Stanford University. Let us get started here. So picking up from the other
day, where have we gotten? Not very far. Behavior-- full
range variability of sexual behaviors,
fixed action patterns. Is this kind of dark here? No. Seeing in some ways
what's interesting is the conservative nature of
sexual behavior across species, other ways the sheer
variety, trying to make sense of what aspects
of human behavior are unique, all of that. Then beginning to march
backwards-- what goes on in the nervous system one second
before sexual behavior occurs? And marching through the
relevant limbic structures, some of which have
strong sex differences, some of which don't. Seeing some ways in
which neurotransmitters in the whole world of dopamine
complicates things enormously, marching through there. Where we had then gotten
to was asking, OK, so what sort of bits of information
in the environment, what sort of ethological
releasing stimuli can trigger the nervous
system to do its thing? And you've got the drill by now. So what we had done
was look at a couple of different sensory
systems, and we had just started to wallow in
the world of pheromones, of pheromonal communication. What we ended with was number
one, the hormone dependency of generating sexually
meaningful pheromones, that business being
that males have to have sufficient testosterone. Females have to have
ovaries on board to be producing pheromones
that carry sexual meaning. What is the reason for that? The fact that a whole lot
of the actual chemicals that constitute sexually meaningful
pheromones are made out of some sex hormone
breakdown products and the sheer bizarrity but
eventual wonderful clarity of what's up with perfumes. Then transitioning
at the very end to the business about how your
endocrine status has a lot to do with your perception of
pheromones from the other sex, that women who are
ovariectomized to low estrogen levels have trouble being
able to differentiate the smell of males and
females, men and women. And estrogen replacement
takes care of that. The exact same thing when you
take away testosterone for men, and what we were just about to
get to before we had to stop was one additional
thing, which is one's opinion about
the pheromones that you were smelling. And this goes back
to a literature, a really interesting
one showing that not only are women
better at differentiating between the smell
of men and women-- gonadally intact men and women. Not only are they
better at doing that around the
point of ovulation, but their preference
for the smell of males gets more dramatic around
the time of ovulation. Meanwhile, over at the
male end of things, something rather
similar in terms of what you make of the pheromones. And this was a famous classic
study in which women volunteers had their armpits swabbed
at different points in their menstrual cycle and
put into little sealed jars, and all sorts of male
volunteers sniffing them and rating their pleasantness. And what you found
was on the average, the odorants were rated in
the unpleasant direction, but they were rated as least
unpleasant around the time that women are ovulating. And I think once we get
past the world of armpit smells in little
glass jars, one can get into the more ethologically
relevant world of men prefer pheromones derived from
women around the time when women are ovulating. Once again, a
testosterone-dependent phenomenon. What we now begin
to look at are some of the physiological effects of
sexual pheromones between sexes within sexes. One example you heard about
in the very first lecture, which is that whole business,
that Wellesley effect the ability of females of all
sorts of different species, including college
freshman human females, to synchronize each
other's cycles, this being done with pheromones,
intersexual perception of pheromones, so
the Wellesley effect. What's also shown in a
number of rodent species is the pheromones, the
smell of an adult female, will delay the onset of
puberty of younger females. And how might one frame that? That is utterly a gene
competition sort of strategy there. This is reproductive
competition. If you arrest the development
of the other females around you, you are going to leave
more copies, et cetera. Meanwhile, a
literature of intramale physiological
effects-- what happens to the physiology of
males in various species when smelling the
pheromones of other males? What you see, first
off, is it depends on who the other guy you're
smelling, the dominance rank. In lots of rodent species and
some primate species as well, males are able to
differentiate between smells of very high ranking males
and very low ranking ones, and what do you know? They're not all that upset
about the low ranking ones. What do you see in terms of
the physiological effects in the number of
species when males are smelling the pheromones
of big, healthy, strapping, androgenic other males? In some cases, it drives down
their testosterone levels. They're totally
physiologically intimidated, this being some great
competitive strategy for males who could pump
out just the right kind of suppressive pheromones. In other species,
though, what you see is a sudden burst
of sperm production, and what's that about? Another version of
the same logic-- this is a counter-strategy. If males have come up, evolved
the means in various rodent species to generate pheromones
that will drive down testosterone levels in
opponents, what males also want to have evolve with some
mechanism of when smelling those sorts of pheromones
to try to counter that by increasing sperm production. What we have here is a
co-evolutionary arms race. Terms of interactions of
pheromones between the sexes, and what I've been
doing here is describing all this without
making use of this, so what you see
is physiologically when the female is
the pheromone donor, and the other recipient is
a female in terms of, say, puberty, decreasing
puberty onset, and what we just saw with
male is donor versus male is in some ways suppressing
some endpoint's testosterone, in some ways increasing
sperm production. What you see in lots
of rodent species, when you're looking at
between genders, when males are the source of
pheromones among rodents, it accelerates puberty
onset in the females. And when you've got
females as the donors, it increases testosterone
level and sperm production in the males of lots
of different species. So all this makes
wonderful, wonderful, sort of sociobiological sense in
terms of how this should work. Elaborations on this, of course. What you also see is
not only puberty onset and being regulated. You also see in all
sorts of species where you can induce
ovulation by sensory stimuli. What you see is the
smell of a female will decrease the likelihood
of induced ovulation. Female-- the smell of
a male will increase the likelihood of ovulation. All sorts of species
that do not have automatic rhythms of
ovulation cycles of that way, but rather they are induced. And one classic example
of that are pigs. Pigs are inducible ovulators,
if you've always wondered whether that's the case or not. And you can go and
recreationally buy a variant of pig pheromone. This is known as Boar
Mate, and no doubt, that's not only patent
pended, but somewhere out in the Midwest,
there's all sorts of TV jingles about Boar Mate. And Boar Mate is an ovulation
inducer in female boars and involving a same
male-derived pheromone, which are found in truffles,
truffles which somehow have stumbled on the means to
induce female pigs to ovulate. And no doubt, that's explaining
some very interesting interspecies interactions,
so that being another realm. Inducible all
physiological changes-- in this case, one classic
demonstration of it. In this case,
probably pheromones of female causing an indirect
measure of testosterone levels in a male. This is a classic
paper, and you will note that I didn't
say females and males. Saying a female and a male. This was a classic paper in
nature some 30 years ago or so, which was written by the very
famous and well-known doctor Anonymous. The author's name was
not published there. And this was a researcher
who did research in an unspecified hemisphere
with an unspecified species, but involved long stretches of
being at a research facility completely on his own in
isolation from other humans, and all sorts of people in
the business for decades afterward have been speculating
on who the author is. And it's generally understood. And what this person noted
was every now and then, he would pick up and
go to the city that was a three-hour
seaplane flight away or some such thing,
where among other things, he had a highly significant
other with a great deal of physical intimacy
and all that stuff from kind of the right
side of the chart. And what he noticed
was what he perceived to be an extraordinary
difference in what he was subjectively interpreting
as testosterone-driven mood and level of energy and all of
that depending on where he was. Not quite being the
type of field ethologist that took blood from
himself, what he did instead was take an indirect assay
building on the well-known fact that testosterone
has something to do with the rate of beard growth. And what he wound up
doing was very soon, having a razor there
every day, shaving, and getting the little bits
of stubble, and weighing it. Weighing it is an indirect
assay of testosterone levels, and what was shown was
sit out there by himself with whatever ungulates
he was obsessing over, and this sort of rate
of beard growth-- go back to the rest of the
world, and it does this. And this square wave
going on like that, this as a very-- and OK, what
are all the confounds here? It's not clear if
it was pheromones. Maybe it was actually
being in proximity to the newspaper
in the town that he returned to now and then. Maybe there was a
confound of whatever aftershave he was using
that was doing something rather to his testes. Nonetheless,
generally interpreted as this being a really
interesting, indirect, and equal-- was one
example of induction of physiological
changes in human males by pheromones from females. So if you ever meet Dr.
Anonymous, who interestingly, has been publishing
papers for about 300 years or so every now and then,
congratulate that individual on the research. So pheromonal stuff--
now elaborations of it, which you should be able
to derive all on your own from some of our
principles by now, which is, what if for example,
you are a female donor and female recipient,
and the whole logic here being decrease the
likelihood of ovulation? Delay the onset of puberty. What if these are siblings,
if these are two sisters? And you were off and
running with that one. It will not work as effectively. Easy kin selection argument. So all sorts of
aspects of relatedness, you will not have your
testosterone levels driven up if you are a hamster, and you
were smelling your sister, all that sort of thing that
makes perfect sense by now. Now switching over-- one last
piece of business, though. In terms of the pheromonal
attractiveness stuff, a handful of studies showing
that among homosexual men, what you have is it's the smell of
men who are preferred to women, and it's when men have
higher testosterone levels that they are preferred. And what we've got there
is an exact same physiology in a somewhat going in the
opposite direction, flipping of things that sure argues for
some interesting biological underpinnings. One final thing-- women not only
prefer the smell of men when around the time that
they are ovulating. Their noses selectively
become more sensitive to such smells, and estrogen has
all sorts of receptors on olfactory neurons. So that makes sense. Leaping over to other
sensory systems-- gustatory stimuli--
this is not one of the more exciting outposts,
unless you are something like a giraffe, in which case
you take part in what is called flehmening, a good old Germanic
ethological term, which is you want all sorts of interesting
reproductive information on somebody else,
and you just don't have the time to sniff
the air for pheromones. So what you do is you go over
and lick the individual's private parts, and suddenly,
you know oh so much about their personal lives. In this case, gustatory
information being passed. We've already heard
about examples of auditory priming,
inducible ovulation in various moose-like species
in the wilds of Minnesota, where what the stags have
these roaring fixed action patterns, which will induce all
sorts of ovulatory responses in females around. So this is another domain. Remember also that
interesting factoid when this was
mentioned previously that in human
females, voices get a little bit higher around
the time of ovulation and in a way that is detectable. Something important in terms
of all this pheromonal stuff in humans, what
has been shown over and over and over again is these
are all subliminal processes as in the humans are not
consciously aware of wow, this one smells more like my
gonadally intact second cousin who was adopted away to Bolivia
for awhile when I was a kid. There is not the consciousness,
but nonetheless, you force people to
make these choices, and implicitly, you get
insight into these same sort of influences. But, of course, by the
time you get to humans, and you talk about sensory
releasers and all of that, you get, of course, the point
endlessly emphasized by Cosmo and God knows where else that
ultimately, the most erogenous organ in humans is the
brain, thought as a releaser, thought as a more powerful
humans are not a particularly olfactory species. We are not a particularly
great auditory one, et cetera, et cetera. An awful lot of these
sexual priming in humans coming by way of
thought bypassing this whole ethological world. More environmental factors,
acute environmental factors that can affect all of
this, and what you've got is a very reliable
way to drive down libido is to make an
organism terrified. Fear as suppressive of
reproductive behavior. What you also have is
extreme rage doing the same. Stress in general--
stress is interesting, because what you get is
a dichotomous outcome, chronic stress. So now we're not talking
about an acute stressor, but all the way
back, chronic stress is extremely suppressive
of reproductive physiology and behavior, which
you will be finding out when you read the relevant
chapter in the zebra's book. But what you see as short term,
there's a lot more variability, particularly among males. What you see is a
lot of variability as to whether short term stress
stimulates arousal or inhibits it. And people have
pointed out all sorts of horrific bits
of evidence showing in circumstances of
extreme arousal and stress, say, during warfare, where
that produces all sorts of violent sexual behavior. No shortage of horrible
historical precedents for those. So a difference between
chronic stress versus acute stress-- more
effects around here. One final interesting bit of
releasing stimulus, stimuli, whatever a bit of a
stimulus is, and one that transcends a
particular sensory system is something called
the Coolidge effect. And the Coolidge effect
probably accounts for like 49% of the
misery encapsulated in human literature and
movies and all of that. What is the Coolidge
effect in species after species after species? You take an individual,
who is sexually sated, which is to say that,
for example, you've got some male rodent who's been
mating with the female rodent there, and has gotten to the
point where he has had enough, enough on some
physiological level or some deeply emotional
what matters to me in my life rodential sort of level. But in any case,
the male is sated, has stopped having
sex with a female. And what the Coolidge
effect is about is he put in a different
female, and things start all over again. Variety as wildly stimulating
of sexual arousal, and the Coolidge effect sure
works in humans and accounts for all sorts of misery. Coolidge, by the way,
was not the scientist who first described
it, but Coolidge refers to Calvin Coolidge,
and as far as I know, this is the only
anecdote ever to occur about the guy, something
where he and his wife were being shown
some chicken farm, and there were
breeding roosters. And when they would get sick
of breeding with this pen, they would stick a new one in. And Mrs. Coolidge made
some sarcastic remark, and he made one back,
and before you knew it, it was the Great Depression. So I actually have no
memory of what they said, but in terms of
wittiness, you get what you can when you
have Calvin Coolidge, so. OK. We hurtle on. We hurtle on here, now beginning
to look at an entire missing category here in my rush. Now we have what's
going on with hormones, longer term hormonal stuff? Not the hormone levels
that you have influenced as a result of sexual behavior,
not the hormone levels just right around the time
of all this neurobiology happening, but now beginning
to talk about hormone levels like over the last 28
days or so in a female. And what one
immediately barrels into is this issue of how much
is sexual behavior in women a function of where
you are in your cycle? What's the reason
even to suspect that the entire world of other
species that will have females coming into estrus,
coming into heat, having elevated
estrogen levels only at very demarcated times of
the year, and what you see is in lots of species,
a large number of them, in fact-- what you see is you
only get reproductive behavior, you only get sexual behavior
in females around the time that they are ovulating. You only get active female
proceptive seeking of sex around those times. By the time you get
to non-human primates, it depends on the species
you're looking at. But in general, it's not quite
as tight of a relationship. So if you had some
rodent across a year, this was all the
points of ovulation. Your pattern of sexual
behavior of a female would look like this. Likelihood of mating
with a male by the time you get to non-human
primates in most species, it looks more like that. It's not quite as dramatic, and
thus, of course, the question becomes, where do
humans fit in on this? And a classic study, extremely
influential in the early '70s was the first to look at this,
which was females, humans, women reporting their
levels of sexual activity, as well as the
likelihood of orgasm per sexual bout, if
that's the right word, and where they
were in the cycle. So this is what you
wound up seeing, and this by any measure,
likelihood of having sex, whatever, the curve looked
something like this. And what they reported
was a big increase around the time of day 14 and
a secondary increase around day 28. Not as large of
one, and when you looked at the
likelihood of orgasm, it was basically doing
the same exact thing. Day 14-- that's just a somewhat
less restricted version of the exact same phenomenon. Never down to zero,
but nonetheless, this is another version of
this exact same phenomenon-- libido sexual proceptivity
increasing in women, in human females around
the time of ovulation. But no other species shows
this one going on here, so what's up with that? Any speculation why you
have the secondary increase around day 28? Come on. Somebody's got to--
yes, you're right. That's exactly what they found. That's exactly what they
found, and good for you feeling comfortable
speaking up in class all in unison like that. OK. What that tends to be
is that women are more relaxed about fear of
pregnancy around the time of their period, and, thus,
sexual behavior increases somewhat around that point. But the thing that everybody
most importantly came away with was just like every
other mammal out there that has regular cycling
or only seasonal ones, high estrogen is when you
get the most sexual behavior. Instead of high estrogen
is the only time you get sexual behavior. Instead, you simply get
the most around then. In the years since,
lots of people have done versions
on this study, and it is frequently difficult
to replicate this phenomenon in terms of a change in
levels of sexual activity in women around the
time of ovulation. What has remained very
clear in the literature though is that sexual arousal
increases around the time of ovulation in women. Very reliable effect. And what that is
interpreted as is behavior here may not be
telling you anywhere near as much as motivation,
arousal, proceptivity at that time, and that's
a more pure measure of what's going on
physiologically there or what's going
on in the brains. Fitting with that is a
very interesting literature suggesting that women act
a little bit differently in terms of proceptive
sexual signaling around the time of ovulation. Studies showing, for example,
that women as assessed by both women and men,
women on the average wear more provocative
clothing around the time that they are ovulating. Yes, people would go and study
things like this for a living. These were not big effects,
but the all-time bizarre study I've ever heard
of in this domain was actually published with
a straight face by this guy, and he's an evolutionary
psychologist, University of New Mexico, a guy
named Jeffrey Miller, who reported the following. And you know what he
was spending his time doing, which he
reported was that around the time of ovulation,
lap dancers get larger tips. OK. That has since been
replicated in E. coli and in various yeast
species, and you know, I'm not going to try to unpack
that one in any sort of way. But nonetheless,
this was reported and shows you just how wonderful
it could be to be a scientist. Can you imagine
that money was being spent on that-- your
research dollars-- instead of strafing people in Kandahar
province or something? So we have a peak there,
this general issue of what does hormonal
cyclicity, in a time scale of weeks to months. What does that do to sexual
behavior in various species? What does that do to sexual
arousal proceptivity? What are some of the
building blocks of that? Estrogen-- as
estrogen levels go up, estrogen increases
the expression of receptors for progesterone. So you can immediately
begin to piece that apart in at least two different
ways, first one being estrogen, thus increasing the
sensitivity in the brain. This is a brain effect. Sensitivity to
progesterone, which has something to do with the
rewarding aspects of sex. You can also translate that
into molecular biology. Estrogen, being a
steroid hormone, is going to bind to its receptor
and do the whole transcription factor, translocation
sort of thing, telling you that
upstream of the gene for the progesterone
receptor is a promoter that's responsive to estrogen
and estrogen receptors. You know how this
one works by now. More pieces of it--
estrogen when rising here, also increases the
synthesis of oxytocin. Back to all that
social bonding stuff, and what that suggests-- I don't
know if it has been studied, but that women will feel
more affiliative with someone they've had sex with if
around the time of ovulation than at other points. That is certainly
the case with a vole, but that is certainly
the case, because they don't mate the rest of the time,
and because male voles suddenly are expressive around there
in terms of their feelings. OK So more building
blocks of it. Estrogen is not only having
effects in the brain, but it's also having
effects throughout the body at those times in terms
of lowering the threshold of certain tactile receptors. What does that mean? That means around
the time that women are ovulating,
thanks to estrogen, they are more
sensitive to touch. And I'm sure this has been
studied in consenting hamsters, but my bet is that more
sensitive to tactile stimulation in some parts
of the body over others. What estrogen also is
doing, as we just heard, is working on the
olfactory system and lowering thresholds for
detecting the smell of males. So we've got all sorts
of ways within the brain and in the periphery to
bias towards more arousal at that time. Wonderful evolutionary biology. No problem at all. One additional piece
of the female story, which is the effects over the
course of this kind of time span-- weeks to months to
years or so-- the effects of those androgens,
those male sex hormones that females are releasing. And what you see
there is that plays a role in proceptivity,
increasing sexual arousal, sexual motivation. Meanwhile, on the other side
of the road, we've got males, and what does testosterone--
testosterone over this time span-- what
does it have to do with sexual behavior in males? Well, on first pass,
it sure looks like it has a lot to do with it. What sort of evidence? Initially, correlative evidence. Well, the time of year
in various species where males do their
mating is the time of year when testosterone
levels are elevated. Over the life span,
testosterone levels go up around puberty
and from about age 30 on, very gently cascade
down into alarming senescence, and what you see there is
a similar profile in terms of sexual behavior. That does not tell us much. These are correlations. Furthermore, correlative
studies in humans, a handful, showing more sexually
active men tend to have higher
testosterone levels, and for what it's worth,
a number of studies have documented a dramatic
drop in testosterone levels in men right around the time
that they become fathers. OK. So figure that one out. Also an increase in vasopressin
levels at that time. You know how to interpret
this one by now. So we've got testosterone
and higher levels of male sexual behavior
going hand in hand. Are we looking at
any causality here? First off, we already know
about one piece of causality, which was the other day, sexual
behavior in men, in males, increases testosterone levels. So that's one reason why
they may go hand in hand. In that scenario,
testosterone has nothing to do with increasing
the likelihood of the behavior. So does testosterone
actually have a causal role in
increasing the likelihood of male sexual behavior? And the answer is yes. And how do you show it? With the most simple classic
way of doing something in an endocrine study,
which is get rid of the guy's testosterone. And you castrate the
male, your rodent male, your non-human
primate male, and what you see is there is a big drop
in levels of sexual behavior. And this could range from male
lever pressing to get access to a female to
courtship displays to extent of pomading
of hair or something in the right neighborhoods,
and whatever the measure is, this is when normal testosterone
levels are on board. And this is after castration,
a very, very dramatic drop. Now to fulfill the second
ironclad requirement in endocrinology, the last
thing you need to do now is after the
subtraction experiment, to do a replacement one. Artificially give
back the normal levels to the castrated individual,
and levels of sexual behavior go back to there. Whoa. OK. That proves that we have a
causal relationship here. Not so fast. First thing to note, which
is 0% testosterone and sexual behavior goes way, way down. It doesn't go to zero. In every species
looked at, starting with the embarrassing sexual
behavior of everyone's pet dogs when they were six years old,
even after being neutered, what you see is there's a level
of residual sexual behavior-- rodents, dogs, primates,
including humans. This is a critical point. How much residual
sexual behavior is there after castration? The more sexual experience
before castration, the more there is going
to be retained afterward. In other words, on a certain
like totally artificial level, this amount of
sexual behavior is being driven by testosterone. This amount, which
persists here, is being driven by
social experience. It's got nothing to
do with the hormones. Yes, this is ridiculous
dichotomizing into this, but the fact
that it doesn't go to zero, and the fact that the
more sexual experience pre-castration, the more
residual behavior, this is a vote for just
how much of a role social experience, social
conditioning plays. Next thing that takes
away from the yes, it's all caused
by testosterone-- now you do an
elaboration on the study. You castrate a male,
and now instead of replacing with
100% of normal levels, you give 10% of
normal levels, or you give 200% of normal levels. And what do you wind up seeing? If testosterone plays a
strictly causative role, even in this range, you are
going to get something-- this is going to
be lower than 100%, and this is going to be higher. That's not what you see. Instead, it is
something like that. You get roughly the
same reinstatement of sexual behavior when you
return testosterone levels over anything
roughly approximating the normal physiological range. What does that tell you? The brain circuits we learned
about the other day involved in sexual motivation-- it
requires testosterone around to work fully, not
entirely, but to work fully. But those brain
regions are not really all that concerned with the
exact level of testosterone. Rough approximation of normal,
rough approximation of normal has the exact same effect. If you were seeing
a tight relationship in a male between the
amount of sexual behavior and testosterone
levels, it's not because every little smidgen
bit of more testosterone is going to drive
more sexual behavior. It's because every little
additional smidgen of behavior is going to drive higher
testosterone levels. So we've got this really
important observation. Yes, testosterone is needed
in species after species, including humans, for the
normal range of sexual behavior. Just as importantly, castration
never drops it down to zero. The more social experience,
that whole song and dance, and very importantly
as well, the system is not sensitive to
little differences in testosterone levels. Stating that a different
way, if some guy has one and 1/2 percent
more testosterone on board than the guy
sitting next to him or than he had last week,
is that going to mean he is going to be more sexually
motivated, more aroused? No, not at all. Within the normal range, the
system doesn't distinguish it. The relevant brain regions
are sensitive to testosterone and require it, but do not care
a whole lot about the levels. One exception, which is
if you instead of, say, 200%, push testosterone
levels like 1000%, tenfold higher than normal,
this is supraphysiological, which means it's out of
the normal range, which means no bodies normally
generate those sorts of levels. Put it up in that range,
and you will get an increase in sexual behavior
and sexual arousal. When do you see this? The idiots who go and
abuse anabolic steroids for their weight lifting or
whatever, people doing that are not pushing up their
testosterone levels into the higher range of what
human bodies can generate. They are pushing it way
above the normal range. In that range, you
do see an increase in sexual proceptivity. In a week or so, what we will
see is the exact same story. It will be the exact
same chart here when asking the question,
what does testosterone have to do with aggression? And what you'll see is the
exact same conclusions. What are we beginning
to see here? That testosterone is not playing
a strictly causative role. It is playing one
of the words that should be becoming repetitive
here and clearly really important. Testosterone is playing
a modulatory role. What testosterone
does is sensitize you towards stimuli that are
evocative of sexual arousal. It lowers the
threshold, and that could be shown in
all sorts of studies, but where it's most clear
cut is in this case. Does testosterone cause
this sexual behavior? No, but when it is on
board, it facilitates it. It modulates it. Theme again and again and again. And that, obviously, has tons to
do with individual differences. One last hormone to mention in
this realm of hormone levels over the last couple of
weeks, months, seasons, or so-- the hormone melatonin. And I think that's the
only time melatonin is going to be mentioned in class. Melatonin has something to do
with telling the body what time of year it is. It is responsive to the amount
of light you are exposed to. What is melatonin about? It is one of the driving
forces on seasonal mating. Those species where you
suddenly get on one afternoon each year, all the wildebeests
ovulate the same afternoon kind of thing-- it
is almost certainly a whole pathway in the brain
sensitive to the amount of light and the amount of
light per day over recent weeks, which by way of
melatonin, triggers the onset of the mating season. Do humans have a
seasonal mating pattern? There's a smidgen
of evidence for it. If we've got it, it is
a very, very weak echo of what you see in
some other species. Now we shift over to getting
really way back then. Instead of over
your last 28 days or over the last three
seasons, now beginning to look at perinatal factors. Perinatal-- before birth. Prenatal-- after birth. Postnatal-- very
early development. First off, focusing
on early environment, environmental factors
having something to do with adult
sexual behavior. What we can translate
that into is ways in which early environment
affects every single one of these subsequent ones. What does early
environment childhood have to do with shaping
of sexual behavior? A theme that's also going
to come out in every topic we're going to hear of
after this, buzz words that should be beginning to be
keeping you awake at night-- modulatory, contingent,
if then, all that stuff. Here is another one. Here's another concept
that comes through. The evidence shows that there
is very little about early life experience, which
influences the quality, the way in which an organism
goes about having sex. What's another
way of stating it? This is a pretty set in stone
bunch of fixed action patterns. Early experience is not about
learning how to be sexual. Early experience
is about learning the appropriate social
contexts for being so. And that is shown in
species after species. That is what
experience is about. Not how to do it,
but when to do it and who you should
not in your right mind try to do something proceptive
to and things of that sort. This is what early
experience is about. And what we're going
to see in a week is the exact same
boring paragraph. Early experience does not teach
organisms how to be aggressive. It teaches organisms
the appropriate context for being aggressive. So what's the sort of evidence
for these early effects? One example, the
whole literature that emerged that is covered
somewhat in the zebra book in another domain, but this
whole literature that emerged in the 1950s, work looking
at captive primates, what are the consequences
of growing up in a certain degree
of social isolation? What happens to behavior--
and eventually, people studying behavior
and physiology-- what happens to behavior in adulthood
if you are a young rhesus monkey, who grows up only
with peers and no mother, or grows up only with
a mother and no peers, or grows up with
Mother being present only intermittently, or at
the most extremes, growing up with neither mother nor
peers or any other member of your species around? You will see in the
book a whole discussion of the ethics of these
studies, but what does your early
social environment have to do with things
like sexual behavior? And what you see
coming out the end is when you looked at
these adult primates, since replicated
over and over, they go about the sexual behavior
the plain old way that everybody else does, but they do
it in totally socially inappropriate context. And thus, you have
these males who were raised in some degree
of isolation early on, growing up and carrying
out perfectly normal sexual fixed action patterns
on the towel in the room, on the bowl of food, on the
who knows what wrong context. You have trying to do things
with animals you should not go anywhere near in
terms of social dominance and such in appropriate context. Early experience shaping
not how but when, what the if-then clauses are. More issues of early experience
shaping adult sexual behavior, arousal, proceptivity,
et cetera-- we already heard one example
of this with humans. That's the whole
kibbutz literature. That was that whole
business that if you spend lots of intimate time
with somebody before age six, what you will do is in some
subliminal imprinting way, decide forever after
this individual does not feel like a potential mate. This individual
feels like a sibling. That was the example in the
recognizing relative lecture of showing that
hooray, we are such a cognitively
sophisticated species. We can figure out who's
somebody's fourth cousin three steps removed by
thinking, and that's how we make our mating
decisions, showing instead in those studies, there is
this non-conscious level. One of the rules that humans
have is lots of exposure intimately to somebody
early on in life, and you are not going
to be very likely to get that proceptive behavior
stuff going on later, part of turning them
into a pseudo kin because of that early exposure. One additional domain
I will touch on here in terms of early
experience, which is, what does early
experience have to do with sexual orientation? And depending on which decade
you are asking this question, the answer would
range from everything to virtually nothing. Going back to the virtually
everything time, which was dominating sort of the first
half of the 20th century, how people thought about the
subject, what you had were two broad models for what
sort of early environments increase the likelihood of
boys becoming gay as adults. And these were the two models. The first one was the absence
of a father figure model, and this was one
straight out of monkeys learning who they should
try to pelvic thrust with or some such thing. This was the argument that
what do father figures provide? Training for appropriate context
for proceptive sexual behavior, growing up absent a
father, father figure, increasing the
likelihood of being gay. The other model was having
this totally pain in the neck neurotic screwed up
mother, who, as basically said between the lines, makes
you crazy when you grow up, and thus you have circa 1950,
psychiatrically certifiable disorder of having a
different sexual orientation. Obviously, where I'm
going to head right now is there has not been a
slightest shred of evidence over the years either for
the missing father figure model of sexual orientation or
the neurotic mothering style model. Complete nonsense. Nonetheless, dominating thinking
about what was going on there. OK. So what we are now
ready to shift to is what's going on with hormones
around this time period. Let's take our five-minute
break, and then we'll resume. Looking at what perinatal
hormone levels have to do with adult
sexual behavior, and you already know the answer. You know it in
your hearts by now, which is, well, it depends on
what species you're looking at. And what we will see is a
very similar thing to the rule there, which is in
lots of species, rodent species, prenatal or
perinatal hormonal environment has everything to do with
adult sexual behavior. And by the time
we get to humans, what we'll see is maybe kind of
sort of more research needed. What we begin with
here, implicit in that, is a dichotomy that runs
through all of endocrinology when thinking about behavior. The effects of hormones
back when you were little, jargon in the field, an
organizational effect of the hormone. And what that is
about is explicitly is what are hormones
doing at a time in terms of organizing what kind of
brain you're developing there. Effects of hormones,
instead, in this range or so, what you are talking about is
an activational hormonal effect. So this is a very sort
of consistent dichotomy that people in the business
use, early, early hormonal environments having
organizational effects on the nervous system,
hormones forever after having
activational effects. So what you see is
in rodent species that perinatal
hormone exposure has massive organizational
effects that dramatically influence sexual behavior. What you also see is it's not
so dramatic and clear cut. A whole literature
initially suggesting that, for example, male
rodents, if they are not exposed to testosterone,
perinatally, will have a different male
rodent sexual orientation later on, a dichotomous outcome. What a huge literature
now shows is something that is evident to
every sort of human sexologist for centuries, which is it's
not a dichotomous function. It is on a continuum in
terms of sexual orientation, and 300 different species
have been documented by now to have both heterosexual
and homosexual behavior at different times in
naturalistic settings. So perinatal hormones
having organizing effects on adult sexual
orientation-- what you see is these are not all or
none properties at all. What else? OK. What you see specifically
in non-human primates is perinatal period. Expose a female monkey fetus
to high testosterone levels, and what you will do is
masculinize the brain. Masculinize the brain, having,
thus, an organizational effect. What does masculinization
then manifest itself as in adulthood? If nothing else is different,
it has no effects at all. On the other hand, if you
inject a female monkey who is masculinized perinatally, if
you inject her with androgens, with testosterone, you get a
wild burst of male fixed action patterns. In other words, you've
got an if-then clause. If and only if there was
prenatal masculinization, then testosterone will have
an acute activational effect on sexual behavior. Translating this. OK. So in the absence in a
normal female monkey, in the absence of prenatal
androgens or adult androgen levels, this is the amount
of male fixed action pattern sexual behavior. Now prenatal androgenization--
normal low action levels in adulthood. Same low levels. Now no prenatal androgenization,
and exposure to androgens in adulthood-- same low levels. Prenatal exposure and
acute activational effects, and suddenly, you get high rates
of male typical fixed action patterns. So what we've got here is
a contingent organizational effect. Yet again, one of our
if-then clauses, this one not being an if this
physiology is going on only in this social environment, then
if this early life endocrine environment occurs coupled with
this acute adult one, then. Yeah, question. [INAUDIBLE]? That is a great question,
and as you're about to see, the answer is so
insanely complicated, you are going to regret having
asked that question for days. But you are going to
find out about it anyway. Apropos of that, I just
forgot a great question during the break, which
is, OK, when you've got those weightlifter
folks, they're abusing their steroids,
their anabolic steroids, their testosterone-derived
drugs, when you push things up into the
supraphysiological range, higher than the body
normally ever comes up with, do you see a phenomenon
from last Wednesday? Does the body down
regulate the number of testosterone receptors? And you see exactly the case,
but you could never down regulate them low
enough to compensate for the huge screaming
testosterone signal. It is a partially successful
compensatory response. What have you got
in terms of humans, in terms of perinatal
androgenization of females? And people used to know
exactly the answer to it. First off, when do you get
human females as fetuses and as predominately in
humans prenatal, rather than postnatal effects? It depends on how fast,
how much of development occurs before birth,
but in humans, when are circumstances
where female fetuses will get heavily androgenized? Historically, two circumstances. One is in the case
of a disease where there is something wrong
with the adrenal glands, and they pump out
tons of testosterone. You remember, if I
actually did say this, and if I didn't, I hope
you're not remembering it hallucinatorily,
but you'll remember that the adrenal glands make a
certain amount of testosterone, and in females, it
pumps out maybe 5% the levels that males do. When you have this disease of
an overactive adrenal system, you pump out way too high
of levels of testosterone, a disease called congenital
adrenal hyperplasia. Hyperplasia, the
number of cells-- OK, come up with a limerick
about that one. I dare you. Is it possible to
come up with a haiku? How many syllables are there in
congenital adrenal hyperplasia? Well, it depends if we're
talking about rodents or not. So congenital
adrenal hyperplasia, a genetic and inborn error
of metabolism in the adrenal glands, and you pump out
huge amounts of androgen. So suddenly, there is a world
of the occasional girl, who was born suffering from
this disorder or the mother suffering from it during
pregnancy, who has been prenatally androgenized. The other population,
thanks to a drug that was very popular in the
1950s, a drug that decreased the likelihood of miscarriage
that was very heavily used at points around then, a drug
called diethylstilbestrol, DES. And in a subset of
women, their biochemistry was such that a lot of the DES
was converted to androgens. So you had kids, who were
prenatally androgenized, girls, either because of this
congenital adrenal hyperplasia or because of DES exposure. So then the question
immediately becomes, OK, so what are they like afterward? And this prompted the
great, large, massive set of studies on the CAH, the
congenital adrenal hyperplasia, on the CAH girls
as they grow up, and you knew exactly what
the expectation was straight out of primates here,
non-human primates, which was this was going to
have masculinizing effects on their behavior. And what was shown
was in adulthood, there were all sorts
of differences. No, not just in adulthood. Starting around
adolescence, there were all sorts of differences
in the behaviors of these girls, and as we'll see next week,
a whole cluster of them were thought to fall into the
realm of aggressive behavior. But what we're seeing
here was eventually, a higher likelihood
of becoming a lesbian in terms of sexual orientation. Whoa. What we've just shown
is prenatal androgens, and you produce a
lesbian later on. That's just-- there's a little
problem with these studies, a slight confound,
and one that's going to be very
pertinent next week as well when talking about
the aggression stuff. The confound being if you
were prenatally androgenized, you would get born with
kind of weirdo genitals, and you would have sort
of intersexual genitals in all sorts of ways. And all of these
girls typically had to have gone through
a dozen rounds of reconstructive
plastic surgery over the first
decade of your life. These were not girls where the
only thing different about them was what sort of hormones
their brains were marinating in back when they were fetuses. These are girls who grow up with
this really interesting part of the body that
all sorts of people seem kind of creeped out about,
but doctors are endlessly examining, and all sorts
of painful surgeries. And this literature
was completely confounded by the
fact that there was all this masculinization
of genitalia and a whole world of surgeries, often confusion
about gender assignment early on in life. Things were not merely a
change in the hormone levels. So it remains
relatively unclear. There is by now, at this
point, weak evidence of prenatal
androgenization increasing the likelihood of a woman
being gay as an adult. I'm seeing here in my notes
I have the words Indonesia, tomboy, and Hobson Jobson. And I haven't a clue
what that's about. So we will just skip over that. OK. What we begin to see
here is another feature of early experience. What does-- where were we--
prenatal endocrine environment have to do with
sexual identification? Which is different than who
you are sexually attracted, but rather what sex you
feel yourself to be. And what we heard the other day
with the transsexualism example is you could have gender being
dictated by your chromosomes and which organ, which
types of gonads you have and hormones and all of
that, but that is not enough to determine that there
are clearly other things that can happen that could produce
a very, very different gender identity. What also was seen from that
literature of individuals who were born intersexual where
they have sexually ambiguous, gender ambiguous genitalia
is it is far from clear which decision to
make, whether that was made circa
1950s by the surgeon with no consultation
with the parents, or, fortunately, these days,
a very different scenario in terms of how successful
the assignment is by the individuals
in the outside world. What's going on in terms
of sexual identity inside? Now what this begins to bring
up is the most miserable, irritating, confusing
thing about the effects of steroid hormones
in the brain, which is where your question came from. And this is where you're all
going to start to regret this, but it actually is necessary
in terms of an important point. So you've got testosterone,
and what does testosterone do? We know already it binds
to testosterone receptors, testosterone receptor, and
does its steroid hormone transcription factor deal. Throughout the 1970s, there
was an astonishing amount of confusing irritative research
done showing the two following things. In some parts of the
body, testosterone has its effect as testosterone. It binds to the
testosterone receptor. In some parts of the body,
there is biochemical conversion of testosterone to something
called dihydrotestosterone. OK. It's not testosterone. It's a little bit
different chemically. It binds to the same
testosterone receptors. It works a little
bit differently. OK, we can live with that. The thing that had people
jumping off buildings was the discovery at
the time that some of testosterone's actions are
due to it being biochemically converted to estrogen,
which then binds to estrogen receptors and
causes male typical behaviors. OK. It's at this point that about
half the people in the field quit and went to
business school, because this was so confusing
and impossible and all of that. This consumed years
of labor of people trying to sort this one out. It goes as follows. Once testosterone
enters a target cell, if this is the scenario
that's going to happen, it's inside the cell. The testosterone is turned
to estrogen. In other words, this weirdo phenomenon has
no effect on circulating testosterone levels. It's only in target cells
that have the enzyme that could do that conversion. OK. So it's an intracellular
phenomenon. If this is leaving you
totally in the dust, don't worry about it, except for
a small point coming in awhile. But if you want to devote
the rest of your life to figuring this
out in more detail, there is something
wrong with you. But what you've
got here is normal circulating levels,
but different effects throughout the body. In general, what is found is
the effects of testosterone in the brain involve this
turning into estrogen, as symbolized meaninglessly
by that asterisk. Throughout the genitals
or throughout the body, and secondary sexual
areas of skin and such, testosterone exerts its
effects by being turned into dihydrotestosterone. And whatever parts are
left over at that point, testosterone just does
its regular old thing. So this is incredibly
confusing how this can be. Immediately, or not so
immediately, two things should come to mind. OK, so prenatal
testosterone levels are going about
their normal prenatal organizational masculinization
effects, and part of it is on how the brain organizes. So what we just saw was prenatal
neurobiological masculinization requires testosterone
to be working like estrogen in the brain. Why don't all the female
fetuses then get androgenized? Since they're not generating
estrogen right on site there within the cell, but
they're getting estrogen through some other route
as their fetal ovaries start to work. Why isn't mom and her
estrogen androgenizing every single fetus out there? How is it possible
to ever get a female? And the answer to
that is there is a protein, which occurs
during pregnancy, that occurs in the circulation. And what it does is
it binds estrogen, and it takes it out of action. It leads to estrogen
being degraded. In other words, estrogen in
the bloodstream of a fetus never has an effect on
any cells in the body. Estrogen, whether derived from
the female fetus beginning to get her ovaries going there,
or from mom's circulation, the estrogen has no effect. And in other words,
the only fetuses that ever have estrogen
inside their neurons are fetuses that are male,
where the estrogen came from testosterone. So you have to
have this protein, and it's something
called alpha fetoprotein. It only occurs in fetal life. This winds up
being the solution. What is implicit
in that, you do not get the organizational
feminizing effects of hormones prenatally because of
estrogen, because you've just guaranteed that doesn't happen. You're getting androgenizing
effects that way. You don't get prenatal
feminizing effects from estrogen. Where does the
brain feminization come from? The irritating
answer back when was this was always-- sort
of the same phrase was always used that the female
brain is a default brain. You have to actively in a
muscular excited chopping down the trees and clearing
the prairie sort of way, you have to actively
do something hormonal to masculinize a brain. And in the absence of that,
you just kind of wind up with one of them female brains. What's clear now is this default
model was not really the case. It's other hormones that
are doing that there. OK. So this totally confusing,
irritating thing that everybody had to assimilate
at the time of testosterone having different effects,
having been converted to different messengers in
different parts of the body, and that having to produce this
whole complex Rube Goldberg sort of solution as to
how to ever get a female. Now one additional
interesting implication-- back to, you remember the other
week, remember-- actually, did I talk about it, or
was it two years ago? Jeez. OK. I think I mentioned
testicular feminized males. Yes. Good. OK. Thank you for the grounding. You remember when
those folks were about. This was someone who was
phenotypically a girl and would not hit
puberty, would not start menstruating until
every other kid in her grade had, and it still
hasn't happened, still hasn't happened. And you take her to the
doctor, and what is discovered is that she is not female. She is a testicular
feminized male, and we went through
exactly what the building blocks were of that. The individual is
chromosomally male, has testes, undescended
testes, is producing tons and tons of testosterone. What was the problem there? We knew already it
was the mutation in the testosterone receptor. So if testosterone
is not able to send a signal through the
testosterone receptor, you don't get a male
phenotype, and you get an individual whose
sexual identity is female, because these are
people who are girls and grow up to
become women, women who simply can't reproduce. But otherwise, the sexual
identification is female. This should be
really puzzling now, because what we've
just seen is if you have this mutation in the
testosterone receptor, you're not going to get
any signaling mediated by testosterone. You're not going to get
any signaling mediated by dihydrotestosterone. But you're going to
get perfectly normal masculinization of
the brain by way of estrogen. In
other words, people who were testicular
feminized males, who in terms of their
sex identification, have been female from
day one and will be for their entire lives,
nonetheless, prenatally they had masculinization
organizational effects on the brain. What does that tell you? All of this great hormone
stuff, in some cases, doesn't hold a candle to social
sex identity assignment, which is when you have
somebody growing up with a certain gender's
genitals, and all of you treat that individual as a girl. It turns out virtually
100% of the time, it doesn't matter that you
still had this pathway working prenatally. All the social cueing produces
a female sexual identity. So we've just gotten a big,
big vote here for this. It's doing all sorts of
exciting endocrine stuff there, which nonetheless,
may not hold a candle to some social environmental
factors at this end. OK. What else do we have here? Something I don't
want to talk about. OK. So hurtling on, now we are ready
to move back another box here, which is genetics. What does the genetic makeup
up of an individual, not of a population or
species, what do genes have to do with sexual behavior? And the answer is lots of
things, starting with the fact that genes determine which
gonads you make as a fetus. And thus, that determines
which sex hormones you were secreting,
and thus, that determines what sort of
genitals you wind up with and secondary sexual stuff, and
off you go running with that. And we've seen that nonetheless,
that can be blunted by, depending on the environment,
the testicular feminized male pathway here showing that. So genes play a role in terms
of just sheer sex determination. What is known about genes
and sexual orientation? This has been studied
a lot, because this is one of those
irresistible subjects that, ooh, people just
can't get enough of. What's up with that? What does the literature show? A certain degree of heritability
of sexual orientation, and you should be able to leap up right
now and say exactly what that means and doesn't mean. Here's the sort of evidence. Twin studies, twin
studies-- when you look at monozygotic
twins, identical twins, there's approximately
50% concordance of sexual orientation. Translated into the terms
that people are usually focusing on in those
studies, which is to say, if somebody is gay,
their identical twins has a 50% chance of being gay. Dizygotic twins, non-identical
twins-- what is the number? Instead it's 22% covariance. What's the number
with other siblings? 9% covariance. So what do we see here? We see a suggestion
that the more genes you have in common with somebody,
but also the more prenatal environment you had with
your non-identical twin, all of that stuff, the greater
the likelihood of sharing a trait of sexual orientation. And you can be off and running
right now about the limitations of that interpretation,
because obviously, this suggests genetic
effects, and it also suggests the whole world of
identical twins being treated differently than
non-identical ones. One additional piece
in that story, and this was another one of those front
page stories in Time, Newsweek, et cetera, and this
came a couple of years after Simon Levey's finding of
that sexually dimorphic nucleus in the brain, that
whole deal there. And this was the reporting
of the first genetic markers for sexual orientation. And this was reported
by a geneticist at National Institute
of Health, a guy named Dean Hamer, who was a
very well-respected geneticist. And what he reported was that
he was finding genetic markers for sexual orientation. In other words, certain
gene locations that were more likely to be shared
between gay siblings, where both were gay, than
between partially gay siblings or non-gay siblings
or however that one runs. You know that one by now. Beginning to find genetic
markers going with this. This was really interesting,
and no surprise-- what the newspapers were
screaming about within days was scientists
announced today they have discovered the gay gene. Great. Maybe we shouldn't let people
learn any science out there. So scientists have
discovered the gay gene. It goes to all the newspapers
and Reader's Digest, and if I recall at the
time, Ronald Reagan as well, but he was completely
demented at that point, so I won't hold it against him. But the people at Newsweek
should have known better. So we have cover stories
about the gay gene. Obviously, you can rip
this to shreds right now. Number one, this was not a gene. This was a genetic marker. You remember the other
week, the difference there. Number two, there was
no consistency in this. What do I mean by this? This pair of
identical twins would tend to share a certain genetic
marker, which was predictive of sexual orientation. And the next pair over, it
wasn't the same area of genes that showed that covariance. It would be a completely
different area that they had in common. In another pair, a
completely different area, you got this genetic covariance
in various twin pairs, but it wasn't the same gene
marker in all those cases. All of them were
different, which makes zero sense in
terms of the genetics. The biggest problem with it
is that since then, all sorts of people have tried to
replicate the finding, and it has never
been replicated. Nonetheless, Hamer became
quite famous for this. He is gay, and he used this
sort of politically some of the same ways that Simon
Levey did with his study, which is, don't tell me about choice. Don't tell me about my
neurotic mother anymore. We are looking at a very hard
wired biological trait-- what sexual orientation you have. Levey's finding I have
found quite convincing in terms of replications. Hamer's-- nobody else has
replicated any actual genetics that he reported. Makes no sense at all. So great limitations in
what you could make of this. OK. This allows us to make our
great final leap to the left with this thing,
this logic that's going to run through
everything we talk about, which is the second you're
talking about genes, you are implicitly talking
about the evolutionary history that brought about the
existence of those genes. And that you're also talking
about the proteins made by those genes and early
environment changing the epigenetic state of
transcribing those genes. Yes, yes, that whole
song and dance now. So now we have to transition to,
what does evolutionary biology tell us about sexual behavior? So the first thing that it tells
us is absolutely obvious, which is organisms have sex for
the good of the species. So that one's out of the way. So now we go to what is
much more logically in terms of contemporary, evolutionary
thinking-- contemporary starting circa 1965 or
so-- the whole notion of maximizing the number of
copies of your own genes, all of that translated into
sort of the economic terms of [INAUDIBLE] copies of genes. What that basically
states is sexual behavior is about reproduction. And people who would
study phenomena like these in various
rodent species or wildebeest ovulating the
same afternoon, all of that, would say, yes, indeed, you
only have sexual behavior when it's around the time when
females are ovulating and yes. Reproductive behavior
is about reproduction. It's about passing
on copies of genes. What soon began to fall apart
was not only making sense of us with our having non-reproductive
sex all sorts of times, was the discovery that we're
not the only species that does that. And far and away
the flagship species as a sort of emblem of
that are bonobo chimps, who are, according to almost
all primatologists out there, the coolest primate
species there is. OK. Bonobo chimps-- they
were historically known as pygmy chimps, which is
to say that when people first discovered them in
terms of scientists, they were viewed as,
well, these are chimps, but they're just kind of
weirdo atrophied chimps, which I don't quite know
how you come up with a pygmy atrophied
chimp, but that was the view. And not very interesting--
what eventually became clear is they are a separate
species of chimp, and bonobo chimps
are utterly different from your standard issue
Jane Goodall chimps. Again, Jane Goodall chimps,
we have a tournament species with extreme high levels
of male aggression. As we will hear
about next week, you have chimps who are
building weapons. You have chimps
that form something resembling organized
warfare, and meanwhile, over, as it turned out, on
the other side of the Congo, which is where the
main division occurs, you only find bonobos in
one area of the Congo basin, and they clearly have been
reproductively isolated from all the rest of
the chimps heading there east all the way to the Indian
Ocean by way of the Congo. There, go on the other
side of the river. You've got the bonobos, and
bonobos are totally different. Bonobos, unlike chimps, have
virtually no sexual dimorphism, so you're off and
running with that one. We know exactly what that means. Bonobo chimps have female
dominance rather than male. All bonobo chimps play the
guitar and sing soulfully. What else? And we have astonishing
amounts of sex. Wait a second. We just went off the rails here. A species with low degrees
of aggression, because they have virtually no aggression
whatsoever, species with low degree of aggression
and with no sexual dimorphism in body size-- what
we're looking at is a pair bonding species,
a monogamous species. Bonobos are not a
monogamous species. Bonobos make-- I don't know
who-- look like a pair bonding species by comparison. Bonobos are the most sexually
promiscuous species on Earth. Bonobos have astonishing
amounts of sex with every other type of
bonobo they could run into. They have sex in
order to reproduce. They have sex in order
to decrease tensions. They have sex in
order to celebrate having decreased tensions. They have sex, because it's an
even numbered day of the month, because this is odd. Every variety, and
the vast majority of it being non-reproductive,
non-reproductive because it's not at a time
when anybody's ovulating, or because it's with
someone of the same sex, or it involves sexual behavior,
which traditionally does not result in eggs getting
fertilized and all sorts of variants that
people only dream about from buying books
and trying to get lessons and this sort of thing. And you have, perhaps,
having something to do with that astonishingly
limber spinal columns, but what you've got is a
totally different picture. Wait a second. They are very low
aggression, and they have no sexual dimorphism,
but they're as far from pair bonding
as you can get. And instead, you have a highly
promiscuous social system, female-dominated,
and they're all just so cool and wonderful
you can't believe it. And every time people go
to primatology meetings, if you study some dumb old
stupid species like a baboon, you spend the whole
time basically feeling like you're some sort
of immature jerk, because you're not
hanging out with bonobos. They are the kings of
primatologists these days, the people who study bonobos. As the soundbite goes,
chimpanzees are from Mars. Bonobos are from Venus. OK. So that's what the t-shirts
say from the bonobo people at the conferences there. Totally different system. So what we already see is
violating our simple rules of what predicts a
tournament species and what predicts
a pair bonding one. What's most striking
here is [INAUDIBLE] reproductive behavior
is reproduction for passing on
copies of the genes, not for the good of the species. But we know individual
selection could [INAUDIBLE]. And here's these guys having
sex with 14 other bonobos while they're all upside
down or who knows what, and it's not just for passing
on numbers of copies of genes. Huge, huge exception there. And huge exception in
lots of other species. And the ecologist
Joan Roughgarden here in the biology
department has made an argument there is far
more non-reproductive sex that goes on in lots of
different species, weakening the classic
Darwinian concept from three, four weeks ago of
sexual selection being a very important
driving force. What sex is very heavily
about is one gender choosing who are going to mate
with the other one, and it's all driven by
that of seeing instead if the world of
bonobos, there's not a whole lot of evolutionary
drive being built around sex equals reproduction. So bonobos are
really interesting. What's the sex there about? One of the common themes
that comes through is it's about promoting
group cohesion, and one of the things that
people emphasize or focus on with bonobos is you look at all
sorts of other primate species, and what do they do when
they're upset about something? They groom each other. What do they do
when they're happy? They groom. What do they do--
social grooming, as termed the social glue, the
social lubricant of a society. You get a troop of
baboons that have just gotten a bad scare from
a lion, and as soon as the coast is clear,
everybody comes down and spends the next 30
minutes grooming each other. And sexual behavior
in bonobos appears to be serving a
very similar role-- all about social cohesion
as well as decreasing individual tensions,
reconciliation, things of that sort. Now this flies on the face of a
dominant theory that was around in the last century,
the first part of it, and this was due to one
of the grand poobahs in this field, a guy, this
Brit named Solly Zuckerman. Solly Zuckerman, who eventually
became Sir Solly Zuckerman, which probably didn't
help him in society at all still despite that,
but old Zuckerman there was, for his time, the
embarrassed Wynne Edwards. He was the Lamarck
of the earliest part of the 20th century. The people who will
only be remembered for coming up with
Lamarckianism, old Lamarck or coming up with something
as idiotic as group selection. What Zuckerman came
up with was the notion that sexual behavior is purely
for promoting group cohesion and for decreasing violence. And all you need to do is go
to half the movies out there or study half the
species on Earth, and what you will see is
sexual behavior or inability of or unrequited or
whatever vanquished is the cause of the majority
of aggression in organisms out there in various
mammals, and that argues very strongly against it. So what you see in most species
that have been studied-- it's a strong argument
against the Zuckerman stance. Nonetheless, you see in
some species like bonobos and Roughgarden's
argument, lots more species than people traditionally
would think, where instead you see sexual
behavior often serving a non-reproductive group
cohesion sort of role. What else does evolution have to
tell us about sexual behavior? One critical issue and
one that was touched on the first couple of
lectures is, what does it cost you to reproduce? And there we get the
hugely important asymmetry, which is sperm don't cost
a whole lot, whereas eggs and pregnancy and postnatal
care and all of that is hugely expensive. What is that the
driving force on according to all the
sociobiological thinking? The fact that in species
after species after species, females are more
selective about who they will mate with than
males, and it's usually the case the males are not
selective in the slightest. And what you've
got instead is just a couple of sperm that accost
you, and that's not a big deal. Increased female selectivity,
higher levels of it than males, argument being that it is
all about the differential costs of pregnancy. What we also saw was
not of pregnancy, but of reproduction
and raising of kids. What we saw was the
interesting realm where you got the
exception to that, which were the pair bonding species. The marmosets, for example,
and what we saw back when was the male does as
much child care as the female does, and the
females always twin. So around the time
that the kids are born, the female has put in far
more of the investment. She's gone through
the pregnancy in terms of caloric expenditure. The males do, if anything,
more of the child rearing in terms of carrying the
kid around when foraging, all sorts of costly stuff
like that, and eventually, what you see is the
curves don't do that. But at some point,
the cumulative amount of calories that the
male has expended is greater than the female. That's when you see
that cuckoldry business. That's where females
will potentially pick up and abandon, and because
the male has made the greater investment at that point, that
is seen very frequently in bird species with pair bonding. So we've got here an
exception to the argument that the cost of reproduction
and child raising is always greater for females
and, thus, will always produce greater female
pickiness for mates than you find in males. Nonetheless, you see
that an awful lot. What else do you see? A whole world not only
of female pickiness, but a whole world
of male attempts to control female
reproductive behavior. And this found in species
after species after species an obvious interpretation
there in terms of male-male
competition decreasing the ability of females to
mate with someone else. And that ranges
from primates who are in consortships, where
the male will do what is often termed mate guarding,
which is he tries to keep the female from
going near any other guy to all sorts of
other stuff as well. And you certainly see
this in the human realm. What are two cultural inventions
humans have come up with to decrease the likelihood--
by men-- to decrease the likelihood of women
being sexually active outside that relationship? The first one is
clitoridectomies, and something else that serves
a very similar function, which is inventions of things
like chastity belts. What's up with that? What you find are
cultural inventions like those in groups that tend
to have occupations where males disappear for long periods. For example, nomadic
pastoralists, where depending on
the time of year, you pick up with your camels
or your cows or whatever, and you, the guy, are going
to spend the next three weeks at the grazing area
that's a good five miles west of there. And what this is about--
the argument culturally for the clitoridectomies is
it decreases female pleasure, decreases the likelihood of
her having sex with someone else when you were elsewhere. What were chastity
belts about when the guy picked up and decided to
spend the next six years trying to liberate Jerusalem
from the Ottomans or whatever off in the Crusades? And just so you don't have any
ideas over the next half decade while I go die from the plague
somewhere in Eastern Europe, that's when those were,
again, a model of cultures where there were
extended periods of men being away from women. You have very often
elaborate cultural inventions for men trying to control the
reproductive access of women. What that also winds
up doing is explaining what was thought to
be the dominant models of reproductive success
and reproductive choice in all sorts of other species. And seen, for
example, in something like baboons, what you had
was termed the linear access model of reproduction. It goes as follows. You have a social
group-- for example, a baboon social
group-- and there is only one female who is in
estrus, only one female who is ovulating. Who winds up mating with her? The alpha male in the troop. Now instead, there's two
females who were ovulating. Who gets the two females? Numbers one and two
in the hierarchy. Three females-- numbers one,
two, and three get the female. And implicit in that is the
activeness implied in the word "get," the passive
lack of choice at the female end of things. This was the linear access
model in which male dominance rank was entirely predictive
of male reproductive success. So that's what people
thought lots about then. That was the original thinking
about the relationship between male dominance rank
and reproductive success. As we will see shortly,
it's not quite so clear. Lots of other species, where
you see males attempting in the evolutionary
sense, attempting to limit female access
to other males-- this is the whole world
of copulatory plugs. Lots of dog canine related
species, where a semen plug is left there in the vagina
of the female, which soon hardens into a
plug like nothing else is happening there. You see that. There are other cases. There are fly species where
the males penis is barbed, and ooh, I heard a--
I'm not drawing that. What are you thinking? Where it's barbed and
where the barbs, in fact, go in the opposite direction,
point back at the male. Once you get the penis in there,
and it's not coming out again. It's like one of
those-- you put your-- [LAUGHTER] Well, it's actually
not like one of those, but you get the point. And what's that about? The male leaves
his penis in there, which he manages to
do without afterward, because they can make new ones. And this is a very different
world you've got here. Then you've got the whole world
we've already heard about about sperm competition, of sperm from
one male in various fly species containing toxins that will
kill the sperm of another male. Then there's a whole
interesting world that goes on, which is when
males mate with a female, they do something
biochemically, which decreases the sexual
attractiveness of the female
subsequent to that. In a number of fly
species, males with mating release a chemical, which
decreases mating pheromone production in the female. And suddenly, nobody else
is interested in her, or there are other
flies species where males release a chemical, which
decreases sexual proceptivity in the female. Viciously clever ways
for males to control female reproductive
behavior after they've left. Male-male competitive
strategies. So what do you see at
the female end of things? No surprise, you see
female counterstrategies. One brilliant one
that evolved in humans is this relatively unique human
phenomenon of hidden ovulation. Yes, all that pheromone
stuff and smelling people's armpits and things that don't
happen much in the real world, but what you see for the most
part is that humans are not terribly aware of where
somebody is in their cycle. Humans have invented
hidden ovulation. What's that meant to do? Decrease paternity certainty. And one argument is
that's a good mechanism for decreasing the likelihood
of competitive infanticide. The other is it
decreases male attempt to control female
sexual behavior, because it's less clear when
you need to be doing that. So counterstrategies. More examples-- this is argued
that in some species that have non-reproductive sex
throughout the cycle, that is a female counterstrategy
to, again, fool the male when ovulation is actually occurring,
increasing the likelihood that at such times, she can
get somebody else's genes. Other strategies-- we've already
heard about one-- [INAUDIBLE] in the competitive
infanticide one, which is that whole world of females
that can fake being in estrus, that go through pseudo
estrus, all of this meant to be ways of keeping
males a little bit less certain of when they should be trying
to control female sexual access, and thus, she has more
choice in the matter. What that brings
us to is thus-- oh, that's something
interesting that I left out. Eh, it's not that interesting. OK. So back to male-male
competition. This was first looking at
male in lots of species, male attempts to regulate
female sexual behavior, female counterstrategies. What's up with
male-male competition in terms of evolution
and sexual behavior? Most obvious one being
is male-male competition for reproductive access
and the standard old models being that linear access model--
one female winds up with number one male, two, and so on. What that thus
begins to explain is when you look at all
social species out there, the leading cause of aggression
is male-male aggression built around female access. And as we'll see
by next week, that is the case as well for every
human culture ever looked at. You also see, of course,
the sperm competition. And once again, we have
one of those issues with humans, which is where do
we fit on the spectrum there? If you have a
monogamous species, males tend to produce only
small amounts of sperm and tend to have small testes. When you have
polygamous species, males want to pump out
insane amounts of sperm to increase the likelihood of
outcompeting some other guy's sperm if it shows
up on the scene or for making a sperm plug, and
what you wind up getting there in those species
are large testes. So you look at the
various primates, and chimps have gigantic
testicles per body size. Gorillas do not. Gorillas that have a
very different world of male-male com--
what about humans? Once again, the
same exact thing. We are about halfway in between. When compared to
other primates, we are intermediate between a
tournament species and a pair bonding species in
yet another domain. We've been hearing about
this again and again. Something really
interesting that has been shown in humans, which is--
no, I'm not going to tell that. That's too hard to explain. But it was great. You would really wish-- so
now what we have is also looking at evolutionary aspects
of female choice in there, and in what cases do you get
female-female competition? First off, the answer
was obvious in terms of looking at traditional
tournament species, which is that females have no choice
who they are mating with. It's linear access models. One female winds up with
the alpha male, two females and so on, and this
was the dominant model in all of primatology
starting in the '60s. And then by around
1980 or so, it was recognized that,
in fact, there's virtually no evidence
for strict linear access models of the main determinant
of who a female mates with is who's the winner of male-male
competitive interactions. People discovered at the
time that, in fact, there was this strange, strange
violation of all these models, because it turned out the models
were not based on behavior. And this generally was
discovered around that time, because that was around
the time that the majority of primatologists on
earth suddenly became female and started looking
at the female end of things and discovered that this
linear access stuff is not, in fact, what occurs. And out of that came a
completely shocking concept that ran through primatology
like a bolt of lightning-- the notion that there was--
this is the technical term-- some degree of female choice. Oh, whoa. That's kind of bizarre,
where females have something to do with who they mate with. And there's been a whole
world of primatology studies since then showing what
female choice is about. First off, how
does female choice occur in a typical
tournament species? You've got this problem. With primates, for example,
you wind up with a pair bond, with a consortship between a
male and an ovulating female, and because it's a
tournament species, the male is twice
the size or has big huge canines or whatever
stuff he's got there. He is physically able
to dominate the female quite readily. You do not see female choice
in those cases being exerted by the female
beating up on the guy and her getting to go mate
with who she's interested in. What you see is much
more clever behavior on the part of the female. She will, for example,
exhaust the guy. Every time he sits down
to feed, the female gets up and starts walking. And he has to jump up and
pile together the picnic and go running after her. Every time he tries to take
a nap, she goes walking. Or what you find with baboons
is the most clever thing that females do is they go
walk and leave the male right in front of his
worst rival, or then they'll do it again
and again and again and get the guy totally
harried out and crazed, and at some point, those
two males will have a fight. And what then happens is
she runs off to the bushes and has what is
technically called a stolen copulation with the guy
she's actually interested in. Maybe it's not so bad
to be a female baboon. So now what this
brings us to insofar as this alternative female
strategy is available, we now come to this
absolutely critical question, one that is run through
the ages, which is, what do female baboons want? Who do they want to mate with? And people are not
positive, but there is some suggestion in the data. It needs to be replicated more. There is this trend, but
there's this suggestion that female baboons like to
mate with male baboons, who are nice to them. No, are they sure? Are they certain? Have they done their
statistics right? They go, and they mate with
guys who groom them a lot, guys who play with
their infants, guys who, when they're in a
bad mood, don't beat up on them but beat up on somebody else. This counts as a prince
of the male baboon. This is someone you
take home to meet mom. When he's in a bad mood, he
pummels someone else, not me. This is someone you
want to mate with. And in the mid 1980s, excellent
primatologist Barbara Smuts of University of
Michigan came up with the very jargony
scientific term that all sorts of
non-human primates have intersexual friendships. And that's not an
anthropomorphic term. What it was though
was people sort of snickering at it in
that the initial notion was that these were just friends. These were platonic
monkey relationships. They were not
about reproduction, and it was not until people
got good enough and enough data to start picking up on all
those stolen copulations to see that the
females were picking up and mating with their nice
guy-- oh, we're just friends. I could never see him--
whoa, and they're suddenly in the bushes with him. And it suddenly turned from the,
yeah, nice guys finish last. OK, they do lots of grooming,
but let's count the number of copies of genes,
to becoming apparent that the being a nice guy was a
viable alternative reproductive strategy as long as there was
this thing of female choice. And what the paternity
studies began to show was that was a very viable
alternative strategy, in part, because you're not
mating anywhere near as much if you were a low
ranking affiliative male. With a female, you're not
mating anywhere near as much as the high ranking males,
but you're not burning out. You're not getting injured. You're not having the
male-male fighting. You live a lot longer,
and this keeps happening. There's a problem,
though, which is suppose you are a
female baboon, and you want to mate with
this nice guy, and one of the things that
he's nice about is he's nice to
your kid, who's now about three or four years old. And there's a very
good chance that where that affiliative
relationship started with him got jump started was
the fact that he was the most likely father of that kid
and has developed somewhat of an affiliative
relationship with the kid and hangs out with them
and hangs out with you. And so you've
established this is a nice guy I want to mate with. But there's a problem,
which was if he was the likely
father of your now three, four-year-old
offspring, the odds are that three,
four years ago, he was a pretty high ranking male. And what that means now
three, four years later is he's likely to be some
aging guy over the hill, whose rank has been dropping. In other words,
not someone who is going to be very effective
at male-male competition, and you get this
horrible sort of tension there going on between the
male-male competitive world generates some Arnold
Schwarzenegger jerk, who's the one who's supposed
to be where she wants to mate with Alan Alda or whoever. And what you have
then is he's not up to the male-male
competitive stuff, because he's some aging guy. And you instead have the
world of stolen copulations. So isn't that great? Isn't that heartwarming? A whole world of what are now
called alternative strategies. If you're some scheming
male baboon wanting to pass on as many
copies of your genes, you may decide the
really manipulative thing to do is to be
nice to some female and groom her more
than she grooms you, which is a very rare
thing for a male baboon to do. So great alternative
strategies, very heartwarming. Not so heartwarming,
because there are other alternative strategies
available in some species, alternatives where male
sexual behavior is not the outcome of explicit
male-male competition, but instead takes an
alternative strategy. And you see one example
of this in orangutans. Orangutans, great
apes, and they've got a very interesting bizarre
social system, but what you have is your basic,
nonetheless, sort of familiar picture of male-male competition
with a large percentage of orangutan male
aggressions built around the reproductive
access to females, and you've got a whole
world of very peripheralized low ranking males
who never mate. And there's an
interesting physiology that goes along with it. That was the picture that
everybody used to have, and then in the 1970s, pioneer
researcher in this, Birute Galdikas, who has studied
orangs for decades out there in Indonesia,
she noted something really disturbing,
which is low ranking, non-reproductive male orangs
have an alternative mating strategy. What do they do? They rape females, and this
was the first introduction of that term into
zoology, and that is not an anthropomorphism. If defined as a violent
process of mating with a female against
her will, this is what goes on in orangutans. A certain percentage
of reproduction is low ranking guys who
have no direct access to females as a result of
male-male interactions. This is not the nice
guy alternative, so there is precedent
for this also. And this is by now very
well-documented behavior among orangutans. Then if you want to
call it with something very subtle and clever,
there's apparently this whole world
of fish species, where low ranking males
can pretend to be a female and take on female coloration
and pretend to be just friends and someone they
can pour their heart out to, and then suddenly one
day they have a penis, and where'd that come from? And everything
suddenly changes there. OK. So we have the very
strict boring models. Females invest more
calories than males, and, thus, they are
much more picky. Males mate with females
entirely as a function of male-male competition,
and thus, evolution is driven by male
aggression and all of that. Let me just see as
people are clearly about to run out the door. For more, please visit
us at stanford.edu.
