Conditional response, alternative strategies, and female orgasm

I'm trying to resist becoming a hotbed of female orgasm blogging, but I just heard a promo for the story on the local news, so it seems impossible to avoid. Moreover, the issue has become a genuinely interesting debate about the role and method of evolutionary analysis. On this, I have a small contribution to make.

The Guardian is running a story on research by Kate Dunn and colleagues (2005) into the heritability of sexual response in women. Here's the abstract:

Orgasmic dysfunction in females is commonly reported in the general population with little consensus on its aetiology. We performed a classical twin study to explore whether there were observable genetic influences on female orgasmic dysfunction. Adult females from the TwinsUK register were sent a confidential survey including questions on sexual problems. Complete responses to the questions on orgasmic dysfunction were obtained from 4037 women consisting of 683 monozygotic and 714 dizygotic pairs of female twins aged between 19 and 83 years. One in three women (32%) reported never or infrequently achieving orgasm during intercourse, with a corresponding figure of 21% during masturbation. A significant genetic influence was seen with an estimated heritability for difficulty reaching orgasm during intercourse of 34% (95% confidence interval 27-40%) and 45% (95% confidence interval 38-52%) for orgasm during masturbation. These results show that the wide variation in orgasmic dysfunction in females has a genetic basis and cannot be attributed solely to cultural influences. These results should stimulate further research into the biological and perhaps evolutionary processes governing female sexual function.

At the Philosophy of Biology weblog, Elisabeth Lloyd (author of aforementioned book on female orgasm evolution) has a post generally supportive of the paper itself, but very critical of press accounts of it. She directs her greatest criticism toward the following comments by study senior author Tim Spector, which appear in the Guardian article:

Tim Spector of St Thomas's hospital in London, who led the research, said: "The theory is that the orgasm is an evolutionary way of seeing if men can prove themselves to be likely good providers or dependable, patient and caring enough to look after the kids."
Women who orgasm very easily may be more likely to be satisfied with poor quality men.
"Perhaps women who had orgasms too easily weren't very good selectors," Professor Spector said. "It paid women to be more fussy and this is one way of doing it. The simple fact is that it takes women on average 12 minutes and men two and a half minutes to reach orgasm. Adjusting to that imbalance is a test."

Lloyd has done a lot of thinking about this hypothesis, and she has a lot of ammo to unload on it. I quote from her post to give her deconstruction with some of its original clarity:

As the Guardian article makes clear, Spector is (re-)proposing a theory that orgasm is a mate-selecting device; he claims that the fact that orgasm during intercourse is difficult to attain is an evolutionary adaptation itself, making the well-known variability in orgasm among women an adaptation.
But we run into trouble immediately. The proposed adaptive state is a conditional response to quality males - have an orgasm if he's a good guy, don't if he's not - and under this theory, clearly the population of women was under selection pressure to have moved towards that optimum peak (balanced by the usual energetic costs, and so on). So why would that be an argument for the variability of orgasmic response, and not an argument for the standard result of a directional selection regime, namely, a peak at the optimum?

She goes on to summarize the data from the study, which fairly convincingly show that all females cannot have been selected to pursue this strategy -- their variability is too extensive:

If selection has been of any appreciable strength, and has been going on at least since the advent of archaic humans, we should expect that nearly all women would have such a conditional response to intercourse, and thus that nearly all women would be capable of orgasm with intercourse under the right conditions. The bad news is that there is no evidence for such a peak at all, that a full third of women rarely or never have orgasm with intercourse, and that as many as one out of ten women don't have an orgasm even once in their lives. There is a small peak in the distribution, but it is located at the non-orgasmic segment of the distribution. In other words, this is the kind of variability he needs to support his theory, and his own data show that the supporting evidence just isn't there, as I'll detail in a moment.
But there's another kind of variability, namely, that some women never have orgasm with intercourse, some women always do, and some women sometimes do and sometimes don't. This kind of variability is the kind that they do document in their study, and this kind of variability would not be selected for under his proposed hypothesis, but perversely, he implies that it would.

Heritability and alternative strategies

But I'm not sure that Lloyd and Spector are really talking about the same hypothesis. (Disclaimer: Hey, I don't know, maybe they are, in which case Lloyd's critique is more valid than I suggest.) The prologue to the Spector quote taken from the Guardian reads as follows:

The findings suggest the failure of some women to orgasm regularly is not a dysfunction, but a sophisticated mate-selection strategy that evolved during prehistoric times.

When I read that, I believed that Spector was arguing that some women (namely the ones with rarer orgasms) may have had an adaptive strategy for conditional response to male quality, leaving unstated the obvious corollary that other women may pursue different adaptive strategies.

After all, the idea that all women follow the conditional response strategy is ridiculous on its face: it cannot explain the women who reach orgasm easily and quickly most of the time, regardless of partner. If female orgasm is an adaptation, clearly there must be at least two distinct strategies: one in which orgasm is difficult and arrived at only through certain efforts, and one in which orgasm is readily achieved. There is no reason why these alternative strategies may not competed with each other in ancient human populations, considering each may have distinct advantages and drawbacks. A quick orgasm may make sex very compelling, possibly resulting in a higher frequency of inseminations -- possibly from multiple male partners. This strategy would reduce the risks associated with partnering with a single male (especially the risk of male infertility), while increasing the genetic diversity of a woman's offspring. In contrast, the conditional response strategy might have the predicted effects in encouraging female choice for male quality. Please remember that neither of these strategies has been tested, nor has the effect of their conjunction; I merely say that the hypothesis is conceivable that both of them coexisted as genetic variants within ancient human populations.

Indeed, there is no reason why there should not have been a large number of different adapted strategies toward female orgasms in past human societies. Human sexual experience must have been highly heterogenous, and the selective consequences of partially heritable mating strategies would interact in a complex way. It has the makings of a very interesting evolutionary problem.

Now, I agree that the uncritical acceptance of these hypotheses is not warranted. And I agree with Lloyd that a nonadaptive hypothesis is also very credible. The data do not point one direction or another at this point. But it is far too soon to discount the possibility that there are multiple adapted sexual strategies in human females that incorporate orgasm in differing ways.

Considering the hypothesis of alternative strategies, Lloyd's critique is mostly hollow. Consider the following passage:

The fact that this new study establishes a heritability of .45 for orgasm with masturbation (which is much more revealing than orgasm with intercourse, as far as basic orgasmic capacity goes), is also very damaging to any adaptationist account, and I'm surprised that technical people aren't saying so. Traits that are species-adaptations, such as, for example, having the capacity for language, or starting off with a good sense of taste, or having a massive brain, have heritabilities near zero. Nearly all the variability has been used up, selected out. This is just the end result of what I've just recited about the peaks in distributions. If selection is strong enough and goes on for long enough, variability around the peak gets weeded out through selection, and we're left with just one type plus random mutation and somatic, developmental, and environmental accident. Traits with heritabilities near .5 are not even close to being decent candidates for species-wide adaptations, for just this reason, as is widely known (I thought...).
FOURTH CONCLUSION: Spector's own heritability results also indicate that female orgasm is not an adaptation. Is it only population geneticists who know that species-wide adaptations have heritabilities near zero? How can it be that an expert on heritability like Spector doesn't know this? I guess this piece of knowledge might be a casualty of over-specialization.

I guess I'm as "technical" a person as has considered the issue lately, and Lloyd is just wrong about this. Certainly it is true that Fisher's Fundamental Theorem predicts that the heritability of a trait will decrease under directional selection, but Lloyd has provided us no reason to suppose that selection on female orgasm need have been directional in its pattern. Even if it were true that female orgasm were centered around a single strongly selected peak, it is far more likely that this peak would be the product of stabilizing selection rather than directional selection. The persistence of genetic variation (and thereby heritability) in such a scenario would depend on the effects of the genes themselves (e.g., is there heterosis? epistasis? antagonistic pleiotropy?). There is no simple answer to these questions, we have no knowledge whatever about the genes influencing female orgasm, and hence, it is impossible to make categorical statements about the likely heritability of the character after a history of selection.

If, as I think is a more likely scenario, there are alternative adaptive strategies toward female orgasm in humans, then it is not only likely, but necessary that the trait have substantial heritability. Unless offspring are similar to their parents, there is no sense in which alternative adaptive strategies can exist as adaptations (although under such circumstances they may well exist as cultural strategies without necessary genetic correlates).

"Species-wide adaptations"

Likewise, Lloyd's "fourth conclusion" confusingly states that "species-wide adaptations have heritabilities near zero." Remember that heritability is simply the proportion of phenotypic variance explained by genetic variance. Heritability may be near zero if phenotypic variance is high while genetic variance is very low. It may also be near zero if phenotypic variance is very low -- if the population just does not vary in the trait under consideration.

What does Lloyd mean by a "species-wide adaptation"? This is not clear to me, because her examples clearly are different in terms of variability. Humans today universally have language, and they universally have large brains (compared to, say, chimpanzees). But while the heritability of linguistic capacity is unknown, the heritability of brain size is very high in today's humans (> 0.9). Thus, it is desirable that we should be very careful in describing a trait as a "species-wide adaptation," at least if by this we mean to include some limit to the degree of potential heritability.

The example of language would seem to imply a discrete feature that differs categorically between species. A simpler example (that does not beg the question of ape linguistic capacity) is one of the human adaptations for obligate bipedality: an adducted big toe. Almost no humans have an opposable big toe; almost no chimpanzees have an adducted one. The distribution of variation of such traits nearly completely separates different species from each other, and within a species their heritability is near zero -- because their variation is near zero.

If this is the kind of trait Lloyd refers to, then it is true but trivial that such traits have heritabilities near zero. The fact that their phenotypic variance within a species is near zero allows no other conclusion. It is equally true that if we assert that female orgasm is a "species-wide adaptation" in the sense of being categorically absent from other species, then we must conclude that its heritability within humans as a categorical trait must be near zero.

But there is no reason to think that any aspect of female (or male) sexuality is a "species-wide adaptation" like an adducted big toe. As Lloyd's example of brain size makes clear, many species-typical adaptations have substantial within-species heritabilities. For example, humans have a high valgus angle, meaning the angle at the knee joint between the long axes of the femur and tibia. This angle facilitates bipedal locomotion by placing the tibia beneath the body's center of gravity during single-legged stance. This trait is clearly species-typical: human femora can easily be differentiated from chimpanzee femora by the valgus angle. But at the same time, the valgus angle itself is variable within humans. That is to say, the distribution of this continuous variable both separates humans from chimpanzees and distinguishes humans from each other. Within humans, much of the phenotypic variance is explained by underlying genetic factors, through the phenotypic correlations with other traits, such as stature, leg length, and pelvis width. Thus, this human-specific trait is moderately heritable within humans.

Human-specific traits in which alternative strategies underlie variation likewise are extensively heritable. As a case in point, human intelligence is substantially different from intelligence in any other hominoid species. Although some (hypothetical) measurement of intelligence might show some slim overlap between humans and chimpanzees in its distribution, the mean values of the two species are so different that they defy scaling. Even so, intelligence is both substantially variable in humans and substantially heritable. This heritability of intelligence may have many causes, but one of them must be the fact that intelligence itself comprises many different mental abilities that each have separate adaptive consequences. It is widely believed that such adaptive variation may in part predispose people to differing behavioral strategies, including variation in personality.

I tend to think this is not very far from the mode of evolution of human sexuality. Dunn et al. (2005:3) in fact consider mental factors as potential behavioral mediators:

Other potentially imoprtant biological factors include androgen levels or receptors, or natural variations in pleasure centres in the brain, resulting from dopamine or other psychological mood effects. All of these processes are probably mediated to some extent by genetic variations. Other associated factors, such as differences between individuals in anxiety and depression, also have heritable components and may partly contribute to the genetic component of orgasmic ability reported here.

It seems shortsighted to consider the evolution of female sexuality in isolation from the complex neurological factors that mediate female social behavior. A low frequency of orgasm during masturbation has little meaning as an adaptive character. The response to social situations, nonsexual interactions with female peers and potential male -- and female -- sexual partners, and long-term stresses must be considered in a full account of the biology of sexuality. The story does not begin or end at the clitoris, but must ultimately focus on the human as a psychological whole.

After all, the first lesson in health class is that the most important sexual organ is the one between the ears.

UPDATE 6/10/05: Elisabeth Lloyd has been kind enough to comment on this post in the comments to her original post on the subject. This has cleared up much confusion, particularly concerning the state of adaptive hypotheses for female orgasm.

Apparently, although I would never have guessed it, my hypothesis of multiple alternative strategies is novel. It seemed almost too obvious to be worth posting to me, since most of my recent thinking has been about brain evolution where these kinds of alternative strategies are common parlance. If you are a scientist reading this, take note: this is one of the great advantages of blogging, since what seems obvious to you may not be so to someone in a different field, and vice-versa.

In her comment, Lloyd acknowledges my point that only directional selection necessarily reduces heritability, but informs us that adaptive hypotheses concerning female orgasm have been framed exclusively assuming directional selection. In this case, her arguments certainly do apply to those hypotheses. This is one of the drawbacks of contemporary adaptationism that is not included in Gould and Lewontin's classic essay, "The Spandrels of San Marco": the frequent assumption that adaptations are the result of directional selection rather than other patterns. It is also a frequent confusion as applied to Sewall Wright's concept of adaptive peaks, which are not maintained by direcional selection, nor are they necessarily reached by it.

At any rate, as I mention above, I scarcely think the hypothesis of alternative strategies is testable. By introducing the possibility of many additional parameters, the hypothesis conceivably may be consistent with almost any distribution of orgasm incidence or facility. The important question is whether the hypothesized strategies may be biologically justifiable, and this will necessarily remain an impossible question to answer as long as the other behavioral correlates of such strategies are unknown. Lloyd's comment points out the problems with some such strategies as applied to the evidence. This is a bouncing ball in a sense: whenever one strategy is demonstrated to be biologically problematic, one might still propose a different set of strategies that would be commensurate with the same observations. At some point this becomes a reductio ad absurdum, but there is little chance that even the first level of two contrasting adaptive strategies can be tested with data now available.

Also note, that the more we consider correlates of female orgasm, the more we approach a non-adaptive hypothesis. That is to say, if female orgasm depends for its frequency, pattern, and existence upon other psychological or behavioral qualities, then it is possibly much simpler to argue that it is selection upon these qualities rather than orgasm itself that has shaped its distribution.

So again, this is a very much more interesting evolutionary problem than at first it might appear, and very intimately connected to the evolutionary history of the human mind.

Many thanks to Elisabeth Lloyd for her gracious and thoughtful comment. I'll never snark about orgasm-blogging again!

References:

Dunn KM, Cherkas LF and Spector TD. 2005. Genetic influences on variation in female orgasmic function: a twin study. Biol Lett (advance online). Royal Society Publications online