "tomorrow" and "yesterday" genes and
reciprocal effects are absent, the character is constant (1). In populations living in the changing environment,
autosomal and gonosomal (male Gm and female Gf) genes are present; this results in evolutionary plasticity,
G/A ≠ 0, GSD ≠ 0; the characters evolve; reciprocal effects may be present (2). When the a and b populations are
mixed, barriers between A genes (dotted line) disappear; i.e., genes are mixed in the F1 hybrids (3). The barriers
between G genes (bold lines) remain for the period of the sexual dichronism. Because of this, two types of GPD and
reciprocal hybrids of both sexes can exist.
As mentioned above, when the environment changes, females are moved from the zone of selection,
whereas males remain in it. Thus, the latter must have a constant genotypic sexual dimorphism for the
reaction norm already at the stage of stability. Genetic information on the broad reaction norm must be
transmitted only maternally, and on the narrow reaction norm, paternally. This can be achieved via ipsialgorithms, i.e., the Y chromosome and the ipsi part of the X chromosome. Why are the narrow reaction
norm and operative specialization characteristic of males rather than females, and can the opposite be true?
Reversion of Sexual Dimorphism in Polyandry
Polyandry, i.e., the mating of one female with several males, occurs in invertebrates, fishes, birds, and
mammals. In polyandry, the female have a broader "section of the channel" than males for transmitting
information to the progeny. In polyandric species, a reversion of sexual dimorphism is often observed:
females are larger and brighter than males; males build nests, hatch eggs, care for the progeny, and do not
fight for females. In polygyny, the opposite trends are observed. Thus, the direction of the dichrony and the
ratio of evolutionary rates depend on the direction of polygamy, i.e., the ratio of channel sections. In a strictly
monogamous population, males and females have the same average channel section; i.e., the number of
fathers is equal to the number of mothers. In this case, the dispersions of ipsi-chromosomes in sons and
daughters are identical. In polygyny, the number of mothers exceeds that of fathers, and the dispersion of the
Y chromosome is lower in sons than that of the ipsi-X chromosome in daughters. In the case of polyandry,
the situation is reversed. The dispersion of the Y chromosome in sons is inversely proportional to the number
of fathers, and the dispersion of the ipsi-X chromosome in daughters, to the number of mothers. In addition,
the Y chromosome triggers the synthesis of testosterone, the concentration of which determines sexual
dimorphism. On the other hand, as shown above, the ratio between the reaction norms of males and females
determines the genotypic sexual dimorphism for any trait.
Thus, I can hypothesize that the reaction norm is inversely proportional to testosterone concentration, and
consequently, the direction of genotypic sexual dimorphism, i.e., the ratio of evolutionary rates of males and
1998 Evol Role Sex Chr Genetika Eng transl.doc
females (Em/Ef) with the ratio of their channel sections (Sf/Sm). Sf/Sm ~ Nfathers/Nmothers ~ σY/σiX ~ Tm/Tf ~
Rf/Rm ~ Em/Ef, where N is the number, σY and σiX are dispersions of Y chromosomes in sons and ipsi-X
chromosomes in daughters, Tm and Tf are concentrations of testosterone, Rm and Rf are reaction norms in
males and females, and ~ is the sign of the positive relationship. Thus, the roles of evolutionary "vanguard"
and "rear-guard" are always played by the more polygamous and the more monogamous sex, respectively.
The wide occurrence of polygyny in nature and the rare occurrence of polyandry are explained by the higher
reproductive potential of males (higher number of male gametes). Polyandry in a strict sense does not exist,
because the possibilities of females in this respect are limited, and they are capable only of oligoandry. On
the basis of the above considerations, I can make the following prediction: in paternal half-sibs (the offspring
of one father and different mothers), daughters have a higher viability, and in maternal half-sibs, sons.
The Evolutionary Significance of Autosomes and Sex Chromosomes
Autosomes, as analogues of females in populations, play the role of the conservative memory of the
dioecious genome and the depot for stable genes shared by both sexes. They are aimed at the conservation of
the genome. Evolutionarily, autosomes are the most ancient chromosomes and contain the basic information
for the species. Their programs (reproduction and recombination) are also more ancient. Autosomes are
stochastically inherited. They are mixed in each generation, ensuring maximum genotypic diversity.
Consequently, in autosomes, especially in hermaphroditic organisms, programs of the sexual process are
realized most efficiently. In this sense, autosomes can be named recombinational chromosomes.
Sex chromosomes play the role of the operative memory or experimental genomic subsystem. Being
analogous to males in populations, they are aimed at changing the genome. 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 aim of sex chromosomes is developing
dichronomorphism for effective evolution. Phylogenetically, sex chromosomes arose later than dioecy; i.e.,
they are evolutionarily younger than autosomes. Triggering and performing the differentiation program, they
form conservative-operative subsystems in the population and distribute roles among them according to
polygyny/polyandry. Because of this, the more monogamous and more polygamous sexes have respectively
broader and narrower reaction norms, irrespective of the gametic type [36]. Thus, two independent,
dichronously evolving subsystems separated by informational barriers are created. Regulating the rates of the
horizontal transfer (along and among chromosomes), sex chromosomes control and restrict the transfer of
new information to the female genome. These chromosomes mainly carry evolving genes that are being lost
and acquired. 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
can be called "antisex" rather than sex chromosomes. In view of their role, I should name them evolutionary
chromosomes.
The Y chromosome is a link between the genome and the environment (cytoplasm). For Drosophila, it
was shown that reproductive isolation between races is determined by the incompatibility of the Y
chromosome of one race with the cytoplasm of the other [45]. The Y chromosome is the "genomic gate" for
new information. This chromosome transforms ecological information into genetic information; i.e., it
creates new genes, mutations. The Y chromosome switches on male sex hormones and thus controls the male
reaction norm. It carries "genes of tomorrow;" initiates, accelerates, and regulates sexual dichronomorphism.
This chromosome provides "testing ground" and "quarantines" for new genes. In view of this, it should be
named "the ecological chromosome."
The contra-X chromosome transfers genes; links the Y chromosome and the female genome; and
stabilizes, relaxes, and destroys sexual dichronomorphism in phylogeny. It is the transportation chromosome,
in which young hemizygous in males genes are tested in ontogeny. As it is subjected to strong selection, it
may be a place for the elimination of useless or deleterious genes coming from autosomes.
The ipsi-X chromosome probably controls sex hormones and the female reaction norm (according to the
polygamy/type). This chromosome carries female genes and/has a high content of modifier genes for
quantitative traits.
1998 Evol Role Sex Chr Genetika Eng transl.doc
The Evolution of Sex Determination
and Sexual Dimorphism. Hormonal and Psychic Sex
In the process of progressive evolution, the determination of sex passes from genie (in hermaphrodites) to
chromosomal (in dioecious organisms) and genomic (in bees). This process is accompanied by an increase in
the level of differentiation and by the expansion of sexual dimorphism. Asexual organisms lack sexual
dimorphism; in hermaphrodites, it exists at the level of primary sexual traits (gametes, gonads, genitalia);
monogamous dioecious organisms have sexual dimorphism at the organismic level (secondary sexual traits);
polygamous dioecious organisms have it at the population level, including sexual dimorphism for the sex
ratio and dispersion. Bees have genomic sexual dimorphism (haploidy-diploidy) and new conservativeoperative differentiation into casts. This differentiation implies the division of the species into two ecological
subsystems: drones of other (rich) families and worker bees, which bring information from neighboring and
remote (honey plants) environments, respectively. Genetically, worker bees are females, but, according to
my concept, they function as a second ecological (male) sex. Thus, reproduction in bees is more advanced
from an evolutionary viewpoint. In fish species having dwarf males (and probably ants and termites, which
have casts), the second conservative-operative differentiation was based on the male genome, with the aim to
transport ecological information to the female genome from two different environments.
Based on the above considerations, the ecological subsystem could be distinguished in the ontogeny at
other levels of sex determination: genic → hormonal → psychological. Androgens are interpreted as
ecological hormones that bring the system closer to the environment, and estrogens are interpreted as
hormones protecting the system from environmental effects. At the behavioral and psychological levels, lefthanders and right-handers can be regarded as analogues of males and females, respectively. By analogy with
the sex ratio (males/females), the ratios androgens/estrogens and left-handers/right-handers (percentage of
left-handers) act as regulators of the distance from the environment and evolutionary plasticity that decreases
in optimal environments and increases in extreme environments [46].
Experimental confirmation of the key idea of the 1965 theory of dichronous evolution of sexes was first
obtained in 1987 [17]. The number of cell divisions in spermatogenesis is much higher than the
corresponding number in oogenesis; errors in DNA replication and repair are the main source of mutations
for molecular evolution. Consequently, the frequency of mutations in sex chromosomes must be higher than
in autosomes. On the basis of this, males were assumed to generate mutations (at least for the evolution of
mammals). It was repeatedly shown in Drosophila, silkworm, and mammals (including humans) that the
level of both spontaneous and induced mutation in heterogametic and homogametic males is higher than in
females [47]. Comparison of nucleotide substitutions in human and murine and rat autosomes, X
chromosomes, and Y chromosomes demonstrated that males act as the main source of mutation for
molecular evolution. Moreover, the ratio of evolution rates Y : A : X = 2.2 : 1 : 0.6 corresponds to the
theoretically expected 2 : 1 : 2/3 ratio [17].
Using a similar method, other authors compared the Y/X ratio of nucleotide substitution in synonymous
genes of humans, orangutans, baboons and squirrel monkeys. The Y-chromosome genes of these species
were shown to diverge faster and to a farther distance than the X-chromosome genes. Thus, in higher
primates, males also lead molecular evolution [18]. The title of both articles begin with the words maledriven evolution. The number of such studies has been increasing. I cited only two of them: the first and the
second, which, in my opinion, are the most elegant. These experiments fully confirm the theory of the
dichronous evolution of sexes at the molecular level. As the new concept of sex chromosomes is an
isomorphic extrapolation of the same ideology from the population to the chromosomal level, these studies
can be regarded as conforming the main points of my concept of sex chromosomes.
WHAT CAN BE EXPLAINED AND PREDICTED ON THE BASIS OF THE NEW CONCEPT?
The new concept revises century-old notions on sex chromosomes. Their significance receives a radically
different (sometimes an opposite) interpretation. For instance, their main role 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 1:1 sex
ratio rather than maintain it. Based on the new concept, the phenomenon of the unequal Y → X crossing over
1998 Evol Role Sex Chr Genetika Eng transl.doc
and the association of the Y chromosome with retroviruses can be explained. DNA regions of murine X and
Y chromosomes were studied by hybridization with retroviral DNA. DNA of murine retroviruses was
revealed in Y chromosomes of ten different lines of mice, whereas in their X chromosome, this DNA was
absent. Another phenomenon that is explained on the basis of the new concept is the capacity of the sperm of
many species to bind alien DNA and transfer it into the egg by fertilization. This was first observed in 1971,
in an experiment on the introduction of the DNA of virus SV40 in rabbit sperm [48]. However, at that time,
this discovery did not receive proper attention. Later, it was confirmed and extrapolated to other animal
species (mice, sea urchins, bees, chickens, swine, cattle, and humans). Studies in which sperm was used as a
vector for producing transgenic animals have received much consideration [49]. Thus, based on my concept,
an important conclusion (prediction) can be made: alien DNA or viruses are bound only by Y-chromosomecarrying sperm; therefore, transgenic animals must consist mostly of males.
Studies of mutation bursts, insertion mutagenesis, and "jumping genes" are intensely developing lines of
research that are directly related to the concept of sex chromosomes. This concept can explain where and
why genes "jump," why the transpositions of mobile elements depend on ecological stresses (temperature, Yradiation, chemical substances, hybrid dysgenesis, etc.), why different genes mutate simultaneously, what the
source of mutations is (oogenesis or spermatogenesis), autosomes or sex chromosomes, X or Y
chromosomes, and so on. As far as I know, these questions have not been even posed.
The concept offers a different explanation to numerous obscure events listed at the beginning of this
paper. For instance, the condensation of the X chromosome in the female genome (Barr's body), irrespective
of the gametic type, is interpreted as a barrier to the spreading of new, nontested information in females
rather than gene-dose compensation; as pointed out above, the latter explanation is a fallacy. Euchromatic Y
chromosomes of plants and nucleotide repeats dispersed among chromosomes are explained by the relatively
late evolution of sex differentiation in plants as compared to animals [11]. If nucleotide repeats are required
for the formation of new genes (before the appearance of sex chromosomes, new genes arose in all
chromosomes), the dispersion of repeats in chromosomes reflects an earlier stage of sex differentiation.
The ecological Y chromosome must be closely associated with stress. This explains a number of
previously known facts, e.g., the relatively larger size of the Y chromosome in some ethnic or social groups
and the higher dispersal of this chromosome in rodents in zones of high seismic activity. I believe that, in the
latter case, it is explained by stresses from frequent earthquakes rather than by high radiation levels or radon
concentrations, as argued the authors. A prediction may be made of the change in size and/or dispersion of
the Y chromosome in regions of frequent or strong earthquakes, other calamities, and social stresses
(genocide, wars, migrations, hunger, etc.). The same must happen in intensely selected animals and plants.
The present paper is theoretical (see the epigraph and [50]). It is devoted to evolutionary relationships
rather than concrete mechanisms underlying horizontal gene transfer, which requires special investigation.
However, I hypothesize that mitochondrial DNA is associated with the Y chromosome, which acts as a
source of induced and directed evolutionary potential rather than spontaneous and random mutations. This is
a program for future investigation.
ACKNOWLEDGMENTS
I am grateful toYu.G. Rychkov andYu.F. Bogdanov for their discussion, helpful criticisms and advice.
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