Many genes, but two major roads to adaptation

In the course of adaptive evolution — evolutionary change via natural selection — gene variants that increase the odds of survival and reproduction become more common in a population as a whole. When we’re only talking about a single gene variant with a strong beneficial effect, that makes for a pretty simple picture: the beneficial variant becomes more and more common with each generation, until everyone in the population carries it, and it’s “fixed.” But when many genes are involved in adaptation, the picture isn’t so simple.

This is because the more genes there are contributing to a trait, the more the trait behaves like a quantitative, not a Mendelian, feature. That is, instead of being a simple question of whether or not an individual has the more useful variant, or allele, at a single gene — like a light switch turned on or off — it becomes possible to add up to the same trait value with different combinations of variants at completely different genes. As a result, advantageous alleles may never become completely fixed in the course of an adaptive evolutionary response to, say, changing environmental conditions.

That principle is uniquely well illustrated by a paper published in the most recent issue of Molecular Ecology, which pairs classic experimental evolution of the fruitfly Drosophila melanogaster with modern high-throughput sequencing to directly observe changes in gene variant frequencies during the course of adaptive evolution. It clearly demonstrates that when many genes contribute to adaptation, fixation is no longer inevitable, or even necessary.

Turning up the heat, homogenizing flies

The authors of the new study, a team from the Institut für Populationsgenetik led by Pablo Orozco-terWengel, conducted what would otherwise be a rather simple experiment in evolutionary change in the laboratory. Starting with fruitflies collected from a wild population in Portugal (yes, Virginia, Drosophila melanogaster has wild populations!) they established three replicate populations of about 1,000 flies, which they put in temperature-controlled conditions somewhat warmer than the original collection location, and allowed them to propagate for 37 generations. Exensive previous work with Drosophila has established that simply moving the flies into a laboratory setting — where they live in bottles, and eat prepared food — exerts natural selection on them, and the increased temperature added a little bit more novelty to the lab environment to make it more likely adaptation would occur.

This experiment is different from all that previous experimental evolution of Drosophila, though, is that the coauthors tracked allele frequencies at thousands of markers during the course of those 37 generations of adaptation to the lab. To do this efficiently, they used an approach called “pooled sequencing.”

The principle behind pooled sequencing is that, if all you care about is the relative frequency of a gene variant in a whole population, you don’t need to know the genotype of any specific individual in that population. So to track changes in allele frequency, the team sampled hundreds of flies from the experimental population, and ground them all up together. (The polite, technical term used here is “homogenized.”) They then extracted DNA from this “pooled” sample, and used a high-throughput sequencer to collect millions of reads — short snippets of DNA sequence — out of the pool as a whole.

To extract allele frequencies from all of those sequence reads, the team identified where each read matched the Drosophila melanogaster reference genome. When multiple reads matched to the same location, but differed in one or more DNA nucleotide bases, they identified those bases as variable markers — single-nucleotide polymorphisms, or SNPs. Because the original DNA sample was pooled from many mashed-together flies, the relative frequency of each different variant of a SNP in the Illumina output should reflect the relative frequency of that SNP variant in the population as a whole.

Using this approach, Orozco-terWengel et al. could track allele frequency changes across more than a million SNP markers by taking these pooled samples from the intial population of flies, then at multiple points during the 37-generation evolutionary experiment. By comparing the allele frequencies in samples taken during the course of adaptation to the allele frequencies in the sample from the starting population, they could identify SNPs that became more common as the population adapted — and, because they had a big sample from across the genome, they could identify those SNPs whose allele frequencies had changed more than would be expected due to genetic drift. They examined samples taken after 15 and 27 generations of evolution, and at the end of the 37-generation experiment.


Is epigenetics totally gay?

In the light of much of what we know about evolution, human homosexuality doesn’t make a lot of sense. Available data suggests that sexual orientation has some inborn, probably genetic, basis. But it’s hard to reconcile that with the fact that gay men and lesbians aren’t, by definition, particularly interested in doing what it takes to pass on any genes that might have contributed to creating their orientation. Natural selection is, all things being equal, pretty good at eliminating genes that make people less likely to make babies.

I’m gay. I’m also an evolutionary biologist. You could say this particular puzzle is tailor-made to attract my interest.

It turns out that there are a number of ways that human populations might accommodate gene variants for same-sex attraction without suspending the rules of natural selection. But it’s also possible that human sexual orientation has a biological basis without being genetic. Natural selection can’t do anything about a trait if variation in that trait isn’t linked to variation at the genetic level. So I was immediately interested by the recent announcement that a team of biologists at NIMBioS, the National Institute for Mathematical and Biological Synthesis, had found that human homosexuality is due not to genetics, but to epigenetics.

However, as soon as I secured a copy of the study itself (available in PDF format here), I was disappointed to find out that the reports of a solution to this particular evolutionary enigma are somewhat exaggerated. The paper doesn’t present any new data that directly links a specific developmental process to human sexual orientation — it’s a review article, gathering existing results in support of a hypothesis that isn’t, at its most basic level, entirely new. But it’s not the job of a review article to present new data; reviews are supposed to gather up what is already known on a topic and identify what new research could do to better answer the questions that remain. And that’s exactly what the new study does.

The paper’s authors are William R. Rice, Urban Friberg, and Sergey Gavrilets — all are evolutionary geneticists who don’t particularly specialize on humans, and Gavrilets especially is best known (to me, anyway) as a theoretician, testing hypotheses using mathematical models and computer simulations. Gavrilets and Rice have previously published one of the most thorough theoretical analyses [PDF] of how gene variants that promote homosexuality might remain in human populations in spite of their selective downside, so they have some established expertise on this topic. In the new paper with Friberg, they introduce a new factor, as mentioned above: epigenetics.

A role for epigenetics

Epigenetics refers to a class of chemical changes to the packaging of DNA that can alter how the genetic code is translated and expressed in visible traits, but without changing genetic code itself. Epigenetic markers, or epi-marks, can attach to the genetic code to “turn off” genes, or make them more active, or change their responses to the activity of other genes. You could think of epi-marks as annotations to the genetic code, like notes in the margins of a book that help a reader remember what passages to return to, or how different parts of the text connect to each other. The prefix epi means “above” or “upon,” so epigentics is a code “upon” the genetic code. Here, I’ll give you a thematically appropriate illustration:

The epigenetic mark-up of the genome is erased and reset very early in development — when an embryo is still a small cluster of cells, not yet implanted in the wall of the uterus. But — and this is the intriguing part — that early epi-mark erasure isn’t perfect. Epi-marks that escape erasure can be passed from parent to offspring, like marginal notes on a photocopied page.

There isn’t any direct evidence that epigenetic markers play a role in human sexual developent. But Rice, Friberg, and Gavrilets argue that what we know so far about the process by which an embryo develops male or female traits suggests that some sort of epi-marks play a role.

In humans, as in most mammals, hormones called androgens (testosterone and its relatives) play a big role in the development of sexual characteristics — embryos carrying an X chromosome and a Y chromosome develop testes, which produce androgens to promote development of male genitals and reproductive anatomy, and eventually sexual attraction to women; embryos carrying two X chromosomes develop ovaries instead of testes, have consistently lower androgen levels throughout development, and typically develop female genitalia and anatomy, and attraction to men.

XY embryos produce, and are exposed to, higher concentrations of androgens than XX embryos — but that’s on average. Individually, the low end of the range of androgen concentrations recorded for XY embryos overlaps with the upper limit of the range of androgen concentrations recorded for XX embryos. Yet the number of embryos in that “ambiguous” range of androgen concentrations is greater than would account for the frequency of children born with ambiguous sexual anatomy or same-sex orientations. In other words, the minimum concentration of androgens necessary to develop a XY embryo into a male is too low to interfere with the normal development of a XX embryo into a female. That suggests that the key difference in male and female development isn’t just hormone levels, but how sensitive embryos are to those levels. Think of it this way: if androgen concentrations are like the thermostat in a room, XY embryos are wearing a couple extra layers of clothing — turn up the heat, and the XYs will start sweating well before XXs start to feel too warm.

That extra clothing could very well be epi-marks that either act to make XX embryos less sensitive to androgens, or to make XYs more sensitive, or both. Rice et al. argue that such markers would help to “canalize” sexual development, making the process robust to variation in the environment encountered by the embryo, and that should be advantageous in most cases. Indeed, there are a few studies that have found differences in epi-marks between XX and XY embryos — though none directly connected to sexual development. If there are in fact sex-specific epi-marks that determine sexual development, and these epi-marks are sometimes transmitted from a parent of one sex to an embryo of the opposite sex — well, maybe things get complicated.

If the model fits

So far Rice et al. have established that the available data are at least consistent with some sort of role for epigenetics in developing human sexual anatomy and psychology. But how would this work evolutionarily? Epigenetic markers are part of biological responses to the environment, but at some level they’re still created by genes. So the authors build and analyze a simple mathematical model to see what might happen to a gene variant that acts the way they propose that sexual development epi-marks might, promoting typical development of one sex, but sometimes promoting atypical development of the other sex.

In broad strokes, this model is very similar to one in the paper Gavrilets and Rice published earlier, in which a gene variant promotes greater fitness when carried by a female, but makes her sons more likely to develop same-sex orientation. The takeaway from that model is that it’s quite possible for the benefits to a mother’s fitness conferred by a variant to outweigh the increased possibility that one or more of her sons might be gay.

In the new model, Rice et al. fold in epigenetics by simulating a gene variant that creates sex-dependent epi-marks — such as epi-marks that reduce an embryo’s sensitivity to androgens. The simulated epi-marks increase the fitness of one sex, but has some probability of carrying over to the next generation, where it might interefere with the development of the opposite sex. In the simplest case they consider, such a gene variant would be favored by selection as long as the benefits it confers to one sex are at least four times as great as the risks for the opposite sex — and if the epi-marks are transmitted less than one hundred percent of the time (which is usually the case), that ratio can be smaller. In fact, if the carryover probability is sufficiently small, selection can favor the epi-marking variant even if the cost to one sex exceeds the benefits conferred to the other.

Better than pure genetics?

Epigenetics is an appealing explanation for same-sex attraction because we have, at best, a fuzzy picture of the genetic basis of sexual orientation. Homosexuality definitely “runs in families”. That is, people with gay or lesbian parents, siblings, aunts, or uncles are more likely to be gay or lesbian themselves; and pairs of identical twins, who share pretty much all their genetic code, are more likely to have the same sexual orientation than pairs of fraternal twins, who share only half their genes.

Yet more sophisticated methods to identify specific genes associated with sexual orientation have failed to find any consistent candidates. (Though, as a caveat, the only genetic association study [PDF] I’ve seen suffers from small sample size and considers a very small number of markers by modern standards.) Moreover, while identical twins share sexual orientation more than fraternal twins, they don’t share it with complete fidelity — only about 20% of gay men who are identical twins have twin brothers with the same orientation.

Epi-markers, which are not so much heritable as somewhat sticky, might explain that fuzziness. For a final twist, Rice et al. used an estimate of the frequency of gay men in the general population (about 8%, which seems high to me) and that 20% “concordance” rate for identical twins to calculate the transmission rate for a hypothetical “feminizing” epi-mark that makes men more likely to be gay: about 50%. That seems high, but the authors argue that we don’t yet now enough about the range of epigenetic transmissibility in humans to rule it out as unrealistic.


So what do we take from this new paper? It’s certainly not positive proof that accidential transmission of epi-markers for sexual development causes same-sex orientations. As I said above, this is a review article, doing what reviews are supposed to do — gather existing evidence, make the case for a hypothesis, and point the way toward fruitful directions for new empirical research.

I came away from the paper more convinced that (as I suggested back in that earlier article) that it may be better to think about the evolution of same-sex orientations not in terms of the selective fitness of gay men and lesbians, but in terms of our parents’ fitness. The new epi-mark model by Rice et al. frames things in just those terms — the gene variant it considers improves the fitness of offspring of one sex, but poses some risk to the fitness of offpsring of the other sex.

Under the Rice et al. model, there’s still a role for gene variants that might be affected by natural selection — but gene variants carried by parents, not necessarily offspring. Epigenetics allows parents to shape their offsprings’ traits in a more subtle fashion than direct genetic inheritance, and Rice, Friberg, and Gavrilets make a convincing case that we’ll need to take this into account as we search for the evolutionary origins of human sexuality.


Bermejo-Alvarez, P., Rizos, D., Lonergan, P. & Gutierrez-Adan, a. 2011. Transcriptional sexual dimorphism during preimplantation embryo development and its consequences for developmental competence and adult health and disease. Reproduction 141: 563–70. doi: 10.1530/REP-10-0482

Gavrilets, S. & Rice, W.R. 2006. Genetic models of homosexuality: generating testable predictions. Proceedings of the Royal Society B 273: 3031–8. doi: 10.1098/rspb.2006.3684

Morgan, D.K. & Whitelaw, E. 2008. The case for transgenerational epigenetic inheritance in humans. Mammalian Genome 19: 394–7. doi: 10.1007/s00335-008-9124-y

Mustanski, B.S., Dupree, M.G., Nievergelt, C.M., Bocklandt, S., Schork, N.J. & Hamer, D.H. 2005. A genomewide scan of male sexual orientation. Human Genetics 116: 272–8. doi: 10.1007/s00439-004-1241-4

Ngun, T., Ghahramani, N., Sanchez, F.J., Bocklandt, S. & Vilain, E. 2011. The genetics of sex differences in brain and behavior. Frontiers in Neuroendocrinology 32: 227–246. doi: 10.1016/j.yfrne.2010.10.001

Pillard, R.C. & Bailey, J.M. 1998. Human sexual orientation has a heritable component. Human Biology 70: 347. PMID: 9549243

Rice, W.R. & Friberg, U. 2012. Homosexuality as a consequence of epigenetically canalized sexual development. Quarterly Review of Biology 87: 343–368. doi: 10.1086/668167


One of these moths is not like the other … but does that matter to Joshua trees?

A huge diversity of flowering plants rely on animals to carry pollen from one flower to another, ensuring healthy, more genetically diverse offpsring. These animal-pollinated species are in a somewhat unique position, from an evolutionary perspective: they can become reproductively isolated, and to form new species, as a result of evolutionary or ecological change in an entirely different species.

Evolutionary biologists have had good reason to think that pollinators often play a role in the formation of new plant species since at least the middle of the 20th century, when Verne Grant observed that animal-pollinated plant species are more likely to differ in their floral characteristics than plants that move pollen around via wind. More recently, biologists have gone as far as to dissect the genetic basis of traits that determine which pollinator species are attracted to a flower—and thus, which flowers can trade pollen.

However, while it’s very well established that pollinators can maintain isolation between plant populations, we have much less evidence that interactions with pollinators help to create that isolation in the first place. One likely candidate for such pollinator-mediated speciation is Joshua tree, the iconic plant of the Mojave Desert.

Joshua trees are pollinated by yucca moths, which are unusually focused, as pollinators go. Your average honeybee will blunder around in a flower, scooping up pollen and drinking nectar, and maybe accidentally pollinate the flower in the process. A yucca moth, on the other hand, gathers up a nice, tidy bundle of pollen in specialized mouthparts, carries it to another Joshua tree flower, and deliberately packs it into place. She does that because the fertilized flower provides more than a little nectar for her—she’s laid her eggs inside the fertilized flower, and when they hatch her offspring will eat some of the seeds developing inside it.

That’s pretty cool in its own right. But what’s especially interesting about Joshua trees, from an evolutionary perspective, is that they’re pollinated by two different moth species. And it turns out that the flowers of Joshua trees associated with the different moth species also look pretty different. The most dramatically different feature is in the length of the stylar canal in the pistil, the part of the flower that determines how the moths lay their eggs.

Trees pollinated by the larger moth species tend to have longer styles (the blue circles in the figure above), and trees pollinated by the smaller moth species tend to have shorter styles (the green triangles). Moreover, the rest of the trees structure differs by moth association as well. In the figure above with the two Joshua trees side by side, the tall, tree-like one is typical of the populations pollinated by the large moth; the short, bushy one is what we usually find in populations pollinated by the small moth. And, through most of the Mojave Desert, the moth-tree association is exceptionally tight: except for a narrow contact zone between the two tree types (where that photo was taken), you only find one tree type, and one moth species, in most Joshua tree populations.

All of this strongly suggests that the two types of Joshua tree must be reproductively isolated by their association with different pollinators, right? Well, maybe. Part of my doctoral dissertation work focused testing this question using genetic data, and in the past couple months, my collaborators and I have published two papers reporting the results of that work, and a related study at the contact zone.

Here’s a graph illustrating that second point: in this analysis, we used a clustering algorithm to determine whether the genetics of each tree in our analysis suggested it belonged to one of two possible groups. In the graph, each bar is colored according to the relative probability that a single tree is in each group belongs to each group. The bars are grouped according to the location of the trees they represent, and which moth species is present at each site. As you can see, there are a lot of bars that aren’t clearly one color or the other—and the ambiguous trees they represent aren’t confined to the sites where both moths are present.

So on the one hand, the different pollinators aren’t doing a very good job of isolating the two forms of Joshua tree. But on the other, that result leaves the very interesting question of why there are two types of Joshua tree at all. An obvious hypothesis is that the two different pollinators are exerting divergent natural selection on the trees they pollinate—and my collaborator Chris Smith will be presenting data to test that hypothesis in the not-too-distant future.


Schemske D.W. & Bradshaw H.D. (1999). Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proceedings of the National Academy of Sciences, 96 (21) 11910-11915. DOI: 10.1073/pnas.96.21.11910

Grant V. (1949). Pollination systems as isolating mechanisms in angiosperms. Evolution, 3 (1) 82. DOI: 10.2307/2405454

Starr T.N., Gadek K.E., Yoder J.B., Flatz R. & Smith C.I. (2013). Asymmetric hybridization and gene flow between Joshua trees (Agavaceae: Yucca brevifolia) reflect differences in pollinator host specificity. Molecular Ecology, 22 (2) 437-449. DOI: 10.1111/mec.12124

Yoder J.B., Smith C.I., Rowley D.J., Flatz R., Godsoe W., Drummond C. & Pellmyr O. (2013). Effects of gene flow on phenotype matching between two varieties of Joshua tree (Yucca brevifolia; Agavaceae) and their pollinators. Journal of Evolutionary Biology. DOI: 10.1111/jeb.12134


We’re not missing the penis bone, we just lost it

What’s that, you say? Baculum is the technical term for the penis bone. Many mammals have one – presumably to aid in sexual intercourse. For mammals that mate infrequently, prolonged intercourse ups the chances that a particular male sires some babies. For mammals that must mate quickly, the baculum provides immediate rigidity. And for all mammals, keeping the urethra straight while copulating is imperative, so maybe it’s there to prevent a kink in the works, so to speak. The truth is, there are a lot of hypotheses about what bacula do but – as you might imagine – they’re kind of difficult to test. Regardless, our nearest evolutionary neighbors, the great apes, all have bacula, as do most other primates. Gilbert and Zevit cite this– the fact that our baculum is missing – as evidence for their argument. Which goes like this:

  1. A rib seems like an unlikely origin for Eve because male and female humans have the same number of ribs.
  2. Ribs also lack “intrinsic generative capacity”, which penises have “in practice, in mythology, and in the popular imagination”.
  3. Most mammals – and especially primates – have bacula, humans do not.
  4. It is therefore “probable” that Adam’s baculum was removed to make Eve, and not a rib.

The authors then continue to support their argument with alternate translations of the Hebrew word for “rib” (which they say could mean “support beam”) and claim the raphe of the human male scrotum is what Genesis 2:21 is referring to when it says “The Lord God closed up the flesh.”** I’m almost convinced!

Almost. Lots of evolutionary innovation occurs through gaining functions, but losing functions (or appendages) also happens. Humans are different from the other great apes in a lot of ways – did you know we’re the only ones with chins? Just because we’re related but lack an otherwise common trait doesn’t mean God took it from us. It’s also interesting to note that some species – like the walrus – have gigantic bacula (like 22 inches gigantic and the largest fossilized baculum from an extinct walrus species comes in at 4 feet). Great apes have much, much smaller bacula – and the closer they are to us, the smaller it is (Figure 1).

Why do humans lack a baculum? Well, there are several theories. Richard Dawkins has hypothesized that sexual selection is responsible, as erectile function may be an honest signal of a potential mate’s health***. Perhaps our mating system – which allows for more and shorter copulations instead of infrequent and longer copulations – made them costly and useless enough to be selected against. Or maybe the bacula serve no purpose – they’re vestigial in great apes. There is a lot of speculation about the “missing” human baculum on the internet and scientific literature – I’m almost embarrassed to be adding to the load – but the point here is that this argument is an odd mix of science and creationism and the end result is a story that makes less sense than if the authors had stuck to one or the other. They invoke phylogenetic concepts to justify their religious opinion – basically, they’re saying “Our nearest evolutionary relatives have bacula (as do most members of our clade Mammalia), so if we don’t have one, God must have taken it – to produce female human beings.”

That last clause there – the part where it creates the second gender, is the part I get least when I consider the distribution of bacula across the animal kingdom. I know humans are special but still – why do some animals have bacula at all? I’m trying to not be disrespectful and snarky – but seriously, this argument is inconsistent with the natural world. Bacula ossify by a different mechanism than, say, your femur – it’s not part of the main skeletal system. This may allow it to be more easily lost and/or gained through time and could help explain why we (and spider monkeys and whales and hyenas and ungulates) aren’t really “missing” it, we just lost it.


The gold-star creationist?

The Life Sciences building at the University of Idaho. Photo by jby.

Academic freedom is a bedrock principle of higher education—part of the point of having classes taught by working scholars is that, at the university level, students should be exposed to the interplay of ideas at the cutting edge of each field of study, and so professors should have latitude to explore controversial topics and defend their own perspectives. 

But there are limits to that principle. Common sense, and the need to organize prerequisites across a multi-year curriculum, dictates that even a tenured professor would get into trouble if she devoted her entire introductory chemistry course to a critical reading of The Lord of the Rings. In a (maybe) less extreme example, a professor who spent an astronomy class arguing that there is a scientific basis to the Zodiac would, at the very least, get a talking-to from his department chair. In order to meaningfully teach a given class, there are topics that need to be covered—and there is material that has no legitimate place in the syllabus.

This is why I was so surprised to learn, a few weeks ago, that the University of Idaho—the institution where I earned my Ph.D., where Noah earned his Master’s degree and Sarah earned both her B.S. and Master’s—has hired someone who believes that the Earth was created over the course of six days about six thousand years ago, to teach an introductory microbiology course.

The course in question is MMBB 154, “Introductory Microbiology,” and the young-Earth creationist in question is Gordon Wilson. Wilson is notorious, among biologists at the U of I, as the “senior fellow of natural history” at New Saint Andrews College, a small, extremely conservative Christian institution located in downtown Moscow, Idaho, just a few blocks from the University campus. 

Wilson is very much on the record in believing that life on Earth was created by direct divine intervention, according to a take-the-text-at-face-value reading of English translations of the first chapter of Genesis. For a sample of the mental gymnastics involved in creationist “science,” look no further than Wilson’s contribution [PDF] to a 2004 conference, in which he posits that God created every living thing with extra “gene sets” for carnivory, venom, pathogenicity, and other “natural evils,” which were, metaphorically, stored under glass to be activated by the Deity in the event of human malfeasance. Maybe more worryingly, Wilson has described [PDF] the conflict between his theology and empirical fact in terms of religious persecution:

God-fearing or Darwin-questioning scientists employed by the state are now in danger of persecution if they allow their religious views or doubts about Darwin to affect their scientific research and/or classroom discussion.

Can someone with those views teach a basic biology course at a public university? 

The National Academy of Sciences describes evolution as the “central unifying theme of biology,” and the American Society of Microbiologists has formally stated that “It is important that society and future generations recognize the legitimacy of testable, verified, fact-based learning about the origins and diversity of life.” You simply can’t have a comprehensive introductory biology (or microbiology) course without covering evolution, and describing it as the extensively verified empirical fact that it is.

Then, of course, there’s the fact that young-Earth creationism is an unambiguously religious position, a doctrine held by a particular subset of Christians—Wilson himself criticizes the “Intelligent Design” movement for “Avoiding the word ‘God’ in their rhetoric.” And advocating for the views of particular religious sect in the capacity of an employee at a public university is a clear-cut violation of the First Amendment of the U.S. Constitution.

All together, that sounds like a pretty straightforward “no.”

But this isn’t the first time the U of I took a chance on Gordon Wilson. The colleague at Idaho who alerted me to Wilson’s new teaching job (whose identity I’ll choose not to disclose) noted that Wilson was hired once before, years ago, on a one-semester gig to teach the same course. I haven’t been able to confirm any description of how he taught the first time around. Then, as now, the task of finding a lecturer to cover the course was probably hampered by the fact that there aren’t a lot of microbiologists willing to move to a small town in northern Idaho for a one-semester “Temporary Lecturer” position—so that, even though the job description [Edit, 18 March 2014: Looks like this page is no longer up even as a Google cache. Fortunately I saved a copy.] calls for a graduate degree in microbiology that Gordon Wilson doesn’t have, the hiring committee may not have had any alternative candidates.

Can a creationist teaching biology at a public university keep his beliefs out of the classroom?

But so maybe Wilson did an acceptable job, that last time around. The ASM statement on the importance of evolution also says, “A fundamental aspect of the practice of science is to separate one’s personal beliefs from the pursuit of understanding of the natural world.” I can, at least in principle, imagine a creationist professor who taught the contents of a microbiology curriculum, complete with the common descent of life on Earth, and never breathed a word of his personal beliefs in the classroom. Could Gordon Wilson—of all people—be that “gold-star” creationist?

I decided the only way to answer that question was to ask Gordon Wilson.

I e-mailed Wilson last week, at his University of Idaho address. I gave him a sketch of my thinking for this article, and asked what he planned to teach about the origins and relationships among the diversity of life on Earth, and about his previous experience teaching Introductory Microbiology at U of I. Wilson wrote back promptly to say that he’d need a few days to respond to my questions in full (he is, after all, midway through teaching a big introductory biology course!) but he noted right away:

I made it clear 9 years ago and this semester that I wasn’t going to promote my views or disparage evolutionary views in class. That said, I have stated that I do not share the views of common descent held by the main stream scientific community. Which is well with in my rights to do. The only thing that I have presented (briefly) is a distinction between historical science and empirical science, and that conclusions drawn from the former don’t have the high level of certainty as conclusions drawn from the latter. This distinction is not a creationist invention. Ernst Mayr holds to this as well. The conclusions drawn from historical science are as good as the presuppositions on which they are based. This was simply a moment to encourage students to exercise some critical thinking skills in assessing truth claims of the scientific community.

In spite of Wilson’s assurance that he wouldn’t “disparage evolutionary views,” that’s not exactly an encouraging answer. The separation between “historical” science and “empirical” science he mentions here is a classic Creationist tactic—boiling down to “we weren’t there, so how can we know except via ancient texts?”—which doesn’t begin to accurately reflect how the overwhelming majority of scientists weigh different forms of evidence. (Readers may recall that this came up in Bill Nye’s recent debate with Ken Ham.)

I wrote back,

Thanks, Gordon. I do appreciate the time pressures of teaching a big mid-semester class, and I’m glad you’re willing to provide some answers. With regard to your response … that gets, I think, at exactly the tension I’m hoping to explore in the article. I certainly do think that you, personally, have the right to come to whatever conclusion you care to about the common descent of life on Earth—but it is one thing to hold a personal belief, and quite another to teach it with the authority of a university lecturer.

To which Wilson replied,

You’re very welcome, Jeremy. 

By the way, I’m not teaching my personal beliefs; I am simply going on record as not holding to the consensus viewpoint. I don’t teach why I don’t hold to the consensus view. Why is that not OK? Is it because the scientific academy doesn’t want undergraduates to know that there are scientists that have non-religious reasons for dissenting from Darwinism?

Taking a word of advice from a recent NiB contribution, I elected not to respond to this; several days later, on the date I’d set as a deadline for his answers, Wilson e-mailed to say that he simply didn’t have time to provide any further response.

The evidence I have, short of attending every “Introduction to Microbiology” lecture, is incomplete. But what I do know is not at all encouraging. Wilson’s public record pretty clearly shows that he considers it his sacred duty to oppose sound scientific reasoning in any venue possible. And in his brief correspondence with me, he admits to using a creationist rhetorical trick in class—and indicates that he can’t (or won’t) “separate [his] personal beliefs from the pursuit of understanding of the natural world.” 

No gold star for Gordon Wilson, then—and here’s hoping this semester will be the last one he spends teaching anybiology course at my alma mater.

Considering the subject matter of this post, we’re going to keep a particularly tight rein on the comments. Keep it polite, and on-topic, if you please.


In flour beetles, coevolution mixes things up

When evolutionary biologists think about sex, we often think of parasites, too. That’s not because we’re paranoid about sexually transmitted infections—though I’d like to think that biologists are more rigorous users of safer sex practices than the general population. It’s because coevolution with parasites is thought to be a major evolutionary reason for sexual reproduction.

This is the Red Queen hypothesis, named for the character in Lewis Carroll’s Through the Looking Glass who declares that “it takes all the running you can do to keep in the same place.” Parasite populations are constantly evolving new ways to infest and infect their hosts, the thinking goes. This means that a host individual who mixes her genes with another member of her species is more likely to give birth to offspring that carry new combinations of anti-parasite genes.

But although sex is the, er, sexiest prediction of the Red Queen, it’s not the whole story. What matters to the Red Queen is mixing up genetic material—and there’s more to that than the act of making the beast with two genomes. For instance, in the course of meiosis, the process by which sex cells are formed, chromosomes carrying different alleles for the same genes can “cross over,” breaking up and re-assembling new combinations of those genes. Recombination like this can re-mix the genes of species that reproduce mostly without sex; and the Red Queen implies that coevolution should favor higher rates of recombination even in sexual species.

That’s the case for the red flour beetle, the subject of a study just released online by the open-access journal BMC Evolutionary Biology. In an coevolutionary experiment that pits this worldwide household pest against deadly parasites, the authors show that parasites prompt higher rates of recombination in the beetles, just as the Red Queen predicts.

The red flour beetle, Tribolium castanaeum, is named for its predilection for stored grain products. This food preference makes the tiny beetles particularly easy to raise in the lab, where they’ve been useful enough as a study organism to rate a genome project, which was completed in 2008.

Tribolium castanaeum reproduces strictly sexually. But, like any other biological trait or process, the beetle’s rate of recombination can vary, and evolve. And, as I’ve explained above, the Red Queen suggests that selection by parasites should favor higher rates of recombination. So the authors of the new study set experimental populations of the beetle to evolve either in parasite-free habitats, or under attack by Nosema whitei, a protozoan that infects and kills flour beetle larvae. 

The team started experimental populations of beetles (fed on organic flour, natch) in each of the two treatments with eight different genetic lines, maintaining them at a constant population by collecting 500 beetles at the end of each generation to start the next generation. To make the coevolution treatment coevolutionary, the authors also transferred spores of the parasite produced in the previous generation to infect each new generation of beetles.

After 11 generations of coevolution, the authors sampled male beetles from four of the experimental populations in each treatment, and mated them with females from the same genetic line. By collecting the genotypes of the sampled males for a small number of strategically chosen genes, and comparing them to the genotypes of the males’ offspring, it was then possible to identify recombination events—offspring who had combinations of alleles at different genes that weren’t seen in their fathers.

And, indeed, the frequency of recombination—the proportion of offspring whose genetics showed signs of recombination events when compared to their fathers—was greater in the experimental lines that coevolved with Nosema whitei

That’s a fairly remarkable result for a simple, relatively short selection experiment, and to my knowledge it’s the first of its kind to deal with recombination, as opposed to sex. There are a few study systems in which natural populations show signs of coping with parasites by having more sex, including C.J.’s favorite mollusks, and there is one good experimental example in which the worm Caenorhabditis elegans evolved to reproduce sexually when confronted with bacterial parasites. But this study marks a new bit of empirical support for the Red Queen: coevolution acting to boost the gene-mixing benefits of sex. 


Kerstes, N., Berenos, C., Schmid-Hempel, P., & Wegner, K. (2012). Antagonistic experimental coevolution with a parasite increases host recombination frequency BMC Evolutionary Biology, 12 (1) DOI: 10.1186/1471-2148-12-18

Morran, L., Schmidt, O., Gelarden, I., Parrish, R., & Lively, C. (2011). Running with the Red Queen: Host-parasite coevolution selects for biparental sex. Science, 333 (6039), 216-218 DOI: 10.1126/science.1206360


The beef I have with The Paleo Diet

I’ve heard a lot about “The Paleo Diet” lately and every time a popular news source (say NPR or ABC or Fox News or New York Times) does a piece, I cringe a little bit. For those of you who have never heard of the Paleo Diet (from Wikipedia):

The paleolithic diet…is a modern nutritional plan based on the presumed ancient diet of wild plants and animals that various hominid species habitually consumed during the Paleolithic era—a period of about 2.5 million years duration that ended around 10,000 years ago with the development of agriculture.

So that’s the basic idea – people restricting their diet to things that we ate before modern agriculture. I don’t really have a problem with the diet, per se – removing highly processed foods and increasing your activity level is a good idea for almost anyone. But the rationale that always accompanies the diet – that’s where the cringe comes in.
The rationale goes like this (again from Wikipedia):

Paleolithic nutrition is based on the premise that modern humans are genetically adapted to the diet of their Paleolithic ancestors and that human genetics have scarcely changed since the dawn of agriculture, and therefore that an ideal diet for human health and well-being is one that resembles this ancestral diet.

I can break this rationale down into three assumptions/statements:
1. Evolution acts to optimize health.
2. Evolution adapted us to eat a specific diet.
3. Therefore, today, we should eat that diet to optimize our health.

As an evolutionary biologist, I think there are logical and scientific flaws to each of these statements.

1. Evolution acts to optimize health.
FALSE. Evolution acts to optimize fitness (the scientific term for how many babies you leave behind), not health (how physically fit and free from disease we are). The line that connects the modern idea of individual health and evolutionary fitness is not necessarily a straight one. For example, many of the “diseases of affluence” that the Paleo Diet aims to alleviate (obesity, heart disease and adult-onset diabetes) have not been shown to actually and negatively affect human fitness. In fact, there is even some correlational evidence that people we might currently describe as “less healthy” have more children and therefore might have higher fitness. Evolution doesn’t really care about health past the point where you’re healthy enough to make a baby. And if our goal is to achieve a modern ideal of health, recreating the conditions to which our ancestors were putatively adapted may not help us get there.

2. Evolution adapted us to eat a specific diet. 
TRUISM/FALSE. The truism here is that evolution has adapted us to our diet. All living things are the product of evolution; Homo sapiens has evolved to be an omnivore. The Paleo Diet makes a far more specific claim, though: that there is a single, specific diet to which we adapted in the past and that we have not since evolved. First, this assumes that all Paleolithic humans ate the same things in approximately the same proportions. This cannot be correct. Even on small geographic scales, the relative quantities of meat, fish, and vegetable matter available for human consumption change drastically. If I had to hunt/gather on the Louisiana coast for my dinner it would look totally different than if I were doing the same in northern Louisiana. Not to mention that one place would differ on a month-to-month basis. Seasonality and geography dictate what would be available to eat, not our evolution.

Second, this assumes that no evolution has occurred since the advent of agriculture. This is demonstrably false. One example of post-agricultural evolution is the human lactase gene, which breaks down lactose, the dominant sugar in milk. In ancestral humans this gene was turned off after infancy; those humans would have been “lactose-intolerant”. Most humans of European descent now have a mutation that keeps that gene turned on their entire lives. Not surprisingly, this gene spread throughout Europe at approximately the same time cattle were domesticated. There are other known examples of agricultural dietary adaptation, and doubtless more to be discovered. If we are going to use evolution to justify our dietary choices, why throw out the last 10,000 years of it?

3. Therefore, today, we should eat that diet to optimize our health.
HMMMM. Omnivory probably does optimize our health – I think a lot dieticians would recommend eating a variety of fruits, vegetables, grains and meat for an ideal diet. But the Paleo Diet has restrictions on which foods you can eat based on when they were introduced to the human diet AND what we know about them based on modern science (list of Paleo foods here & new link not requiring password here). For example, lean meats good, fatty meats bad. Paleolithic humans probably ate fatty meats every chance they got, don’t you think? Good fat was probably hard to come by in some places. We just think of fatty meat as “bad” because of cholesterol and whatnot – I’d go so far as to say evolution has trained us to love fatty meats, isn’t that why bacon tastes so good?

Here’s the other thing: basically anything you buy in a store probably wasn’t around a million years ago, regardless of how close it seems to being “natural”. Humans might have eaten wild pigs, but modern pigs are a different beast altogether. The same goes for apples or carrots or organic blueberries. Oddly enough, diet soda makes the “Foods to be eaten in moderation” category but “Dairy” is to be avoided entirely. What evolutionary sense does that make?

In summary, humans are certainly a product of their evolutionary history, but ALL of it, not a restricted subset of it. That history can give us great insight into why we are the way we are, and it might be a great way to generate hypotheses about which foods we should eat and in which proportions in order to be healthy. There is, however, a lot of uncertainty about what ancient humans actually ate, and whether that food made them healthy. Furthermore, evolutionary reasoning may explain what things we observe today, but it cannot be used to tell us what we ought to do. That is the realm of modern scientific evidence, not evolutionary first principles.

Now if you’ll excuse me, I believe someone mentioned bacon?

PS – Noah Reid contributed greatly to this post.

PPS – The wikipedia page for the Paleo Diet has a lot of information with a bunch of citations to primary literature on many aspects of the diet; check it out if you’re interested in what the experts have to say.


In flour beetles, coevolution mixes things up

When evolutionary biologists think about sex, we often think of parasites, too. That’s not because we’re paranoid about sexually transmitted infections—though I’d like to think that biologists are more rigorous users of safer sex practices than the general population. It’s because coevolution with parasites is thought to be a major evolutionary reason for sexual reproduction.

This is the Red Queen hypothesis, named for the character in Lewis Carroll’s Through the Looking Glass who declares that “it takes all the running you can do to keep in the same place.” Parasite populations are constantly evolving new ways to infest and infect their hosts, the thinking goes. This means that a host individual who mixes her genes with another member of her species is more likely to give birth to offspring that carry new combinations of anti-parasite genes.

But although sex is the, er, sexiest prediction of the Red Queen, it’s not the whole story. What matters to the Red Queen is mixing up genetic material—and there’s more to that than the act of making the beast with two genomes. For instance, in the course of meiosis, the process by which sex cells are formed, chromosomes carrying different alleles for the same genes can “cross over,” breaking up and re-assembling new combinations of those genes. Recombination like this can re-mix the genes of species that reproduce mostly without sex; and the Red Queen implies that coevolution should favor higher rates of recombination even in sexual species.

That’s the case for the red flour beetle, the subject of a study just released online by the open-access journal BMC Evolutionary Biology. In an coevolutionary experiment that pits this worldwide household pest against deadly parasites, the authors show that parasites prompt higher rates of recombination in the beetles, just as the Red Queen predicts.

The red flour beetle, Tribolium castanaeum, is named for its predilection for stored grain products. This food preference makes the tiny beetles particularly easy to raise in the lab, where they’ve been useful enough as a study organism to rate a genome project, which was completed in 2008.


Kerstes, N., Berenos, C., Schmid-Hempel, P., & Wegner, K. (2012). Antagonistic experimental coevolution with a parasite increases host recombination frequency BMC Evolutionary Biology, 12 (1) DOI: 10.1186/1471-2148-12-18

Morran, L., Schmidt, O., Gelarden, I., Parrish, R., & Lively, C. (2011). Running with the Red Queen: Host-parasite coevolution selects for biparental sex. Science, 333 (6039), 216-218 DOI: 10.1126/science.1206360


How to celebrate Valentine’s Day: A note on the Red Queen and maintaining sexual reproduction

This year’s Valentine’s card of choice

HAPPY VALENTINE’S DAY! As a perpetually single girl this is my favorite holiday of the year. The first and second half of those statements may appear conflicted. However, every year on Valentine’s Day, I send out glorious amounts of Valentine’s to all my single friends (See below for this years!), eat chocolate and drink red wine while ordering myself sexy lingerie on the internet. Yeah, it’s a pretty awesome holiday. This year, one of my favorite evolutionary biologists has upped the excitement by publishing a paper on what conditions favor sex! Perfect for Valentine’s Day!

Why organisms reproduce sexually is one of the great mysteries in evolutionary biology (I’d like to note that here I’m talking about sex in terms of reproduction. It isn’t a mystery to me why organisms copulate, the differences being if that sex comes with offspring while copulation is just good old fashioned fun). There are a number of theoretical reasons that they shouldn’t! One of the strongest arguments was first laid out by John Maynard Smith (1978) who noted that an asexual female can produce twice as many offspring per individual than a sexual female, who wastes half of her effort producing males. This almost immediately results in sexuals being driven to extinction and is termed “the two-fold cost of males.”

There have been a number of different mechanisms of selection that have been proposed to explain sex: host-parasite interactions (Bell 1982), elimination of deleterious alleles (Mueller 1964), and various forms of selection (Charlesworth 1993; Otto and Barton 2001; Roze and Barton 2006). However, none of these alone are able to theoretically overcome the two-fold cost of producing males, so many biologists have started taking a pluralist approach (West et al. 1999; Howard and Lively 1994) and combing one or more of the advantages to being sexual in an effort to understand why the birds do it, the bees do it, and even educated fleas do it.

The theoretical problem with sex

Hodgson and Otto (that’s MacArthur “Genius Grant” recipient Sarah “Sally” Otto) recently published such a model, looking at how directional selection for advantageous alleles and host-parasite coevolutionary interactions could potentially combine to favor sexual reproduction. They specifically looked at host-parasite interactions that are mediated by one allele in the parasite matching or mismatching one allele in the host resulting in infection or no infection. This kind of interaction (referred to as the Matching Allele Model) at equilibrium results in negative frequency dependent selection causing oscillations in both populations, which are called “Red Queen” dynamics.

I mentioned the Red Queen in my last post, so I’ll just touch on it again here. Famed paleontologist Van Valen (1973) noted that organisms tend to continuously evolve to their environment, which is also constantly changing. He noted it was similar to a passage in Lewis Carrol’s Alice in Wonderland, and dubbed this hypothesis The Red Queen. Graham Bell (1982) used the Red Queen to talk about host-parasite interactions, noting that as hosts and parasites are both evolving in response to each other, then the Red Queen should be stronger than other, less changeable environmental factors. The Red Queen has since been used to evaluate conditions under which the negative frequency dependent selection can favor sexual selection in hosts when under strong selection by parasites, both empirically and theoretically.  Unfortunately, theory generally finds that sexual reproduction is only favored by the Red Queen under conditions where selection is unrealistically strong. However, there are a few conditions that, when coupled with the Red Queen, favor sex.

Hodgson and Otto simulated a model in which they considered three different loci in the host population, one that mediates host-parasite interactions, one that directional selection acts on and one that dictates how much recombination occurs (the sex allele). The frequency of this “sex allele” in the population is tracked through time and allows you to look at when sex is favored and when it is driven to extinction. The parasite population have only one locus of interest, which interacts with the host’s interaction locus.

In general the “sex allele” was favored, but it was more strongly favored in simulations where the beneficial allele was strongly beneficial. Moreover, the frequency of the modifier allele changed more slowly when selection on the host-parasite interaction allele was weaker. Finally when both loci were linked, the amount of sex in the population increased the most. The authors conclude that this interaction favors sex in the population because the genetic mixing uncouples the fate of beneficial alleles from those being selected against in host-parasite interactions*.

This result is contrary to previous work, and generates a scenario under which sex can be maintained. Moreover, it fits well with the empirical data. where many host-parasite interactions have been shown to be mediated at a single loci. It’s a very simple solution laid out in an excellent and easily accessible model. What an excellent way to spend your Valentine’s Day, reading about sex!

Now if you’ll excuse me, there are some dark chocolate covered strawberries with my name on them.

* I’d like to take a moment to note that I love Sally Otto’s models. I hope someday I can write models as well formulated and elegant as she does … in every paper she writes.

Literature Cited:

Charlesworth B (1993) Mutation-selection balance and the evolutionary advantage of sex and recombination. Genetic Research Cambridge 61: 205-224.

Hodgson EE and SP Otto (2012) The red queen coupled with directional selection favours the evolution of sex. Journal of Evolutionary Biology doi: 10.111/j.142-=9101.2012.02468.x

Jokela J, Dybdahl MF and CM Lively (2009) The maintenance of sex, clonal dynamics, and host-parasite coevolution in a mixed population of sexual and asexual snails. American Naturalist 174: S43-S53.

Maynard Smith J (1978) The evolution of sex. Cambridge University Press, London.

Muller HJ (1964). The relation of recombination to mutational advance  Mutat Res 106: 2–9.

Otto SP and N Barton (2001) Selection for recombination in small populations. Evolution 55: 1921-1931.

Roze D and N Barton (2006) The Hill-Robertson effect and the evolution of recombination. Journal of Evolutionary Biology 12: 1003-1012.

Van Valen, L (1973) “A new evolutionary law” Evolutionary Theory 1: 1¬30.


Predatory Open-Access Journals?

Last summer, I worked with NESCent and Google’s Summer of Code to write a small piece of software. I think it’s quite useful for the specific thing it does and some researchers in my immediate peer group who have used it agree. I wrote up a short manuscript describing the program and very quickly got it rejected from Molecular Ecology Resources and Bioinformatics. It went on the back burner for several months until I got a solicitation from a new open-access journal that was offering a discounted rate for articles received before a certain date. So I submitted to this journal, after looking up some of their papers and a few people that have published there and convincing myself it wasn’t a flat-out scam.

One day after I submitted, I got an email asking me to review my own article. I know, right? How could that ever happen with a legitimate journal? I declined, they sent it to others to review and about a month later I got three reviews back that were short (0.5 – 1 page), but addressed real questions about my manuscript and included helpful suggestions. I incorporated the changes as best I could and resubmitted. About a week after the resubmission, I saw Beall’s List of Predatory Open-Access Publishers, which includes the aforementioned  journal on the list of “questionable, scholarly open-access publishers”. The author of the list says: I recommend that scholars not do any business with these publishers, including submitting articles, serving as editors or on editorial boards, or advertising with them. Also, articles published in these publishers’ journals should be given extra scrutiny in the process of evaluation for tenure and promotion.

Then, this morning, I got final acceptance of the manuscript and I’m not sure what to do.

I’m not trying to pull one over on anyone and I don’t necessarily disagree with the above text, but I don’t think this paper will be able to go anywhere else and I’m not convinced this journal is Bad. Not a lot of places publish small pieces of discipline-specific software (if you know of any, let me know). I believe this would be a really useful tool for somebiologists and in fact, there are a couple of people waiting to cite the manuscript. I don’t want to encourage predatory journals, but open-access articles that do not-super-important science might actually have a place in our field.

I would LOVE thoughts on this. I certainly don’t view this manuscript as equivalent to a Molecular Ecology or Evolution publication – but do all pubs have to be top (or middle) tier? Is there a solution here, like including impact factors on CVs? Or maybe new fangled software like Google Citations can alleviate this problem since they show the overall publishing record of an individual/article? Please weigh in!