ISSN 2079-0597, Russian Journal of Genetics: Applied Research, 2018, Vol. 8, No. 1, pp. 1–10. © Pleiades Publishing, Ltd.

, 2018.
Original Russian Text © E.V. Daev, 2016, published in Ecologicheskaya Genetika, 2016, Vol. 14, No. 3, pp. 3–12.

Biological and Social Aspects of Human Sexual Orientation:

Chemocommunicative Hypothesis
E. V. Daev
Department of Genetics and Biotechnology, St. Petersburg State University, St. Petersburg, 199034 Russia
e-mail: mouse_gene@mail.ru
Received August 25, 2016; in final form, October 7, 2016

Abstract⎯Failure to understand the role of biological and social factors in the formation of some socially
important traits in humans could result in unjustified tension in interpersonal relationships. It is caused by a
distorted perception of frequently unreliable information, its ambiguity due to the uncertainty of the termi-
nology used and, as a consequence, the impossibility of its correct analysis. Using the term sexual orientation
demonstrated the way how genetic understanding of the trait’s formation and data on the control mechanisms
of sex formation may clarify and complement our knowledge on the subject. The hypothesis of the chemo-
communicative model in the formation of sexual orientation in humans is discussed.

Keywords: sex, sexual behavior, sexual orientation, role of genes and environment, chemosignals, chemocom-
municative model
DOI: 10.1134/S2079059718010045

INTRODUCTION accompanied by the share of studies containing genetic

Synecological intraspecific relationships, in particular
regulating the reproduction of the species, might play a
significant role in the formation of the inherited variability
and spatial-temporal structure of the animal populations
[1, 2]. Nevertheless, insignificant attention has been paid
to the scientific study of these aspects of intraspecific rela-
tionships, especially in humans. According to this point of
view, the exploration of the possible mechanisms of the
formation of sexual orientation in humans as one of the
factors determining the reproductive potential of the
Homo sapiens species appears to be promising.
Nowadays, the problem of the existence of differ-
ent variations of sexual orientation (hereinafter, SO)
has been attracting increasing attention. Considering
the ambiguous attitude of the world community to
several SO variants, the role of biological, genetic, and
social mechanisms in its formation appears to be espe-
cially urgent [3].
A comparison of the publications according to the
Scopus database every five years from 1996 to 2015
demonstrates the following points:
(a) The number of publications on human sexual
behavior, which grew by a factor of 2.3 (from 10422 during
the first five years to 24185 during the last five years), was
characterized by an increase in the share of studies con-
taining the terms gene and genetic from 5 to 8%;
(b) In contrast, the consistent increase in the number
of studies on sexual orientation (quadrupling between the
first five-year period and the last five-year period) was
terminology decreasing from 8–10 to 5%.
One of the possible reasons for a decreasing fre-
quency of genetic-based studies on SO could be the
unclear definition of this trait and the lack of corre-
spondence of the definition with the formal require-
ments of classic genetics.
COMMON REPRESENTATION
OF THE SEXUAL ORIENTATION TRAIT
Sexual orientation is a trait expressing the sexual
attraction to the same-sex (homosexuality), opposite-
sex (heterosexuality), or both-sex (bisexuality) indi-
viduals [4, 5]. It is also determined as the direction of
sexual interest to subjects of the same, opposite, or
both sexes, especially when this orientation was
mainly based on physiological rather than sociological
reasons [6]. The definition of SO as a variant of the
preference of sexual activity with subjects of a certain
sex [6], etc., could be found. The ambiguity of such
definitions is notable due to the use of extremely vague
words such as attraction, interest, and activity. For
instance, sexual attraction is divided into physical and
romantic or emotional [4]. Such epithets add little to
the scientific knowledge of the nature of SO.
The nature of the SO trait is extremely complex
(complex trait) and consists of many labile components
in each case depending on the interaction between a
unique genotype and not less unique combinations of
changing environmental factors.

1
2 DAEV
In order to better understand SO as a phenotypic
trait for subsequent study, it should be taken in mind
that in each case SO represents a specific set of forms
of an individual’s behavior toward others. Let us give
working definition of SO as the summative behavioral
response of the person to the brain’s analysis and subse-
quent synthesis of all outward information of the pri-
mary, secondary, and tertiary sexual parameters of
other individuals. Moreover, the unique SO of each per-
son is determined by the biological and gender charac-
teristics of the state of its organism at every moment.
Only specificity of manifestation of at least one form
(or multiple forms) of behavior make it possible to
evaluate SO by a researcher. Nevertheless, such a sum-
mary complex of behavioral traits represents the most
important factor of synecological relations directly
correlated with reproduction in both humans and
other animal species that reproduce sexually.
Let me propose in a simplified manner the sequence
of events finally resulting in the formation of SO. We ini-
tially try to give a working definition of the term sex,
since sexual orientation is inextricably linked with the
existence of the male or female sex and their behav-
ioral differences.
DIFFERENTIATION BY SEX
AND SEXUAL BEHAVIOR
The term sex can be determined as follows:
Sex represents a single-unit inherited multicompo-
nent complex of specific characteristics manifested in two
phenotypes designated as man and woman in humans
(male and female in animals).
In fact, male and female sexes represent the two
arrays of phenotypes distinguished by a set of specific
characteristics. Sometimes the integrity of such a set
might be significantly impaired, which results in the
impossibility to specify the sex. In this case, an indi-
vidual (animal or human) is called intersex.
According to one of the proposed models of sexual
differentiation in mammals, the sex is determined by
the genes of the sex chromosomes at the initial stage.
They both control the formation of gonads and partic-
ipate in the local specialization of brain tissue via the
interaction of hormonal and autonomous cellular
mechanisms with so far unidentified regulatory mole-
cules [7, 8].
Sex in humans is considered to be primarily deter-
mined by the presence of sex chromosomes (XX or
XY), which were captured in a zygote. According to
the Ensembl genome browser, release 83 (2015) [9],
the length of the human Y chromosome, based on
whose genetic material the differences between femi-
nine and masculine phenotypes are represented, is
only ≈1.6% of the reference genome (≈57/3547 Mb).
Considering diploidy, the differences between male
and female organisms by the number of genetic mate-
rials comprise only ≈0.8% and even less if we consider
RUSSIAN JOURNAL OF GENETICS: APPLIED RESEARCH
the presence of pseudoautosomal regions. The differ-
ence in the number of coding genes is ≈0.2–0.4%.
Accordingly, the difference between female and male
phenotypes is likely to be strongly exaggerated and
overemphasized. Based on a simplified representation
of the proportionality between the number of genes
and the number of gene-controlled phenotypic traits,
an individual difference should only comprise 0.2–
0.4% of all phenotypic traits (Fig. 1).
At the same time, the published data indicate that
male and female human phenotypes also depend on
the allelic composition of the parental haplotypes of
autosomes. For example, the existence in a zygote of
two recessive mutant alleles of the CYP21A2 (chromo-
some 6) gene encoding 21-hydroxylase—an enzyme
responsible for the adrenal steroidogenesis—might
result in the phenotypic transformation of an organ-
ism with female sex chromosomes into the male one.
The degree of masculinization would depend on the
combination of certain mutant alleles [10]. In extreme
cases a man with XX-chromosomes can be distin-
guished from a man with XY-chromosomes only if he
goes to physicians regarding the question of infertility
in marriage.
The SRD5A2 gene is located on autosome 2. The
alleles of this gene encode different variants of 5-alpha-
reductase, the enzyme involved in converting testoster-
one into dihydrotestosterone. Mutations affecting
enzymatic activity cause more-or-less expressed femi-
nization in people with XY-chromosomes [11].
The presence of distinct alleles in the aromatase
gene (CYP19A1) located on chromosome 15 results in
feminization of both male and female phenotypes [12].
It is likely that the contribution of autosomal genes
involved in determining the sex in humans (except for
CYP21A2, SRD5A2, and some others) has been sig-
nificantly underestimated. This was confirmed in a
model of transgenic mice XEOSox9 and XOSry, Eif2s3x.
The experiments on transgenic overactivation of the
Eif2s3x gene located on the X-chromosome and of the
autosomal Ѕох9 gene demonstrated spermatogenesis
induction and producing mice offspring was possible
even in the absence of the Y-chromosome, although it
above all determines the male phenotype under the
natural conditions [13].
Therefore, multiple intersexual variants differing in
the degree of phenotype expression between the typi-
cal female and male and so different SO variants might
exist. Everything is determined by a specific mutation
in a particular gene, the alleles’ content in other genes,
and environmental conditions, including socially
determined factors.
To date the most famous androgen insensitivity
syndrome (AIS) was associated with mutations in the
AR gene (located on the X-chromosome) encoding the
androgen receptor. An individual bearing XY-chromo-
somes in some cases could be indistinguishable by
phenotype (except for infertility) from women with
Vol. 8 No. 1 2018