How many genes does it take to make a squid eye?

This is an article about cephalopods and eye evolution, but I have to confess at the beginning that the paper it describes isn’t all that interesting. I don’t want you to have excessive expectations! I wanted to say a few words about it, though, because it addresses a basic question I get all the time, and while I was at it, I thought I’d mention a few results that set the stage for future studies.

I’m often asked to resolve some confusion: the scientific literature claims that eyes evolved multiple times, but I keep saying that eyes show evidence of common origin. Who is right? Why are you lying to me, Myers? And the answer is that we’re both right.

Eyes evolved independently multiple times: the cephalopod eye evolved about 480 million years ago, and the vertebrate eye is even older (490 to 600 million years), but both evolved long after the last common ancestor of molluscs and chordates, which lived about 750 million years ago. The LCA probably did not have an image-forming eye at all.

And that’s the key point: a true eye is a structure that has an image forming element, a retina, and some kind of morphological organization that allows a distant object to form a pattern of light on that retina. That organization can be something as simple as a cup-shaped depression or pinhole lens, or as elaborate as our camera eye, or an insect’s compound eye, or the mirror eyes of a scallop. An eye is photoreceptors + structure. Eyes have evolved multiple times; they’ve even evolved multiple times within the phylum Mollusca, and different lineages have adopted different strategies for forming images.

i-0f6286e48f36b86c30ae81bdbfc6f415-eye_phylo-thumb-500x210-70144.jpeg
(Click for larger image)
Phylogenetic view of molluscan eye diversification. Camera eyes were independently acquired in the coleoid cephalopod (squids and octopuses) and vertebrate lineages.

The LCA probably didn’t have an eye, but it did have photoreceptors, and the light sensitive cells were localized to patches on the side of the head. It even had two different classes of photoreceptors, ciliary and rhabdomeric. That’s how I can say that eyes demonstrate a pattern of common descent: animals share the same building block for an eye, these photoreceptor cells, but different lineages have assembled those building blocks into different kinds of eyes.

Photoreceptors are fundamental and relatively easy to understand; we’ve worked out the full pathways in photoreceptors that take an incoming photon of light and convert it into a change in the cell’s membrane properties, producing an electrical signal. Making an eye, though, is a whole different matter, involving many kinds of cells organized in very specific ways. The big question is how you evolve an eye from a photoreceptor patch, and that’s going to involve a whole lot of genes. How many?

This is where I turn to the paper by Yoshida and Ogura, which I’ve accused of being a bit boring. It’s an exercise in accounting, trying to identify the number and isolate genes that are associated with building a camera eye in cephalopods. The approach is to take advantage of molluscan phylogeny.

As shown in the diagram above, molluscs are diverse: it’s just the coleoid cephalopods, squid and octopus, that have evolved a camera eye, while other molluscs have mirror, pinhole, or compound eyes. So one immediate way to narrow the range of relevant genes is a homology search: what genes are found in molluscs with camera eyes that are not present in molluscs without such eyes. That narrows the field, stripping out housekeeping genes and generic genes involved in basic cellular processes, even photoreception. Unfortunately, it doesn’t narrow the field very much: they identified 5,707 candidate genes that might be evolved in camera eye evolution.

To filter it further, the authors then looked at just those genes among the 5,707 that were expressed in embryos. Eye formation is a developmental process, after all, so the interesting genes will be expressed in embryos, not adults (a sentiment with which I always concur). Unfortunately, development is a damnably complicated and interesting process, so this doesn’t narrow the field much, either: we’re down to 3,075 candidate genes.

Their final filter does have a dramatic effect, though. They looked at the ratio of non-synonymous to synonymous nucleotide changes in the candidate genes, a common technique for identifying genes that have been the target of selection, and found a grand total of 156 genes that showed a strong signal for selection. That’s 156 total genes that are different between coleoids and other molluscs, are expressed in the embryonic eye, and that show signs of adaptive evolution. That’s manageable and interesting.

They also looked for homologs between cephalopod camera eyes and vertebrate camera eyes, and found 1,571 of them; this analysis would have been more useful if it were also cross-checked against other non-camera-eye molluscs. As it is, that number just tells us some genes are shared, but they could have been genes involved in photoreceptor signalling (among others), which we already expect to be similar. I’d like to know if certain genes have been convergently adopted in both lineages to build a camera eye, and it’s not possible to tell from this preliminary examination.

And that’s where the paper more or less stops (I told you not to get your hopes up too high!) We have a small number of genes identified in cephalopods that are probably important in the evolution of their vision, but we have no idea what they do, precisely, yet. The authors have done some preliminary investigations of a few of the genes, and one important (and with hindsight, rather obvious) observation is that some of the genes are expressed not just in the retina, but in the brain and optic lobes. Building an eye involved not just constructing an image-forming sensor, but expanding central tissues involved in processing visual information.

Fernald RD (2006) Casting a genetic light on the evolution of eyes. Science 313(5795):1914-8.

Yoshida MA, Ogura A (2011) Genetic mechanisms involved in the evolution of the cephalopod camera eye revealed by transcriptomic and developmental studies.. BMC Evol Biol 11:180.

(Also on FtB)

Someone tell Santa about good kids’ books

There aren’t enough children’s books telling the story of evolution — every doctor’s office seems to be stocked with some ludicrous children’s book promoting that nonsensical Noah’s ark story, but clean, simple, and true stories about where we came from are scarce. Here’s one, a new children’s book called Bang! How We Came to Be by Michael Rubino. Each page is formatted the same: on the left, a color picture of an organism (or, on the early pages, a cosmological event); on the right, a short paragraph in simple English explaining what it is and when it occurred. The book just marches forward through time, showing us where our species came from. Easy concept, nice execution, and it fills a gap in children’s literature.

It’s short enough to be good bedtime reading, and simple enough for pre-schoolers. The illustrations are thought-provoking enough for older kids, but won’t keep them engaged for too long — they’ll be asking for more books to satisfy their curiosity about these strange creatures that lived billions or hundreds of millions or tens of millions of years ago. Which is exactly what we want to do to our kids, right?

(Also on FtB)

How to examine the evolution of proteins

In my previous post, I described the misguided approach Gauger and Axe have taken to criticizing evolution, and one of the peculiarities of their criticism is that they cited another paper by a paper by Carroll, Ortlund, and Thornton which traced (successfully) the evolutionary history of a class of proteins. Big mistake. As I pointed out, one of the failings of the Gauger/Axe approach is that they’re asking how one protein evolved into a cousin protein, without considering the ancestral history …they make the error of trying to argue that an extant protein couldn’t have directly evolved into another extant protein, when no one argues that they did.

The tactical error is that right there in the very first paragraph of their paper, Carroll, Ortlund, and Thornton point out the fallacy of what the creationists were doing.

Direct comparisons among present-day proteins can sometime yield insights into the sequence and structural mechanisms that underlie functional differences. Such “horizontal” comparisons, however, cannot determine which protein features are ancestral and which are derived, so they are not suited to reconstructing the events that produced functional diversity.

They don’t mention Gauger and Axe, of course — this paper was written before the creationists wrote theirs — but a methodological flaw is still spelled out plainly, the creationists reference it so I presume they read it, and they still charged ahead and did their flawed study, and then had the gall to claim their work was superior.

Ah, silly creationists. They just assume their target audience won’t bother to read the work they’re citing, and isn’t competent to understand it anyway. And they’re usually right.

The crew doing the work in the Carroll paper did not make the same mistakes. They are doing ancestral sequence reconstruction (ASR), so the effort to work backward to trace ancestral states is implicit. The bulk of the paper describes the sequencing of homologous and paralogous genes in more organisms (in this case, especially cartilaginous fishes), and the analysis of synthesized, reconstructed ancestral proteins, so it’s built entirely on an empirical foundation. And their answers actually advance our understanding of the base-by-base changes that led to the evolution of the current set of proteins. I think they were courteous and sensible (and probably, the idea didn’t even occur to them) in not comparing their work to that of the creationists — it would have been less than gracious to point out how ugly, cheap, and cheesy the stuff coming out of the Biologic Institute looks.

What the real scientists were studying is a class of receptors that respond to mineralocorticoid and/or glucocorticoid hormones. These proteins are similar in sequence and structure to one another, and are clearly paralogous: they arose by an ancient gene duplication event, somewhere around 450 million years ago. The two copies have since diverged to have different roles in hormone physiology.

The two receptors are called MR, for mineralocorticoid receptor, and GR, for glucocorticoid receptor.

MRs are activated by adrenal hormones, aldosterone and deoxycorticosterone, and to a lesser exent, cortisol. The receptors are extremely sensitive to the hormones. These hormones are important in regulating salt balance, and you might well imagine that in our fishy ancestors, as well as ourselves, regulating the concentrations of salts in our blood and tissues is a very important function. Deviations can cause death, after all.

GRs are activated by high doses of cortisol; these receptors are much less sensitive, requiring high doses of the hormone to trigger a response. They are important in regulating stress responses: they adjust the immune system and sugar metabolism. These aren’t ‘twitchy’, fast response functions like maintaining salt balance is; they are long-term, ‘last-ditch’ reactions to growing stresses, so functionally it makes sense that activation requires high levels of accumulated hormone.

Using ASR techniques — phylogenetic analysis and estimating the most likely sequence of the ancestral protein — the investigators have put together a picture of the receptor before MR and GR diverged. This protein is called AncCR, for Ancestral Corticosteroid Receptor, and it has been synthesized in the lab, so we know about its properties. AncCR is a lot like MR: it’s sensitive to low concentrations of hormone, and it responds to low concentrations of a broad spectrum of hormones.

The pedigree of these proteins is illustrated below.

i-8821726c17d966da50a695e8a1d903b7-grmr_phylo-thumb-500x280-70023.gif
(Click for larger image)
Simplified phylogeny of corticosteroid receptors. Ancestral sequences are shown at relevant nodes: AncCR, the last common ancestor of all MRs and GRs; AncGR1, the GR ancestor of cartilaginous fishes and bony vertebrates; AncGR2, the GR ancestor of ray- and lobe-finned fishes (including tetrapods); AncMR1, the MR ancestor of cartilaginous fishes and bony vertebrates. (AncGR1.0 and AncGR1.1 are different reconstructions of node AncGR1, inferred from datasets with different taxon sampling.) Black, high sensitivity receptors; gray, low sensitivity receptors. Single and double gray dashes mark functional shifts towards reduced sensitivity and increased specificity, respectively. Support values are the chi-square statistic (1 – p, where p equals the estimated probability that a node could occur by chance alone) calculated from approximate likelihood ratios. The length of branches from AncCR to AncMR1 and to AncGR1, expressed as the mean number of substitutions per site, are indicated in parentheses.

The MRs are similar in function to the AncCR, so they aren’t particularly interesting in this context — there’s no big question about how the MRs retained similar properties to their ancestor. The interesting questions are all about the GRs: what changed to make GRs different from the ancestral protein? What amino acid changes set AncGR1 apart from AncCR?

The investigators have an answer. The first step was the evolution of reduced hormone sensitivity, so that these receptors only responded to very high concentrations of the hormone, and the second step was a loss of sensitivity to the mineralocorticoids, already handled by the MRs, so that they only respond to high doses of cortisol, which at this point became exclusively a stress hormone. And they know exactly which amino acids changed to confer the reduced sensitivity.

They identified three changes: the conversion of a valine at position 43 into an alanine, called V43A; the conversion of an arginine at position 116 into a histidine, R116H; and the conversion of a cysteine at position 71 into a serine, C71S. They also know the effect of the mutations. V43A and R116H each loosen the structure of the receptor so that it’s less sensitive, and when both mutations are present the effect greatly reduces sensitivity about 10,000-fold…too much! They make the mutant hormone too insensitive, and much less insensitive than their reconstructed AncGR1.

The most interesting change is C71S. It basically does nothing to the sensitivity; make the C71S change to AncCR, and you get a receptor protein that is essentially indistinguishable in its response. This is effectively a neutral mutation. It can spread freely through a population with no deleterious or advantageous effect.

C71S does have one significant effect in cooperation with the other two mutations: it buffers both V43A and R116H. When all three mutations are present, the desensitizing effects of V43A and R116H are reduced to produce the level of sensitivity expected for the AncGR1 protein. This means we can reconstruct the order of the amino acid changes in evolution. First came C71S, because it doesn’t cause any particular adaptive change, and because if either V43A or R116H came first, the resulting receptor would be generally non-functional. The existence of C71S first means the subsequent V43A/R116H changes produced receptors that are still functional, but simply operate only at higher concentrations of the hormones.

All of these changes are perfectly compatible with an evolutionary model of their origin. No sudden leaps, no deleterious intermediates are required — everything hangs together beautifully and is backed up by solid empirical evidence. In addition, the work explains the mechanics of receptor-hormone interactions, stuff I haven’t explained here, but if you’re a biochemist, there’s much to savor in the paper.

It’s an amazing contrast to the Gauger and Axe paper, too. No wonder I’m not a creationist!

Carroll SM, Ortlund EA, Thornton JW (2011) Mechanisms for the evolution of a derived function in the ancestral glucocorticoid receptor. PLoS Genet.7(6):e1002117. Epub 2011 Jun 16.

I wish I could go

It’s a conference, in Oregon, and it’s about The Future of Evo-Devo, all wonderful things, and it’s on 10-12 February — right in the thick of the traditional Darwin Day hoopla, the days when I’m like a big egg-laying bunny at Easter. I’m already booked for Pullman, Washington, then Florida, then Las Vegas in that week.

You’ll just have to go in my place and report back. Yes, you — the one looking around quizzically and wondering “why me?” Because I said so. Book it now. Portland, 10 February, the Nines Hotel.

Coincidentally, I’m giving a talk at UNLV that is kind of about the future of evo-devo: I’m going to be both pessimistic and optimistic, and talk about the mainstreaming of evo-devo into the discourse of evolution and development, and propose that it isn’t so much a revolution in evolution as it is developmental biologists finally adopting views much more copacetic with standard model evolutionary thinking. There may be a lynching afterwards.

(Also on FtB)

Urge to kill…fading…fading…fading

Steven Pinker has a new book coming out next week, and I’m very much looking forward to it. It is titled The Better Angels Of Our Nature: How Violence Has Declined, and its premise is that humans have been becoming increasingly less violent over time. I’m very sympathetic to this view: I think cooperation, not conflict, has been the hallmark of human evolution.

There’s an overview of Pinker’s argument at Edge.

Believe it or not–and I know most people do not–violence has been in decline over long stretches of time, and we may be living in the most peaceful time in our species’ existence. The decline of violence, to be sure, has not been steady; it has not brought violence down to zero (to put it mildly); and it is not guaranteed to continue. But I hope to convince you that it’s a persistent historical development, visible on scales from millennia to years, from the waging of wars and perpetration of genocides to the spanking of children and the treatment of animals.

It’s full of charts — all kinds of graphs illustrating correlations and changing rates of war fatalities, homicide, slavery, etc. He identifies five causes of violence: exploitation, dominance, revenge, and ideology (I know, that’s four…I guess he left one out). He also identifies four forces that counter violence: the state as a mediator of justice, trade, an expanding circle of empathy, and reason.

I think the final and perhaps the most profound pacifying force is an “escalator of reason.” As literacy, education, and the intensity of public discourse increase, people are encouraged to think more abstractly and more universally, and that will inevitably push in the direction of a reduction of violence. People will be tempted to rise above their parochial vantage point, making it harder to privilege their own interests over others. Reason leads to the replacement of a morality based on tribalism, authority and puritanism with a morality based on fairness and universal rules. And it encourages people to recognize the futility of cycles of violence, and to see violence as a problem to be solved rather than as a contest to be won.

It would be so nice to read a book that’s optimistic about humanity’s future. I’m definitely getting a copy.

(Also on FtB)

Zietsch replies

I criticized the Zietsch and Santilla paper on the female orgasm. Now one of the authors has responded.

One response he makes is that some of the limitations to the study that I pointed out were also explicitly recognized in the paper. This is true; however, my purpose in mentioning them was to highlight the fact that they make it impossible to draw even the tentative conclusions the authors do…which obviously is not something that was done in the paper. Admitting that assessing orgasmic function with self-reports, for instance, is a limitation doesn’t really change the fact that extremely weak evidence was published to support a particular hypothesis.

Another problem I raised is that the comparisons between male and female orgasmic response were inappropriate. They compared the timing of male orgasm to the likelihood of women having an orgasm at all. My objection is two-fold: they are using phenotype as a proxy for a genetic difference, which is problematic in a trait so strongly responsive to an environmental difference, and it treats two parameters, timing and likelihood, as equivalent in men and women. I don’t think these are necessarily directly connected at all. Zietsch’s reply emphasizes that he does think this is a valid comparison.

Indeed, we measured susceptibility to orgasm in response to sexual stimulation (let’s call it ‘orgasmability’) by assessing the likelihood of orgasming during sexual activity in women and the time taken to orgasm during sexual activity in men. That’s because during sex, men tend to reach orgasm faster than women and generally cannot continue once it is reached. Even when women reach orgasm faster than their man, they can generally continue intercourse until he reaches orgasm, sometimes achieving more orgasms. As such, women’s orgasm during sex is time limited – if she doesn’t reach it in relatively quick time, she might not have it at all, whereas men can go until they finish. That’s why we measure likelihood of orgasm in women and time to orgasm in men, consistent with countless other studies and definitions of orgasmic ‘dysfunction’ in men and women in DSM-IV.

How odd. If sexual activity is limited mechanically by the maintenance of the man’s erection, then yes, it would be true that women’s orgasm during sex is time limited. However, given that vaginal intercourse and female orgasm are only weakly connected, isn’t this an unfortunately male-centered perspective? I will confess that personally, if my sexual performance were measured only by time to orgasm, I’d be considered a pathetic lover (admit it, all you guys reading this: it’s true for you too), but somehow my sexual encounters go on considerably longer, to the delight of both participants. Human sexual activity is considerably more complex than wham-bam-thank-you-ma’am, as I’m sure Zietsch knows.

It’s also a self-destructive assumption. Was there ever a time in our evolutionary history when sexual interactions were limited by male time-to-orgasm? I suspect not; caveman/cavewoman sex probably involved a fair amount of courting and cuddling and playing, just as it does nowadays. And if it didn’t — if it really were nothing but 3-to-5 minute intromission and ejaculation sessions — then there was no opportunity for female orgasm to be selected for. So this is really all an irrelevant objection.

Also…extremes in variation in the timing of the male sexual response are considered dysfunctional because they deviate far from a solid norm. A man who takes a half-hour of focused stimulation to achieve orgasm is probably experiencing some real problems. A woman, on the other hand, who takes that long is not that unusual at all; she is not ‘dysfunctional’. She is normal. It’s a problem when your study assumes that a stable, normal, healthy condition in a woman is comparable to a dysfunctional condition in a male.

Now one central explanation I offered was that male orgasmic response was strongly canalized — that is, there had been selection for multiple genetic processes keying on a strong environmental cue, the presence of testosterone, that made the male response much more robust. The byproduct hypothesis postulates that the female orgasmic response uses the same genetic circuitry, but is more weakly expressed because the cue is largely missing. Unfortunately, we seem to be arguing past each other.

Myers makes some other points that suggest that although he read the paper, he didn’t read it very carefully, since he misses its main point. The by-product theory, as described in detail by Lloyd (2005), says that female orgasm is currently (and always has been) maintained by ongoing selection on the male orgasm. Selection can only operate on additive genetic variation, so if the male orgasm has zero heritability (i.e. zero additive genetic variation) as Myers suggests, then there is no selection on it and therefore no indirect selection on female orgasm. (Hidden genetic variation with no phenotypic effects in males but expressed in females, which Myers alludes to, is irrelevant here because it’s invisible to selection, assuming no direct selection on female orgasm). He goes on to talk about males and females sharing orgasm-related circuitry and genetic apparatus (which nobody denies) – but, to be repetitive, selection only acts on genetic variation – for selection on the male orgasm to act on the female orgasm, additive genetic variation in male orgasm needs to correlate with additive genetic variation in female orgasm. If such a correlation exists there would be a correlation between opposite-sex siblings, and that’s what we tested.

Well, male orgasm has almost zero heritability. There is a low frequency of dysfunction that can be selected against. But largely, it’s true, males hit puberty and they’re generally sprouting erections and ejaculating frequently; selection has done its job and given us guys a remarkably reliable physiology in that regard (and I for one say hooray for evolution). We males are so good at that part of sex that it’s unlikely that there is currently much selection going on on our side of the sexual divide to make orgasm more likely, and so you can remove us from the equation right now and for a long time in the past — we’re done, and all the evidence suggests that that part of our evolution was established at least since mammals evolved.

So Zietsch and Santtila went looking for some kind of significant variation in the male population, and found one in the self-reported variation in time to orgasm. Could there be natural genetic variation in that parameter? Sure. But my objection is that it probably is not significant (was selection for sexual performance ever so strong that males who ejaculated in 3 minutes had an advantage over males who took 5 minutes? I doubt it), and that a self-reporting survey on such a charged question would not produce valid results. 35% of their sample reported spending more than 10 minutes in active intercourse before orgasm, which ought to set off alarm bells right there.

But of course, we males are only half the population. There is known variation in the frequency of orgasm in women, Zietsch and Santilla found the same thing in their survey (note again, though, the unreliability of self-reporting), and we could imagine selection working on that variation. Males are done, as I said, with robust testosterone-dependent developmental mechanisms that assemble a reliable orgasm-generating machine, but there could be, for instance, selection for non-testosterone-dependent orgasm pathways in women, since there is variation in the population.

Only there doesn’t seem to be. There doesn’t seem to be a pattern of women who can orgasm 3 minutes after a penis touches their vagina being more reproductively successful than women who take 20 minutes of clitoral stimulation, nor is there any reason to think faster orgasms would make a woman more fertile. That’s the basis of the byproduct theory — a lack of evidence that selection can or does actually operate on the range of variation in the female half of the human population.

The heart of Zietsch and Santilla’s argument above, though, is this weak one, that unreliable self-reported data shows a lack of correlation in time to orgasm in males and frequency of orgasm in their female siblings. I argue that the variation they describe in the males is unreliable;it is also not significant, even if true; and they haven’t shown that the genetic basis of any variation is even relevant to the genetic basis of orgasm frequency in women. While the neural and physiological basis of orgasm may be shared in men and women (that is a foundation of the byproduct theory), the details of the regulation of the expression of the phenotype are also likely to be dependent on different genetic circuitry. I’d argue that there are multiple pathways in development leading to the formation of the orgasm response, and that all of them contribute to the male pattern, but a major contributor, testosterone-dependent development of the brain and reproductive system, is largely absent in women, leading to a greater reliance on auxiliary systems.

If you want to show that the byproduct hypothesis is false, one good way would be to find, for instance, an estrogen-dependent developmental process that contributes to the female orgasm. That’s what I’d like to see: evidence of a parallel pathway that would only be under selection in females. Showing that would at least be evidence of historical selection for activation of orgasm in women.

One more uncomfortable problem that I’m sure was unintentional: A male scientist writing about female physiology has his work criticized by a number of bloggers; he responds to two of the male critics but ignores a female critic. Again, it’s probably just chance, but it’s an omission that doesn’t leave a good impression. I’ll assume it was just because my argument was so much more magisterial by virtue of my entirely non-sexist authority that he had to reply to me.

(Also on FtB)

Why do women have orgasms?

One of my favorite science books ever is Elisabeth Lloyd’s The Case of the Female Orgasm, which does a beautiful job of going case-by-case through postulated adaptive explanations for female orgasms and showing the deficiency of the existing body of work. It’s a beautiful example of the application of rigorous scientific logic; it does not disprove that female orgasms have an adaptive function, but does clearly show that the scientists who have proposed such functions have not done the work necessary to demonstrate that fact, and that some of the explanations are countered by the evidence. Her conclusion was that the likely explanation for the female orgasm was that it wasn’t directly adaptive: women have them because men are selected for having them, and that the women are just along for the happy ride, just as men have nipples because there has been selection for women to have them.

A lot of people detest the book, though. It does rather ruthlessly cut through many adaptive scenarios, and some people just seem to have a bias that if something exists, it must have a purpose. And for some reason, there is an odd preconception that purposeless features are counter to evolution (they aren’t).

Now there’s a new paper out by Zietsch and Santtila that purports to challenge the non-adaptive explanation. It fails. It fails pretty badly, actually. I’ll go further: I thought it was a terrible paper, especially in contrast to the clarity of Lloyd’s work. Here’s the abstract:

The evolutionary basis of human female orgasm has been subject to furious scientific debate, which has recently intensified. Many adaptive explanations have been proposed, invoking functions from pair bonding and mate selection to sucking up sperm, but these have been attacked as being based on flawed logic and/or evidence. The popular alternative theory is that female orgasm is not adaptive and is only evolutionarily maintained as a by-product of ongoing selection on the male orgasm-ejaculation system. This theory has not been adequately tested. We tested one of its central tenets: that selection pressure on the male orgasm is partially transmitted to the female via a positive cross-sex correlation in orgasmic function (susceptibility to orgasm in response to sexual stimulation). Using questionnaire data from over 10 000 Finnish twins and siblings, we found significant genetic variation in both male and female orgasmic function, but no significant correlation between opposite-sex twins and siblings. This suggests that different genetic factors underlie male and female orgasmic function and that selection pressures on male orgasmic function do not act substantively on female orgasmic function. These results challenge the by-product theory of female orgasm.

So their method was to survey twins and siblings about their sexual performance, and an absence of a correlation between different-sex siblings was interpreted to suggest an absence of a shared, heritable property between males and females. The logic of this experiment falls apart at every level.

First, they are relying on self-reporting of a trait that has strong psychological and cultural components, without making any effort to isolate any of the variables that would bias the subjects’ answers. I would be extremely cautious in interpreting the answers, yet the authors are making quantitative assessments of an inferred genetic network on the basis of some very mushy data.

Secondly, and this one drove me up the wall in trying to read this paper, they are comparing men and women…but asking the two sexes completely different questions. How can you even compare the answers? Men were asked, “How fast have you typically ejaculated after the intercourse (vaginal or anal) has commenced?” — a question about speed that assumes a 100% incidence of orgasm, and only considers intercourse. Women were asked, “Over the past four weeks, when you had sexual stimulation or intercourse, how often did you reach orgasm?” — so no constraint on how orgasm was achieved, or how long it took, but they do limit the interval. In order to compare a time to a frequency, the authors crunch the numbers down to a single value they call a measure of orgasmic function in males and females. But this is still bogus: they really are comparing apples and oranges at every step.

It seems to me that the relevant parameter to measure is whether the subject has any capacity to have an orgasm — do they have the physiological machinery to carry out this function? The question of how robustly this property is expressed is a different issue altogether. When you look at their data this way, it looks just as flawed, but with another twist. All of 1.9% of the male subjects reported never achieving orgasm through intercourse; 12% of the female subjects reported “rarely or never” having an orgasm in the last 4 weeks. This is actually a surprisingly good number; worldwide frequency of anorgasmia in women is typically around 20%, but the sample the authors are taking their data from is fairly homogeneous, consisting of Finns between 18 and 49. Again, though, the results highlight the cultural variability: the female response seems to be much more sensitive to environmental conditions, while the male response is strongly canalized. You can’t assess orgasm in women without taking a whole battery of social issues into account, while men are easy. The orgasmic response in men is locked in as a response to testosterone levels, which are reliably high in most men, while the same response in women relies on other, probably diverse, developmental cues to be switched on.

The situation is that when you examine orgasm in men, you find a heritability that’s near zero — what that means is that there are almost no phenotypic differences in the population that can be accounted for by genetic variation. There could be hidden variation that is swamped out by a robust environmental effect (like testosterone!), but you can’t measure it. One interesting way to look at women, though, is they have the same genetic variations as men, but those variations are unmasked and exposed phenotypically by the absence of the canalizing effect of testosterone, and that’s one mildly suggestive result of this paper — they found a correlation in the frequency of orgasmic response in monozygotic female twins that was stronger than that between dizygotic female twins. Similarly, they found a correlation in the rapidity of orgasmic response between male monozygotic twins, which suggests there could be some genetic component there, as well.

But you can’t compare the male and female measures! They’re different things! Men and women could be sharing the very same genetic circuitry behind orgasm, supporting the by-product hypothesis, but the different endocrine regimes of male and female embryos could be activating entirely different auxiliary genetic circuitry that contributes to the response. In fact, I’d consider it extremely unlikely that female orgasm doesn’t use exactly the same genetic apparatus as male orgasm. If anyone wants to really show that the byproduct hypothesis is false, a demonstration that the female orgasm is produced by pathways that are independent of, and evolved in parallel to, the male machinery would be more than sufficient. A study that is built around subjective reporting of the experience of orgasm isn’t going to do it, though.

A few other sites have looked at this paper.

Greg Laden has more on the behavioral biology of primates, but I’m afraid he doesn’t really get the byproduct theory at all — he keeps talking about the adaptive value of female orgasm, but they’re all post-hoc rationalizations. That culture adapts to the existence of female orgasms does not imply that female orgasms evolved as an adaptive phenomenon. I can show that orgasms make women happy; the question is, does the happiness of women contribute to the evolutionary success of the species? And I’m sorry, evolution doesn’t care.

Scicurious rightly concludes that the paper does not demonstrate what the authors claim it does, but I get the impression that she hasn’t read Lloyd — she has a brief summary of the adaptive alternatives that is fairly casual. Really, Lloyd demolishes them all. She doesn’t necessarily prove that they’re wrong, nor does she claim to do so, but she does show that most of the hypotheses are little more than wishful thinking.

Zietsch B, Santtila P (2011). Genetic analysis of orgasmic function in twins and siblings does not support the by-product theory of female orgasm Animal Behaviour DOI: 10.1016/j.anbehav.2011.08.002

(Also on FtB)

Freebie!

As Jerry Coyne has alerted us, there is a free evolutionary biology textbook available on Kindle — grab it while you can (if you don’t have a kindle, just put the free Kindle app on your computer).

I haven’t had a chance to look the book over myself. Eugene Koonin is a respected name, but books that claim to establish a “Fundamentally New Evolutionary Synthesis” put me off a bit. Other stuff in the summary sounds interesting, though, just downplay the grandiose claims a bit when reading it.

(Also on FtB)

Not like a worm?

Ann Coulter is back to whining about evolution again, and this week she focuses on fossils. It’s boring predictable stuff: there are no transitional fossils, she says.

We also ought to find a colossal number of transitional organisms in the fossil record – for example, a squirrel on its way to becoming a bat, or a bear becoming a whale. (Those are actual Darwinian claims.)

Darwin postulated that whales could have evolved from bears, but he was wrong…as we now know because we found a lot of transitional fossils in whale evolution. Carl Zimmer has a summary of recent discoveries, and I wrote up a bit about the molecular genetics of whale evolution. Whales have become one of the best examples of macroevolutionary transitions in the fossil record, all in roughly the last 30 years — which gives us a minimal estimate of how out of date Ann Coulter’s sources are.

But then she writes this, which is not only wrong, but self-refuting.

To explain away the explosion of plants and animals during the Cambrian Period more than 500 million years ago, Darwiniacs asserted – without evidence – that there must have been soft-bodied creatures evolving like mad before then, but left no fossil record because of their squishy little microscopic bodies.

Then in 1984, “the dog ate our fossils” excuse collapsed, too. In a discovery the New York Times called “among the most spectacular in this century,” Chinese paleontologists discovered fossils just preceding the Cambrian era.

Despite being soft-bodied microscopic creatures – precisely the sort of animal the evolution cult claimed wouldn’t fossilize and therefore deprived them of crucial evidence – it turned out fossilization was not merely possible in the pre-Cambrian era, but positively ideal.

And yet the only thing paleontologists found there were a few worms. For 3 billion years, nothing but bacteria and worms, and then suddenly nearly all the phyla of animal life appeared within a narrow band of 5 million to 10 million years.

It’s so weird to read that: yes, people have been predicting that the precursors to the Cambrian fauna would have been small and soft-bodied (what else would you expect), and that they would be difficult to fossilize…but not impossible, and further, scientists have been out finding these fossils. Somehow this is a refutation of evolution? What we’re seeing is exactly what evolution predicted!

What we have is a good record of small shelly fossils and trace fossils from the pre-Cambrian — before there were fully armored trilobites, there were arthropod-like creatures with partial armor that decayed into scattered small fragments of shell after death, and before that there were entirely soft-bodied, unarmored creatures that left only trackways and burrows. Even in this period Coulter wants to call abrupt, we find evidence of gradual transitions in animal forms.

And then to claim that there is an absence of transitional forms because all that was found were worms! Um, if you take an animal with an armored exoskeleton or bones, and you catch it before the hard skeleton had evolved, exactly what do you think it would look like? Like a worm.

As evolution predicted. As the evidence shows.

I can’t even guess what Ann Coulter was expecting a pre-Cambrian animal to look like. Not like a worm, apparently…but like what?

(Also on FtB)