A variety of mammals, including primates, communicate
through pheromones, which are volatile chemical signals
produced by glands and detected through the vomero-nasal
organ (VNO). This manner of communication is effective
and fundamental for eliciting innate responses to locate
sexual partners and inducing sexual behavior. Pfau, Jordan,
and Breedlove, (2019) hypothesized that progressive
degeneration of a single-gene coding for pheromones receptors
in the VNO of mammals may have triggered a cascade
of functional and behavioral consequences that facilitated
the development of new modes of sexual communication,
including same-sex sexual behavior in primates and humans.
This hypothesis is compelling, testable, and heuristic.
In their Target Article, Pfau et al. (2019) suggest that, during
primate evolution, inactivation of the transient receptor
potential cation channel 2 (TRPC2) gene caused a shift from
strictly pheromonal-driven sexual behavior toward a more
flexible sexual response that allowed for occasional samesex
sexual behavior. In other words, a more flexible sexual
response to different and varied stimuli might have allowed
the use of sex, including same-sex sexual activity, in both
sexes, in contexts beyond reproduction such as dominance
displays, reconciliation, and appeasement (de Waal, 1989).
The main evidence in support of Pfau et al.’s (2019)
hypothesis comes from knock-out (KO) TRPC2 mice. Pfau
et al. found that this experimental strain of KO mice exhibits
delay development and altered intraspecific interactions such
as sex discrimination and male–male aggression (Leypold
et al., 2002; Stowers, Holy, Meister, Dulac, & Koentges,
2002). Most importantly, compared to wild mice strains,
adult male and female KO TRPC2 mice were observed to
engage in unprecedented levels of same-sex sexual behavior
including mounting and pelvic thrusting.
Comparing KO TRPC2 mice and Old World monkeys,
Pfau et al. (2019) furnish evidence that catarrhine primates,
which lack a VNO, also have a nonfunctional TRPC2 gene.
They argued that like KO TRPC2 mice, catarrhine primates
exhibit reduced aggressions and delayed development. Based
on these comparisons, they proposed that this TRPC2 single-
gene inactivation might explain not only the cause of
same-sex sexual behavior in nonhuman primates, but also the
cause of sexual orientation in humans. Further, they proposed
that the inactivation of the TRPC2 gene promoted a series
of behavioral and social transformation that are common in
domesticated animals and self-domesticated humans (Hare,
2017; Hare, Wobber, & Wrangham, 2012).
The primate data do not fit Pfau et al’s (2019) hypothesis
perfectly, however, and as the authors admit, there are some
prosimians (e.g., brown lemurs, Lemur fulvus, and sifakas,
Propitecus verreuxi; Bagemihl, 1999), as well as some New
World monkeys (e.g., common marmoset, Callitrix jacchus,
and Geoffroy’s tamarin, Saguinus geoffroyi) that have intact
TRPC2 genes and show same-sex sexual behavior (e.g.,
Manson, Perry, & Parish, 1997; Rothe, 1975). Conversely,
there are a number of Old World monkeys such as gibbons
and olive colobus (Procolobus verus) that lack a functional
TRPC2 gene, but have never been shown, in field observations,
to exhibit same-sex sexual behavior in either sexes.
However, these are minor exceptions, and in general Pfau
et al.’s hypothesis is supported by the primate data.
Pfau et al.’s (2019) hypothesis could also be tested in
other mammals known to have same-sex sexual behavior.
For example, dogs (Canis spp.) are known to have same-sex
sexual behavior both in females (Beach, Rogers, & LeBoeuf,
1968) and in males (Dagg, 1984), and at the same time they
are macrosmatic with a keen olfaction. Other possible animal
models include domesticated cattle and wild bison, since
same-sex sexual behavior has been extensively reported for
both (Jezierski, Koziorowski, Goszczyński, & Sieradzka,
1989; Lott, 1983). What about their vomero-nasal receptor
activity? Contrary to my expectation, dogs and cattle have a
markedly degenerated VNO, and most of the genes coding for
receptors in the VNO have completely degenerated and are
inactive, while their keen olfaction is due only to the primary
olfactory epithelium (Young & Trask, 2007). This evidence
from domestic mammals is, thus, consistent with the hypothesis
that a relation exists between vomero-nasal pheromone
receptor activity and same-sex sexual behavior. However,
there is evidence suggesting that in cattle the TRPC2 gene
is present and active contrary to Old World monkeys (Grus,
Shi, Zhang, & Zhang, 2005).
Research on the genes implicated in pheromone detection
and the evolution of the VNO of mammals (Moriya-Ito,
Hayakawa, Suzuki, Hagino-Yamagishi, & Nikaido, 2018)
suggests that there are a multitude of genes classified in two
super-families, which are expressed in the VNO, and some
of them in the main olfactory epithelium as well. Both the
vomero-nasal receptor genes type-1 (V1Rs) with single exon
and type-2 (V2Rs) with multiple exons are seven-transmembrane
G protein-coupled receptors (Nei, Niimura, & Nozawa,
2008). Both vomero-nasal receptor families have closely
related homologs in the vertebrate taste system: V1Rs are
closely related to T2R bitter taste receptors (Chandrashekar
et al., 2000), and V2Rs are closely related to T1R sweet and
umami taste receptors (Hoon et al., 1999).
Grus et al. (2005) found that these genes originated in
fishes, are extremely variable among mammals, and evolved
through duplication, deletion, and inactivation. Vomeronasal
receptor coding genes belong to the super-family of
genes with the highest numerical variability across species.
The proportion of intact V1Rs relates to multiple aspects of
VNO anatomy, including its relative size (Garrett & Steiper,
2014). The large variation of V1Rs in mammals may be an
adaptation to a broad range of environments, and the comparison
of V1Rs repertoires is critical for inferring the importance
of the VNO to each species (Garrett & Steiper, 2014).
Moriya-ito et al. (2018) reconstructed the phylogeny of
V1R genes in primates, almost all code for receptor proteins
that are present in the VNO. Moriya-ito et al. suggested
that, in general, V1Rs underwent positive selection, grew in
number, and are expressed in the VNO of prosimians. This
correlates with the socioecology of many prosimians, which
are nocturnal, solitary, and communicate extensively with
pheromones, including for mating (Dixson, 1995). It has been
also found that in Old and New World primates V1Rs show
a generalized trend toward degeneration (Grus et al., 2005;
Yoder & Larsen, 2014) and this regressive selection happened
not only in primates, but also in whales and bats (Grus
et al., 2005). Yoder and Larsen (2014) showed a reduction in
the number of intact V1Rs in anthropoids for which the VNO
was reduced or vestigial (Smith et al., 2002, 2011), which
suggested a correlation between the progressive inactivation
of V1Rs and reduction of the VNO. Young and Trask (2007)
also found that V2Rs families have completely degenerated in
humans, chimpanzees, macaques, cattle, and dogs. Each now
possesses 9–20 pseudogenes, but no intact V2Rs.
Rather than hypothesizing a single-gene inactivation as in
Pfau et al.’s (2019) Target Article, is it possible that general
regression of vomero-nasal functions is causally associated
with release from strict sexual response to pheromones and,
by extension, an increase in same-sex sexual behavior? It is
noteworthy that visual sexual signals, like the genital skin
swellings, are very widespread among Old World monkeys
and apes, but not in prosimians and New World monkeys
(Dixson, 1983). It has been proposed that sexual swelling
might visually signal receptivity in widely dispersed social
animals like chimpanzee, macaques, and baboons, but could
also be interpreted as evidence of the substitution of pheromone
signals with visual ones.
Now we come to my main concern with the argument forwarded
by Pfau et al. (2019): TRPC2 inactivation seems like
just one of the many genes involved in pheromone communication
in the VNO, which underwent regression partly in
New Word monkeys and completely in Old World monkeys,
as in other diurnal mammals. Why, then, suggest a specific
gene, TRPC2, as the driver of the whole behavioral transformation?
Instead, why not hypothesize that these behavioral
transformations resulted from the combined inactivation
and degeneration of a variety of genes involved in pheromone
detection and in the development and function of the
VNO. It could be argued, alternatively to Pfau et al.’s Target
Article, that the general regression of these genes allowed
the progressive shift from chemical communication toward
visual communication, including same-sex sexual behavior
as seems to have happen in New and Old World primates,
but also in sea mammals, bats, cattle, and dogs (Young &
Trask, 2007) .
The only evidence reported in Pfau et al.’s (2019) Target
Article against this more general hypothesis is that in
Gαi2 KO mice inactivation of this g-protein disrupts aggression,
but sexual behavior is not affected (Norlin, Gussing,
& Berghard, 2003). Disruption of Gαo, another g-protein
crucial for VNO function, also reduces aggression without
impacting sexual behavior (Chamero et al., 2011). Norlin
et al. (2003) reported unaltered sexual partner preference
in their Gαi2 KO mice, but Chamero et al. (2011) do not
report on any sexual behavior, so we do not know whether
any sexual changes occurred in their Gαo KO mice. Apart
from these cases, were KO mice ever produced for all other
V1Rs and V2Rs that are expressed in the VNO of mammals?
What modification in sexuality might such mice show?
Awaiting further evidence, my interpretation, at present, is
that circumstantial data best fit the more general hypothesis
for a global reduction of gene activity coding in the VNO.
We can imagine that, whenever chemical reception and communication
receded in favor of the visual communication,
selection pressures change. This might have begun when
ancestral primates invaded a diurnal niche, increased in social
complexity, developed trichromatic vision, and adopted the
use body signals (e.g., genital swelling), thereby eliciting
the evolution of sexual, rather than chemical, communication
signals (Moriya-Ito et al., 2018). Diurnal vision might
have enhanced brain size and reduced splanchno-cranial size
(Camperio Ciani, 1989), thus reinforcing reduction in VNO
size. Once sexual behavior was released from the limitation
of chemical activation, then sexuality could become much
more flexible and could be used by ancestral primates for
social communication in a variety of contexts. In extant primates,
same-sex sexual behavior might be used to modulate
aggression, reconcile conflicts, reinforce dominance rank,
and reduce social tension, thereby enriching social complexity.
The extreme example is the complex use of sexuality by
our closest relative the bonobo (Pan paniscus), in which sex
is used in the largest variety of social contexts, compared to
all other primates (Manson et al., 1997).
If my interpretation of the evidence is correct, no single
gene, such as TRPC2, but rather a whole set of genes (V1Rs,
and possibly V2Rs) lost importance. All those genes were
implicated, in one way or another, with pheromones detection
and communication in the VNO. When the VNO becomes
less important for sociosexual communication, its associated
genes become less useful and they experience more relaxed
selection pressure. The loss of selection pressure allows
for mutations to arise, such as stop codons, and generates
inactive pseudogenes (Moriya-ito et al., 2018). A relevant
exception pertains to those genes that shift function from
pheromones detection to oxygen detection. These genes are
maintained under stabilizing selective pressure, thus preserving
their functionality (Niimura, Matsui, & Touhara, 2014).
In sum, I would like to see stronger evidence that the loss of
a functional TRPC2 gene played an exclusive role in evolution
of same-sex sexuality, as opposed to a general evolutionary
transformation in mammals—not just primates—of
many vomero-nasal receptor genes, toward amplification or
degeneration.
A final critique of the Target Article, but one that is no less
relevant, is that Pfau et al.’s (2019) hypothesis does not apply
to human homosexuality. Most Old World primates have been
observed to engage in same-sex sexual behavior. Very occasionally
this involves some homosexual partner preference
(Vasey, 2002), but never exclusive homosexual orientation
as in humans. In humans, same-sex-sexual behavior lost its
social communication function almost completely to become
a sexual orientation.
I am skeptical that the olfactory and pheromonal processes
posited by Pfau et al. (2019) caused a homosexual “orientation”
in humans. The evolutionary dilemma of human
homosexual orientation has little to do with same-sex sexual
behavior, which is only one ingredient of the phenotype.
Homosexuality in humans is characterized by a novel and
specific phenotype: an individual exclusively attracted sexually
and romantically to same-sex individuals. This is the
evolutionary dilemma, exclusive same-sex sexual attraction,
which inhibits reproduction and reduces fertility. How could
such a phenotype evolve and how could it be maintained in
the population at a constant, albeit low, frequency? If this
phenotype has a genetic basis, then it should become extinct
rapidly, which we know does not happen (Camperio Ciani,
Battaglia, & Zanzotto, 2015). What are the fitness advantages
of exclusive same-sex sexual behavior in our species? Occasional
same-sex sexual behavior does not exclude heterosexual
sex and reproduction. On the contrary, it might provide a
selective benefit to individuals, in reducing aggressiveness
by using sexual pleasure to facilitate appeasement, but even if
this is true, it is generally not the case in humans. In animals,
same-sex sexual behavior enriches communication, sociality,
and ultimately benefits individuals, so there is no evolutionary
dilemma here. This is the ultimate reason that same-sex
sexual behavior evolved in many social organisms (Bagemihl,
1999). That said, these social uses of same-sex sexual behavior
do not produce exclusive homosexuality.
Pfau et al., in the Target Article, contend that the absence
of reports on possible homosexual orientation in primates,
including bonobos, might be ascribed to the possibility that
researchers not have detected it yet. They suggest that the
absence of evidence is not evidence of absence, but in this
case, it is improbable. Vasey (2002) reported facultative
(i.e., nonexclusive) homosexual preference for a few animals,
including the domestic rams and few other ungulates,
as well as female Japanese macaque (Macaca fuscata). These
females occasionally show a preference for same-sex sexual
partners over opposite-sex alternatives, but nevertheless they
mate heterosexually and they all reproduce, according to my
direct experience (Camperio Ciani, 1997; Corradino, 1990).
Moreover, most primatologist will acknowledge that primates
are difficult to locate in the wild, especially forest dwelling
ones; however, once located, sexual behavior becomes overt
(both visually and vocally) and very conspicuous in most
species, if not all. Sexual interactions in wild primates are
much easier to observe than in our species. Infinite hours of
observation, including in the wild, focusing on sexual behavior
in males and females have been undertaken by ethologists.
With such a large sample, it would have been easy to
locate individuals that engage in exclusive same-sex sexual
behavior, but no one has. I have been observing several species
of macaques in North Africa and South-East Asia and
commonly observe same-sex behavior among both females
and males, but never once have I observed a single-subject
mating exclusively with same-sex partners (Camperio Ciani
1986; Camperio Ciani, Mouna, & Arhou, 2000; Camperio
Ciani et al., 2005). There is only one species in which some
males exhibit a homosexual orientation, but this is in sheep,
not in primates, and is restricted to domesticated, that have
been artificially selected. Domestic rams can thus furnish
information on the neurophysiology and endocrinology of
homosexuality, but they cannot furnish information about
how natural selection might have produced such a phenotype
(Roselli, Larkin, Schrunk, & Stormshak, 2004).
Pfau et al. (2019) suggested that if homosexual individuals
occur in small groups, as might be the case for many
primates, there might be no possibility of finding a homosexual
partner with the same orientation. This, they suggest,
might help account for the lack of observations of exclusive
same-sex sexual partner preference in primates. This speculation
is untenable. First, many primates, including baboons,
macaques, and vervets, live in large multi-male multi-female
groups. If occasional same-sex behavior is already present
within a species—as is the case for many primates—an exclusively
homosexual individual, should one exist, could find
several same-sex partners with whom they could engage in
sex, even if those partners were not exclusively homosexual
themselves. This in fact happens also in our own species,
where exclusive homosexual individuals can find occasional
partners who are heterosexual (Whitam, 1992).
In conclusion, the hypothesis that the decline of pheromonal
communication allowed for the evolution of social
complexity, including same-sex sexuality, is compelling. In
my view, the idea that a single gene, and not a whole set of
genes, promoted this shift needs further testing. Regardless,
Pfau et al.’s (2019) hypothesis while heuristic for the evolution
of same-sex sexuality in nonhuman primates, fall short
of explaining the evolution of an exclusively homosexual
phenotype as seen in humans.
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