body odour, genetic variability, and sexual orientation: A
reply to D. Oliva
Fink and Nick Neave
Ludwig-Boltzmann-Institute for Urban Ethology, University
of Vienna, Austria.
2. Human Cognitive Neuroscience Unit, Division of Psychology,
Newcastle upon Tyne, UK
In a letter to the Editor, D. Oliva has raised the hypothesis
that there might be a guiding thread through pheromone communication
from unicellular organisms up to humans, which may serve as
an explanation for human homosexual orientation. Although we
do not want to reject this hypothesis in its entirety, as links
between olfactory signals and human sexual orientation remain
poorly understood, the argument seem to be too simplistic in
light of evolutionary adaptationism and neurobiological research,
and requires further investigation and discussion. Our reply
should not be regarded as criticism, but rather to encourage
further academic discussion.
Evolutionary theory suggests that humans have evolved adaptive
mechanisms to increase genetic variability when searching for
a mate. Within the mating game an individual should therefore
seek honest signals of genetic quality in a potential partner.
This ability is also essential for many other aspects of social
behaviour, such as the maintenance of stable social groups,
inbreeding avoidance, and the modulation of competitive relationships
(see ). Several studies have suggested that the polymorphic
Major Histocompatibility Complex (MHC) in animals - referred
to in humans as the Human Leukocyte Antigen (HLA) - is under
natural and sexual selection, and may provide such an honest
cue, as its immunological function is the discrimination of
self and nonself within the immune system.
In rodents it has been shown that body odour is significantly
influenced by the MHC and that it can be discriminated by members
of different species . Wedekind et al. [3, 4] have shown
that the HLA influences both body odours and body odour preferences
in humans, as females rate body odours from males with differing
HLA as more pleasant than odours from males with similar HLA's.
Further, they report that scorings of pleasantness of body odour
were correlated negatively with the degree of MHC similarity.
Ober et al.  found that isolated human populations avoid
mating with individuals with same HLA haplotypes than expected
by chance. These authors consider this as evidence that the
HLA or linked genes influence human mate choice. Consequently,
MHC/HLA seems to affect body odour preferences by the degree
of similarity or dissimilarity. According to evolutionary theory,
the reason for such a conserved mechanism - which is not exclusively
human - is the increase of heterozygosity in the progeny.
Of course, it has been proposed that similarities between the
regulatory mechanisms governing yeast (Saccharomyces cerevisiae)
mating-type genes and mammalian MHC genes exist  but as D.
Oliva states, the fusion of two haploid cells, generating one
diploid zygote, creates individuals with different genomic inheritance,
and high genetic variability in the population. As for humans,
the reason for sexual recombination is the better possibilities
of adaptation to the environment. The suggestion of a common
pattern in homosexual orientation instead of finding a heterosexual
mate through olfactory communication from unicellular organisms
up to humans requires further explanations on the possible evolutionary
advantages such a mechanism.
From a neurobiological point of view we know that the olfactory
systems maintains a significant proportion of the genomes of
many higher organisms that is devoted to encoding the proteins
of smell . However, the extent to which olfactory signals
may contribute to homosexuality remains unknown. Some research
has demonstrated that while females demonstrate hypothalamic
activation when smelling an androgen-like compound, male hypothalamic
activation occurs in the presence of an estrogen-like substance
. In other words, it seems that there is a different behavioural
response in humans to sex-dissociated olfactory hypothalamic
activation. If we theoretically extend this finding, a change
in sexual orientation mediated by olfactory signals would mean
that the brain of a heterosexual individual is designed in a
way that it reacts to olfactory signals of the other sex but
the brain of a homosexual individual is activated by same-sex
odours. To our knowledge this interesting hypothesis has as
yet, received no empirical support.
In humans, hypothalamic nuclei have been shown to have a neuronal
density in homosexual men that is approximately half of that
seen in heterosexual men [9, 10]. Additionally, homosexual men
exhibit a positive Luteinizing Hormone (LH) response to administered
oestrogen that is intermediate between women and heterosexual
men (see for review ), However, Hendricks et al.  observed
no significant differences between heterosexual and homosexual
subjects in the likelihood of their exhibiting elevated LH concentrations
in response to exogenous estrogens. Elias and Valenta  have
postulated that anatomic differences in the anterior hypothalamic
nuclei that regulate sexual orientation in males may lead to
alteration in the gonadotropin releasing hormone (GnRH) pulse/frequency
leading to a more female-type pattern of gonadotropin secretion
in homosexual males. However, the question remains, what could
be the reasons for such a change of density of the hypothalamic
nuclei? As a consequence we have to ask when sexual orientation
is determined during ontogeny?
There is considerable evidence that sexual orientation is hormonally
encoded into the brain in fetal and/or neonatal life influenced
levels of testosterone and oestrogen. Robinson and Manning 
have shown that the ratio of the length of 2nd and 4th digits
(2D:4D) is negatively related to prenatal testosterone and positively
to oestrogen. They found that 2D:4D was lower in a sample of
homosexual men than in sex- and age-matched controls. These
data tend to support an association between male homosexuality
and high fetal testosterone. Homosexual orientation has also
been suggested to be possibly related to hemispheric functional
asymmetry . This may fit to the link between lowered 2D:4D
in homosexuals and the cerebral lateralization effects caused
by prenatal testosterone and estrogens [16, 17].
Taken together, prenatal neuroendocrine events are in all likelihood
a factor in the development of human sexual orientation and
functional brain asymmetries. However, the precise contribution
of biological factors to the development of sexual orientation
remains to be elucidated. It is not yet clear if biological
factors directly wire the brain so that this will support a
particular sexual orientation but linking yeast and human sexual
orientation seems to be at this stage too tentative. Therefore,
it seems imperative to consider homosexual orientation not exclusively
as biologically dependent, but rather as nature and nurture
dependent neuroendocrine alterations of sexual brain organization.
Only this may liberate homosexuals from pathological labelling
and other forms of discrimination.
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