Wednesday, December 1, 2010

Out of the Shadows: I No Longer Believe in Human Pheromones


From my earliest fascination with animal behavior in college, through my pure sensory research phase at the Monell Center, and into my mercenary research phase in the fragrance industry, the question of human sex pheromones was never far from mind. Having studied sexual behavior and smell, I eagerly read the new studies and attended the promising talks hoping to see a definitive answer emerge. Curiously, as more research was done the case for human pheromones became more tentative. Researchers I knew and respected couldn’t even agree on basic physiological facts: do humans have a vomeronasal organ or not? If it exists is it functional? If it’s functional, does it deliver a behaviorally relevant message?

I grew increasingly impatient with this state of affairs. I wasn’t the only one seeking clarity: an endless parade of associate beauty editors, science reporters, and generally intelligent people asked me whether there was anything to the idea of human sex pheromones. The best I could offer them was the lame proposition that while the molecules and the means to perceive them might still exist, the effects of human sex pheromones were unlikely to be as dramatic as those in insects or rodents. This didn’t satisfy the associate beauty editors nor did it satisfy me. Reserving judgment in the face of conflicting data is a bedrock principle of science but it doesn’t make for good sound bites.

According to the definitions first developed in the early 1960s, a sex pheromone should trigger an invariant, reflex-like behavior in most people who smell it, and it should consist chemically of (ideally) one to (at most) a small handful of specific molecules. In theory, uncorking a sample tube of male pheromone ought to make women go gaga, while a nose full of female pheromone should make men go stiff, something along the lines of the wickedly clever story by Roald Dahl called Bitch.

So, thousands of studies and millions of research dollars later, where are we?

Richard Doty, a smell researcher at the University of Pennsylvania, has now supplied the book-length answer. In The great pheromone myth, Doty provides an exhaustive—and sometimes exhausting—account of the science behind mammalian pheromones. But this is much more than a summary of 50 years worth of research—it is a thorough and relentless examination of the evolving scientific claims made for the pheromone concept itself. And it is here that Doty has provided a major contribution: nothing less than an complete take-down of human pheromones.

The great pheromone myth is an argumentative tour de force. Like a skilled prosecutor cross-examining witnesses, Doty sets the trap by quoting researchers themselves as he reviews the definition of pheromones. From one scientist to the next we find inconsistencies, contradictions, and special pleading. The cumulative effect is devastating: it demonstrates the intellectual incoherence surrounding the term. A pheromone is a simple chemical—except when it’s a blend of chemicals. A pheromone has an innate releaser effect on other animals—except when learning or context is involved. Doty also quotes those who along the way cautioned about extending the pheromone concept from insects to mammals. Like a good courtroom lawyer, he plants seeds of doubt in the minds of jurors.

Doty spells out the technical shortcomings of animal and human experiments, but he always returns to his theme: that the results rarely meet the criteria for a pheromone, even as the criteria become ever more expansive and flexible. 

As Doty dismantles one pheromone claim after another, he also builds a powerful case for the behavioral and physiological effects mediated by body odors. Mothers recognize infants, infants recognize mothers, lover recognize each other—all through natural body scent. Many of these effects involve learning and the evaluation of context, even in rats. For example, “male rats exhibit an increase in testosterone and luteinizing hormone following exposure to the wintergreen-smelling odorant, methyl salicylate, when the odor had been paired with previous copulation.” Mice raised until weaning with artificially perfumed parents later prefer to mate with similarly scented mice; mice raised unscented prefer unscented partners. These results show the importance of smell in sexual behavior and speak to learning and adaptability; but they are hard to square with the idea that mammals respond only to pheromones composed of highly specific natural body scents.

To all of which one might reply, so what? So what if there is no solid evidence in mammals that meets the narrow technical definition of pheromones? What’s wrong with calling all these various effects pheromonal?

The problem is that the pheromone concept does no intellectual work. It provides no leverage for discovering new facts or phenomena. Pheromones are the intellectual version of elastic-waisted fat pants—the concept expands to accommodate each and every claim made for it. Once upon a time instinct theory was equally in vogue and used to “explain” all sorts of behavior. Today it’s rarely invoked. By specifying the roles of context and learning, behavioral science simply outgrew the need to appeal to instinct.

Today we are seeing a new wave of research by scientists such as Denise Chen, Bettina Pause, Johan Lundström, and others showing that body odors can transmit emotional state from one person to another, and can alter brain processing and hormonal levels. It’s clear that we are much more affected by the scent of other people than previously thought. The effects are many and varied; more will doubtless be revealed. But what is gained by shoving them all under the umbrella of “pheromones”? Very little, I believe. Like Doty, I’m pessimistic the public will ever give up its fascination with pheromones, but it’s time for scientists to file them away—right next to phlogiston—in the drawer labeled “formerly useful concepts”.

14 comments:

~x~ said...

On this one count, you may be mistaken.

Also, the thing where he doesn't review blind *works* because he's evaluating the bottles and the companies that chose to back the juice.

Nathan Branch said...

Avery -- Very thoughtful and concise article. You've talked before about your research into pheromones and how it constantly lead you to nothing but dead-ends, so it must be a relief of sorts to run across a book that compiles so much information into one place and makes a sound case for abandoning the study of human pheromones.

No more wasted time and money!

But a great conversational starter, right?

Avery Gilbert said...

~x~:

?

Avery Gilbert said...

Nathan Branch:

You must be referring to the long-suppressed story of how I almost caused a perfumer riot at Givaudan by having my technicians mix a female rhesus monkey sex pheromone in the lab.

Ah, good times, good times.

This means I'll probably never again be asked to comment for a sex and scent story in Allure-Cosmo-SELF-Men's Health-Redbook-Shape-Fitness-InStyle. Despite the fact that I believe there is overwhelming evidence for smell being central to sexual attraction, arousal and bonding.

I'm just done with the term "pheromone".

~x~ said...

randomness.
cause i read you pretty much daily, and then the guide is my bathroom book...
random + apologetic = me

EdC said...

"...Despite the fact that I believe there is overwhelming evidence for smell being central to sexual attraction, arousal and bonding."

Avery,
Your way is now clear to develop and spread the true theory of how smell does help. Fragrance houses still want us to buy 'fumes before a big date. And buyers still want a little help with that date. without pheromones they'll have to come to you.

Avery Gilbert said...

~x~:

Whew. I thought it was me.

James V. Kohl said...

Nothing in the 1959 definition indicated an invariant response, and with what is now known about epigenetics, the insect model of pheromones extends very well across species to include human responses. As I have continued to detail in the past two decades, the effect of pheromones is on hormones and the hormones are associated with the behavioral affect. The physiology we share with other animals is very telling when it comes to genetically predisposed responses to stimuli from our social environment. Food odors do not cause an invariant response, why would pheromones?

Avery Gilbert said...

James V. Kohl:

As you point out in your book, smells can alter behavior indirectly by modulating hormonal and other physiological responses. This has been called the “priming pheromone” effect. Doty believes the evidence for priming pheromones in mammals is weak and artifactual.

I think we agree that the effect of an odor often depends on the smeller’s sex, age, hormonal state, status rank, previous exposure and experience. Here’s my point: If we stretch the definition of pheromone to include all these qualifiers, we pretty much drain the term of meaning. For example, a male mouse prefers to mate with Chanel No. 5 scented females because that’s what an experimenter applied to his mother. Under the wide open definition that makes Chanel No. 5 a pheromone.

So the alternatives are (A) a tight definition under which nothing qualifies as a sex pheromone, or (B) a loose definition which makes the concept worthless. I choose (C) none of the above.

James V. Kohl said...

Avery,

I will try to succinctly address your points.

The required levels of biological organization (i.e., gene-cell-tissue-organ-organ system) have been detailed. So has the evolved neurophysiological mechanism that links mammalian pheromones to their priming effect on hormones. The evidence is not weak, it's overwhelming!

I do not advocate stretching the original definition of pheromones. They are social odors and they release definite behaviors. The definite behaviors exist because of the developmental (hormone-driven) processes the pheromones effect.

I do not advocate limiting the original definition. There is no science from any species that indicates that the concept infers (as Doty does on page 3) “…that a plurality of mammalian behaviors and endocrine responses is uniquely determined in an invariant way by single or small sets of chemical stimuli….”

The male mouse (or the males and females of any species) must first have been genetically predisposed to respond (or not) to the epigenetic influence (on hormones) of a mother’s pheromones. Otherwise no animal could be conditioned to respond to the initial association of a mother’s pheromones with the odor of a perfume.

Maternal pheromones can be considered sex pheromones because females produce more of the hormones that metabolize to the pheromones of females than do males (and vice versa). These sex pheromones also are processed by a sexually differentiated olfactory system, which allows them to have a different effect on the hormones of males than on the hormones of females, and the effect on hormones is what causes the behavioral affects.

The sexual dimorphism is the main reason to keep the concept of sex pheromones, as they are central to the development of sexual preferences. Food odors, for comparison, are central to the development of food preferences, but there is no sexual dimorphism in the food odors or in how they effect the hormones of males and females, or in how those hormones affect behavior.

If we eliminate the concept of sex pheromones, there is no biologically based explanation for the development of either typical or atypical mammalian sexual preferences (and associated behaviors that are sometimes manifest). Doty's attempt to disprove the existence of mammalian pheromones, which include mammalian sex pheromones is akin to me attempting to prove that food odors don't exist. After all, no single or small sets of food odor uniquely determine in a invariant way the plurality of mammalian behaviors and endocrine responses associated with the development of food preferences.

The rest of the story will become much more clear in the next few months as the eusocial insect model of olfactory/pheromonal influences is extended to mammals, including humans.

Kind regards,

Jim

Anonymous said...

I fully support the opinion of James Kohl about pheromones. There are numerous papers that show evidence for (i) priming effects of released intraspecific semiochemicals on the hypothalamus-hypophyseal-gonadal axis of both non-mammalian and mammalian species, resulting in elevated (steroid) hormone secretion, and (2) the releasing effects of such compounds on the behavior of many vertebrates. I recently reviewed the knowledge on such semiochemicals, termed pheromones, in my recent book ‘Intraspecific chemical communication in vertebrates with special attention to sex pheromones’, 191 pp; ISBN: 978-90-77713-78-5; @ 2011 by R. van den Hurk (r.vandenhurk@planet.nl).
The opinion of Doty that pheromones are a myth is a consequence of the lack of an appropriate and uniformous pheromone definition. In my opinion, pheromones are excreted, intraspecific working semiochemicals that (at least initially) act unconscious and in concentrations of nanograms to picograms. If a semiochemical is effective only in larger concentrations, it isn’t a pheromone but an odorant. When administered in higher concentrations, pheromones often result in no or a repulsive behavioral effect.
The Chanel 5 experiment shows a learned effect on mammals. Chanel 5 is not excreted by mammals, so cannot be termed a pheromone. It is an odorant.
Within a group of zebrafish, the significance of a sex pheromone has to be experienced (learned); isolated male conspecifics do not have the skill to discriminate female sex pheromones. Upon a confrontation with a female, the males start fighting often resulting in their death. A pheromonal experience is possibly recorded in a certain part of the cortex, whereafter a pheromone does not necessarily act unconscious anymore.

Rob van den Hurk

James V. Kohl said...

Published yesterday in Socioaffective Neuroscience & Psychology. Along with the other articles in this issue, my article makes clear that pheromones are ubiquitous from microbes to man, and the molecular mechanisms of their effects on behavior are the same in insects and mammals, as would be expected from what is known about the difference between nutrient chemicals and pheromones.

Human pheromones and food odors: epigenetic influences on the socioaffective nature of evolved behaviors .


Background: Olfactory cues directly link the environment to gene expression. Two types of olfactory cues, food odors and social odors, alter genetically predisposed hormone-mediated activity in the mammalian brain. Methods: The honeybee is a model organism for understanding the epigenetic link from food odors and social odors to neural networks of the mammalian brain, which ultimately determine human behavior. Results: Pertinent aspects that extend the honeybee model to human behavior include bottom-up followed by top-down gene, cell, tissue, organ, organ-system, and organism reciprocity; neurophysiological effects of food odors and of sexually dimorphic, species-specific social odors; a model of motor function required for social selection that precedes sexual selection; and hormonal effects that link current neuroscience to social science affects on the development of animal behavior. Conclusion: As the psychological influence of food odors and social orders is examined in detail, the socioaffective nature of olfactory cues on the biologically based development of sexual preferences across all species that sexually reproduce becomes clearer

Avery Gilbert said...

To my readers:

James V. Kohl's most recent comment was submitted yesterday morning but not immediately posted because Blogger directed it to a spam inbox. I discovered this a few minutes ago and posted it immediately. I apologize for the delay.

The paper he refers to is available here.

Regarding his argument, I have only one observation. If there are so many parallels between pheromones/social odors and food odors, doesn't that argue against pheromones being a special class of chemicals in mammals?

James V. Kohl said...

Avery,
Thanks. Unlike nutrient chemicals associated with food odors, pheromones are a special class of chemicals because they are species specific across species from microbes to man.