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Research

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.

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Research

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.

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Research

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.

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Research

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. 

References

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

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Research

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?

https://nothinginbiology.org/reduslim/

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.

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Research

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.

References

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

Categories
Research

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.

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Research

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!

https://nothinginbiology.org/

Categories
Research

A guide to the science and pseudoscience of A Troublesome Inheritance, part I: The genetics of human populations

This is the first in a series of guest posts in which Chris Smith will examine the evolutionary claims made in Nicholas Wade’s book A Troublesome Inheritance. Chris is an Associate Professor of Evolutionary Ecology at Willamette University. He uses population genetic approaches to understand coevolution of plants and insects, and he teaches the interdisciplinary course “Race, Racism, and Human Genetics” with Emily Drew.

Last month the former New York Times writer Nicholas Wade released his latest book on human evolution, A Troublesome Inheritance: Genes, Race, and Human History (2014, Penguin Press). In it, Wade argues that the genomic data amassed over the past ten years reveal real and meaningful biological differences between races, and that these differences explain much of the cultural and socioeconomic differences between people. If you haven’t read a newspaper or picked up a magazine in the last month, you may not have noticed that Wade’s book has—predictably—prompted intense and impassioned reaction from scientists, sociologists, and commentators from across the political spectrum. Writing for the Wall Street Journal, Charles A. Murray, author of The Bell Curve, called Wade’s book, “A delight to read … [that] could be the textbook for a semester’s college course on human evolution.” On the other hand, Arthur Allen, in his review for the New York Times, predicts that many readers will find Wade’s book to be, “a rather unconvincing attempt to promote the science of racial difference.”

Writers with considerably more gravitas than I have already pointed out that Wade seems to have a rather poor handle on the literature he reviews. Mike Eisen, professor of Molecular Biology in the Howard Hughes Medical Institute (HHMI) at University of California at Berkeley, writes that, “the book is riddled with scientific and logical flaws” and Wade’s “representation of modern genetics is simplistic and selective.” Likewise, Allen Orr, former president of the Society for the Study of Evolution, in his essay for the New York Review of Books warns that, “[Wade] is not the surest guide to a technical literature.” This is an understatement, to say the least. Indeed, many of Wade’s claims represent significant misunderstandings or misinterpretations of the literature.

Here, I offer the first in what I hope to be a series of posts examining Wade’s scientific claims, with a particular focus on his arguments about evolution and human genetics. I aim to review these in greater detail than has already been done elsewhere, but in terms that are still accessible to a general audience. I will not deal here with Wade’s arguments about the history of Western civilization and the relative contributions of economics and culture to the ascendancy of the West, which are topics that are well outside of my expertise.

Wade begins with the premise that recent population genetic studies reveal that human evolution has been “recent, copious, and regional.” On these very general points, I have no disagreement. The idea that all changes in allele frequencies ceased with the invention of agriculture is a notion that no one—apart from some of my introductory biology students—takes at all seriously. Likewise, it is inarguable that human populations vary genetically. As the evolutionary geneticist Richard Lewontin put it, “you don’t need a population geneticist to tell you that.”

However, starting from these uncontroversial (and frankly, rather banal) premises, Wade goes on to draw all manner of dramatic conclusions. Among other things, Wade works out that modern genetics confirm the existence of “three primary races”, that Europeans were genetically preprogrammed to become the world’s dominant culture, that African Americans may have evolved through natural selection to be inherently violent and socially deviant, and that Jews are genetically predisposed to careers in banking. (Seriously. You can’t make this stuff up!) Needless to say, the available evidence does not support Wade’s grandiose conclusions, many of which are directly contradicted by the very work he cites in support of his arguments. Over the next several weeks I will review several of Wade’s major claims, and evaluate what—if anything—the available data say about them.

Does modern genetics confirm the existence of human races?

Humans as a whole are unusual among primates in that we are remarkably genetically similar to one another (Gagneux et al. 1999). Needless to say, however, humans are not all genetically identical, and variation among humans is not distributed randomly. Rather, as is true of most mammals, genetic variation has a measurable geographic pattern in that people that live near each other tend to more genetically similar to one another. Within humans that pattern of geographic variation (or geographic structure) also bears a very strong mark of human history. Humans originated in Africa, and began to disperse into the rest of the world about 50,000 years ago, moving first into the Middle East, then into Europe, Asia, and finally into Oceania and the Americas. As a result, most of human genetic diversity is found within Africa, the source population. 

Human populations outside of Africa show progressively less and less variation as one moves further from Africa (Wang et al. 2007); as humans colonized each part of the globe in turn, each group of colonists carried with them only a subset of the genetic variation found in its source population. The combined effects of geographic structure and the history of humanity’s spread from our African homeland means that, for some genes, particular variants (alleles) are more common in some parts of the world than in others. So, given a sample of DNA from an individual, by looking at which genetic variants that individual carries at many, many genes we can estimate from where in the world that individual originated, often with a stunning degree of precision (Novembre et al. 2008). In addition, work by Noah Rosenberg and colleagues showed that when you use statistical tools (for example, the program STRUCTURE), to group individuals together into a pre-determined number of evolutionarily ideal populations, these populations largely correspond to continents of origin—but with some important exceptions, as we will see (Rosenberg et al. 2002; Rosenberg et al. 2005).

A guide to the science and pseudoscience of A Troublesome Inheritance, part I: The genetics of human populations

A measure of genetic variation (expected heterozygosity) contained within human populations located progressively further from east Africa, where modern humans originated. Image is from Wang et al. (2007), figure 2A.

In summarizing these facts about human genetic variation, Wade is largely on the mark. However, he misses several important points, both of which have major implications for Wade’s conclusions. The first of these, as has been pointed out by Jennifer Raff on her blog, Violent Metaphors, and as Jeremy Yoder explains in great technical detail at The Molecular Ecologist, STRUCTURE (the software used to cluster individuals into populations) does not, on its own, identify how many clusters actually exist. Rather, the investigator defines the number of populations in advance, and STRUCTURE then clusters the individuals accordingly[1], trying to find the statistically ‘best’ arrangement of individuals.

So, for example, a scientist might obtain a sample of genetic data from people living in each of several villages in the Alps, including some villages in Germany, and some in Switzerland. She would then feed these data into STRUCTURE. STRUCTURE will then ask for directions about how the data should be analyzed, including how many clusters it should use when grouping the individuals. In this case, since samples were taken from each of two countries, the scientist might tell STRUCTURE to assign the people into two populations. STRUCTURE will then assign each individual into a particular population, trying to create populations that—based on the frequency of genotypes within each resulting cluster—appear to be freely interbreeding.

Depending on how STRUCTURE organizes the individuals into these clusters, potentially interesting conclusions could be drawn. For example, we might find that the two clusters correspond to political boundaries—with people from villages in each country clustering together. Alternatively, the results might show that people from different villages that speak the same language cluster together, with the French and German speakers each forming separate groups, suggesting that language is more important than geography in determining who mates with whom. However, if the scientist had chosen to group the people into three clusters, instead of two, a different result might have emerged. For example, she might have found that both geography and language matter, with all the French speakers from Switzerland forming one cluster, the German-speaking Swiss another, and the people living in Germany forming a third.

Importantly, how many clusters are identified is a decision made by the scientist, not something that STRUCTURE determines. So, figuring out how many populations actually exist requires that we use some other criteria. At the time that Rosenberg completed their initial analyses, appropriate statistical tools for identifying the “optimal” number of clusters had not been developed [2]. Rosenberg’s group did, however, evaluate how the number of clusters chosen in advance affected “clusteredness” (the extent to which each individual is identified as belonging to one population, as opposed to having ancestry in multiple populations). They found that the highest levels of clusteredness were reached when STRUCTURE was asked to group individuals into 5 or 6 clusters (both of these produced similar levels of clusteredness when all individuals and all the genetic data were included) (Rosenberg et al. 2005).

The second important point that Wade seems to miss is that these idealized populations (or population clusters) do not correspond to any conventional racial classifications. Although Wade, conveniently, never explicitly defines what he actually means by race, he repeatedly makes the claim that modern genetics identifies “three primary races,” which he identifies as Africans, East Asians, and Europeans. These groupings correspond to the ‘negroid’, ‘mongoloid’, and ‘caucasoid’ races described by classical physical anthropology. The trouble is that none of the contemporary studies of human genetic variation actually find this.

Although Rosenberg and colleagues’ work showed that for five clusters the resulting groups correspond reasonably well to continent of origin—Africa, Europe, Asia, Oceania and the Americas (Wade manages to fold this into his ‘three primary races’ narrative by calling the Oceania and American groups as ‘minor continental races’), subsequent work by Sarah Tishkoff, which used a statistical criterion to identify the ‘best’ number of population clusters, identified 14 groups, nine of which were contained entirely within Africa (Tishkoff et al. 2009). That is, if we allow the data to identify human ‘races’ without guidance, we find 14, not Wade’s “three primary races”.

References

Bryc K., T. Karafet, A. Moreno-Estrada, A. Reynolds, A. Auton, M. Hammer, C. D. Bustamante & H. Ostrer (2010). Genome-wide patterns of population structure and admixture among Hispanic/Latino populations, Proceedings of the National Academy of Sciences, 107 (Supplement_2) 8954-8961. DOI: 10.1073/pnas.0914618107

Cavalli-Sforza L.L., C.R. Cantor, R.M. Cook-Deegan & M.-C. King (1991). Call for a worldwide survey of human genetic diversity: A vanishing opportunity for the Human Genome Project, Genomics, 11 (2) 490-491. DOI: 10.1016/0888-7543(91)90169-f

Evanno G. & J. Goudet (2005). Detecting the number of clusters of individuals using the software structure: a simulation study, Molecular Ecology, 14 (8) 2611-2620. DOI: 10.1111/j.1365-294x.2005.02553.x

Gagneux P., U. Gerloff, D. Tautz, P. A. Morin, C. Boesch, B. Fruth, G. Hohmann, O. A. Ryder & D. S. Woodruff (1999). Mitochondrial sequences show diverse evolutionary histories of African hominoids, Proceedings of the National Academy of Sciences, 96 (9) 5077-5082. DOI: 10.1073/pnas.96.9.5077

Moreno-Estrada A., J. C. Fernandez-Lopez, F. Zakharia, M. Sikora, A. V. Contreras, V. Acuna-Alonzo, K. Sandoval, C. Eng, S. Romero-Hidalgo & P. Ortiz-Tello & (2014). The genetics of Mexico recapitulates Native American substructure and affects biomedical traits, Science, 344 (6189) 1280-1285. DOI: 10.1126/science.1251688

Moreno-Estrada A., Fouad Zakharia, Jacob L. McCauley, Jake K. Byrnes, Christopher R. Gignoux, Patricia A. Ortiz-Tello, Ricardo J. Martínez, Dale J. Hedges, Richard W. Morris & Celeste Eng & (2013). Reconstructing the population genetic history of the Caribbean, PLoS Genetics, 9 (11) e1003925. DOI: 10.1371/journal.pgen.1003925

Morton SG (1839) Crania Americana: An essay on the varieties of the human species. J. Dobson, Philadelphia.

Novembre J., Katarzyna Bryc, Zoltán Kutalik, Adam R. Boyko, Adam Auton, Amit Indap, Karen S. King, Sven Bergmann, Matthew R. Nelson & Matthew Stephens & (2008). Genes mirror geography within Europe, Nature, 456(7218) 98-101. DOI: 10.1038/nature07331

Rosenberg N.A., Sohini Ramachandran, Chengfeng Zhao, Jonathan K. Pritchard & Marcus W. Feldman (2005). Clines, clusters, and the effect of study design on the inference of human population structure, PLoS Genetics, 1 (6) e70. DOI: 10.1371/journal.pgen.0010070

Rosenberg N.A. (2002). Genetic structure of human populations, Science, 298 (5602) 2381-2385. DOI: 10.1126/science.1078311

Tishkoff S.A., F. R. Friedlaender, C. Ehret, A. Ranciaro, A. Froment, J. B. Hirbo, A. A. Awomoyi, J.-M. Bodo, O. Doumbo & M. Ibrahim & (2009). The genetic structure and history of Africans and African Americans, Science, 324(5930) 1035-1044. DOI: 10.1126/science.1172257

Wang S., Mattias Jakobsson, Sohini Ramachandran, Nicolas Ray, Gabriel Bedoya, Winston Rojas, Maria V. Parra, Julio A. Molina, Carla Gallo & Guido Mazzotti & (2007). Genetic variation and population structure in Native Americans, PLoS Genetics, 3 (11) e185. DOI: 10.1371/journal.pgen.0030185

[1] STRUCTURE groups individuals into a predetermined number of clusters ‘K’, in such a way that the distribution of genetic variation (the genotype frequencies) within each cluster makes it appear that mating is occurring at random. That is, the software seeks to arrange individuals into groups in a way that minimizes the overall departures from Hardy-Weinberg equilibrium and linkage equilibrium.

[2] Subsequently a statistical approach has been suggested (Evanno et al. 2005), which selects the optimal number of clusters based on the rate at which the probability of observing the data, given the number of clusters posited, increases as more clusters are proposed. To my knowledge this approach has not been used to identify the optimal number of clusters in the Rosenberg dataset.

[3] The difference between genetic variation between races versus genetic variation within races is an important distinction (one that Wade entirely misses), which I will take up in a future post.

[4] Note that ‘genetic differentiation’ is not the same thing as genetic variation. Overall, Native American populations harbor far less genetic variation than the people of any other continent, having traveled further from Africa than any other group. The Moreno-Estrada result refers to a statistical measure of genetic variation called Wright’s FST, which measures the extent of genetic exchange between two populations, or, more precisely, the degree to which the distribution of genetic variation differs from what we would expect if the people living in each population were as likely to mate with someone from the other population as with someone from their own population.