The true story of the Archaean genetic expansion

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I’ve been giving talks at scientific meetings on educational outreach — I’ve been telling the attendees that they ought to start blogs or in other ways make more of an effort to educate the public. I mentioned one successful result the other day, but we need more.

I give multiple reasons for scientists to do this. One is just general goodness: we need to educate a scientifically illiterate public. Of course, like all altruism, this isn’t really recommended out of simple kindness, but because the public ultimately holds the pursestrings, and science needs their understanding and support. Another reason, though, is personal. Scientific results get mangled in press releases and news accounts, so having the ability to directly correct misconceptions about your work ought to be powerfully attractive. Even worse, though, I tell them that creationists are actively distorting their work. This goes beyond simple ignorance and incomprehension into the malign world of actively lying about the science, and it happens more often than most people realize.

I have another painful example of deviousness of creationists. There’s a paper I’ve been meaning to write up for a little while, a Nature paper by David and Alm that reveals an ancient period of rapid gene expansion in the Archaean, approximately 3 billion years ago. Last night I thought I’d just take a quick look to see if anybody had already written it up, so I googled “Archaean genetic expansion,” and there it was: a couple of references to the paper itself, a news summary, one nice science summary, and…two creationist distortions of the paper, right there on the first page of google results. I told you! This happens all the time: if there’s a paper in one of the big journals that discusses more evidence for evolution, there is a creationist hack somewhere who’ll quickly write it up and lie about it. It’s a heck of a lot easier to summarize a paper if you don’t understand it, you see, so they’ve got an edge on us.

One of the creationist summaries is by an intelligent design creationist. He looks at the paper and claims it supports this silly idea called front-loading: the Designer seeded the Earth with creatures that carried a teleological evolutionary program, loading them up with genes at the beginning that would only find utility later. The unsurprising fact that many gene families are of ancient origin seems to him to confirm his weird idea of a designed source, when of course it does nothing of the kind, and fits quite well in an evolutionary history with no supernatural interventions at all.

The other creationist summary is from an old earth biblical creationist who tries to claim that “explosive increase in biochemical capabilities happened in anticipation of changes that were to take place in the environment”, a conclusion completely unsupportable from the paper, and also tries to telescope a long series of changes documented in the data into a single ancient event so that they can claim that the rate of innovation was so rapid that it contradicts the “evolutionary paradigm”.

So lets take a look at the actual paper. Does it defy evolutionary theory in any way? Does it actually make predictions that fit creationist models? The answer to both is a loud “NO”: it is a paper using methods of genomic analysis that produce evolutionary histories, it describes long periods of gradual modification of genomes, and it correlates genomic innovations with changes in the ancient environment. It is freakin’ bizarre that anyone can look at this work and think it supports creationism, but there you are, standard operating procedure in the fantasy world of the creationist mind.

Here’s the abstract, so you can get an idea of the conclusions the authors draw from the work.

The natural history of Precambrian life is still unknown because of the rarity of microbial fossils and biomarkers. However, the composition of modern-day genomes may bear imprints of ancient biogeochemical events. Here we use an explicit model of macro- evolution including gene birth, transfer, duplication and loss events to map the evolutionary history of 3,983 gene families across the three domains of life onto a geological timeline. Surprisingly, we find that a brief period of genetic innovation during the Archaean eon, which coincides with a rapid diversification of bacterial lineages, gave rise to 27% of major modern gene families. A functional analysis of genes born during this Archaean expan- sion reveals that they are likely to be involved in electron-transport and respiratory pathways. Genes arising after this expansion show increasing use of molecular oxygen (P=3.4 x 10-8) and redox- sensitive transition metals and compounds, which is consistent with an increasingly oxygenating biosphere.

This work is an analysis of the distribution of gene families in modern species. Gene families, if you’re unfamiliar with the term, are collections of genes that have similar sequences and usually similar functions that clearly arose by gene duplications. A classic example of a gene family are the globin genes, an array of very similar genes that produce proteins that are all involved in the transport of oxygen; they vary by, for instance, their affinity for oxygen, so there is a fetal hemoglobin which binds oxygen more avidly than adult hemoglobin, necessary so the fetus can extract oxygen from the mother’s circulatory system.

So, in this paper, David and Alm are just looking at genes that have multiple members that arose by gene duplication and divergence. They explicitly state that they excluded singleton genes, things called ORFans, which are unique genes within a lineage. That does mean that their results underestimate the production of novel genes in history, but it’s a small loss and one the authors are aware of.

If we were looking for evidence for evolution, we might as well stop here. The existence of gene families, for cryin’ out loud, is evidence for evolution. This paper is far beyond arguing about the truth of evolution — that’s taken for granted as the simple life’s breath of biology — but instead asks a more specific question: when did all of these genes arise? And they have a general method for estimating that.

Here’s how it works. If, for example, we have a gene family that is only found in animals, but not in fungi or plants or protists or bacteria, we can estimate the date of its appearance to a time shortly after the divergence of the animal clade from all those groups. If a gene family is found in plants and fungi and animals, but not in bacteria, we know it arose farther back in the past than the animal-only gene families, but not so far back as a time significantly predating the evolution of multicellularity.

Similarly, we can also look at gene losses. If a gene family or member of a gene family is present in the bacteria, and also found in animals, we can assume it is ancient in origin and common; but if that same family is missing in plants, we can detect a gene loss. Also, if the size of the gene family changes in different lineages, we can estimate rates of gene loss and gene duplication events.

I’ve given greatly simplified examples, but really, this is a non-trivial exercise, requiring comparisons of large quantities of data and also analysis from the perspective of the topologies of trees derived from that data. The end result is that each gene family can be assigned an estimated date of origin, and that further, we can estimate how rapidly new genes were evolving over time, and put it into a rather spectacular graph.


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Rates of macroevolutionary events over time. Average rates of gene birth (red), duplication (blue), HGT (green), and loss (yellow) per lineage (events per 10 Myr per lineage) are shown. Events that increase gene count are plotted to the right, and gene loss events are shown to the left. Genes already present at the Last Universal Common Ancestor are not included in the analysis of birth rates because the time over which those genes formed is not known. The Archaean Expansion (AE) was also detected when 30 alternative chronograms were considered. The inset shows metabolites or classes of metabolites ordered according to the number of gene families that use them that were born during the Archaean Expansion compared with the number born before the expansion, plotted on a log2 scale. Metabolites whose enrichments are statistically significant at a false discovery rate of less than 10% or less than 5% (Fisher’s Exact Test) are identified with one or two asterisks, respectively. Bars are coloured by functional annotation or compound type (functional annotations were assigned manually). Metabolites were obtained from the KEGG database release 51.0 and associated with clusters of orthologous groups of proteins (COGs) using the MicrobesOnline September 2008 database28. Metabolites associated with fewer than 20 COGs or sharing more than two- thirds of gene families with other included metabolites are omitted.

Look first at just the red areas. That’s a measure of the rate of novel gene formation, and it shows a distinct peak early in the history of life, around 3 billion years ago. 27% of our genes are very, very old, arising in this first early flowering. Similarly, there’s a slightly later peak of gene loss, the orange area. This represents a period of early exploration and experimentation, when the first crude versions of the genes we use now were formed, tested, discarded if inefficient, and honed if advantageous.

But then the generation of completely novel genes drops off to a low to nonexistent rate (but remember, this is an underestimate because ORFans aren’t counted). If you draw any conclusions from the graph, it’s that life on earth was essentially done generating new genes about one billion years ago…but we know that all the multicellular diversity visible to our eyes arose after that period. What gives?

That’s what the blue and green areas tell us. We live in a world now rich in genetic diversity, most of it in the bacterial genomes, and our morphological diversity isn’t a product so much of creating completely new genes, but of taking existing, well-tested and functional genes and duplicating them (blue) or shuffling them around to new lineages via horizontal gene transfer (green). This makes evolutionary sense. What will produce a quicker response to changing conditions, taking an existing circuit module off the shelf and repurposing it, or shaping a whole new module from scratch through random change and selection?

This diagram gives no comfort to creationists. Look at the scale; each of the squares in the chart represents a half billion years of time. The period of rapid bacterial cladogenesis that produced the early spike is between 3.3 and 2.9 billion years ago — this isn’t some brief, abrupt creation event, but a period of genetic tinkering sprawling over a period of time nearly equal to the entirety of the vertebrate fossil record of which we are so proud. And it’s ongoing! The big red spike only shows the initial period of recruitment of certain genetic sequences to fill specific biochemical roles — everything that follows testifies to 3 billion years of refinement and variation.

The paper takes another step. Which genes are most ancient, which are most recent? Can we correlate the appearance of genetic functions to known changes in the ancient environment?

the metabolites specific to the Archaean Expansion (positive bars in Fig. 2 inset) include most of the compounds annotated as redox/e– transfer (blue bars), with Fe-S-binding, Fe-binding and O2-binding gene families showing the most significant enrichment (false discovery rate<5%, Fisher’s exact test). Gene families that use ubiquinone and FAD (key metabolites in respiration pathways) are also enriched, albeit at slightly lower significance levels (false discovery rate<10%). The ubiquitous NADH and NADPH are a notable exception to this trend and seem to have had a function early in life history. By contrast, enzymes linked to nucleotides (green bars) showed strong enrichment in genes of more ancient origin than the expansion.

The observed bias in metabolite use suggests that the Archaean Expansion was associated with an expansion in microbial respiratory and electron transport capabilities.

So there is a coherent pattern: genes involved in DNA/RNA are even older than the spike (vestiges of the RNA world, perhaps?), and most of the genes associated with the Archaean expansion are associated with cellular metabolism, that core of essential functions all extant living creatures share.

Were we done then, as the creationists would like to imply? No. The next major event in the planet’s history is called the Great Oxygenation Event, in which the fluorishing bacterial populations gradually changed the atmosphere, excreting more and more of that toxic gas, oxygen.

What happened next was a shift in the kinds of novel genes that appeared: these newer genes were involved in oxygen metabolism and taking advantage of the changing chemical constituents of the ocean.

Our metabolic analysis supports an increasingly oxygenated biosphere after the Archaean Expansion, because the fraction of proteins using oxygen gradually increased from the expansion to the present day. Further indirect evidence of increasing oxygen levels comes from compounds whose availability is sensitive to global redox potential. We observe significant increases over time in the use of the transition metals copper and molybdenum, which is in agreement with geochemical models of these metals’ solubility in increasingly oxidizing oceans and with molybdenum enrichments from black shales suggesting that molybdenum began accumulating in the oceans only after the Archaean eon16. Our prediction of a significant increase in nickel utilization accords with geochemical models that predict a tenfold increase in the concentration of dissolved nickel between the Proterozoic eon and the present day but conflicts with a recent analysis of banded iron formations that inferred monotonically decreasing maximum concentrations of dissolved nickel from the Archaean onwards. The abundance of enzymes using oxidized forms of nitrogen (N2O and NO3) also grows significantly over time, with one-third of nitrate-binding gene families appearing at the beginning of the expansion and three-quarters of nitrous-oxide-binding gene families appearing by the end of the expansion. The timing of these gene-family births provides phylogenomic evidence for an aerobic nitrogen cycle by the Late Archaean.

So I don’t get it. I don’t see how anyone can look at that diagram, with its record of truly ancient genomic changes and its evidence of the steady acquisition of new abilities correlated with changes in the environment of the planet, and declare that it supports a creation event or front-loading of biological potential in ancestral populations. That makes no sense. This is work that shouts “evolution” at every instant, yet some people want to pretend it’s an endorsement of theological hocus-pocus? Madness.

Scientists, you need to be aware of this. The David and Alm paper is an unambiguously evolutionary paper, using genomic data to describe evolutionary events via evolutionary mechanisms, and the creationists still appropriate and abuse it. If you publish anything about evolution, be sure to google your paper periodically — you may find that you’ve been unwittingly roped into endorsing creationism.

David LA, Alm EJ (2011) Rapid evolutionary innovation during an Archaean genetic expansion. Nature 469(7328):93-6.

Paul Nelson takes a stab at Ontogenetic Depth again…which makes me go stab-stab-stabbity-stab

Paul Nelson has deigned to write a two-part essay on “Ontogenetic Depth“, his sciencey made-up term for a metric that he claims makes evolution essentially impossible. We’ve been wrangling over this for a long time — he and Marcus Ross introduced this in a poster at the Developmental Biology meetings in 2004, titled “Understanding the Cambrian Explosion by Estimating Ontogenetic Depth”, and in our conversation at that time I certainly got the impression that he and Ross were busy collecting this peculiar thing alien to creationists called “data”. I have asked him multiple times over the last 7 years how to estimate this hypothetical number; at the meetings, I recall asking him specifically how I would go back into my lab and measure it in my zebrafish. He was evasive. We’ve been trying to get him to explain this datum, which was his pretext for getting into a professional meeting, and gotten nothing.

Well, now we’re done. His first point in his first essay is that “ontogenetic depth” is “A Biological Distance That’s Currently Impossible to Measure”.

Oh.

So what the heck were Paul Nelson and Marcus Ross doing? Nelson was certainly doing his best to pretend that they were actually doing real work on this metric, but I should have known better: a failed young-earth creationist philosopher could not possibly have been soiling his hands with empiricism. Now he’s frantically arguing that it doesn’t matter, that once upon a time no one knew the distance from the earth and the sun, but they could at least name the concept, so he can take credit for at least recognizing a real problem, and he can also patronizingly thank me for pointing out that they don’t actually have the tools right now to actually measure it.

Wait, how can they thank me for that? I’m picturing Nelson and Ross sitting at a microscope and looking at eggs of a nematode or a zebrafish or a frog, rubbing their hands in anticipation of a productive morning, and then staring at each other and wondering what to do next…and end up inventing a term for something that they don’t know how to measure. And then a year or so later, Nelson encounters me, I peevishly tell him that he doesn’t know how to measure cell division and differentiation in terms of a single numeric metric, and seven years after that, Nelson finally slaps his forehead and admits “Hey, we don’t know how to measure that!”

I don’t want credit for pointing out the obvious to the clueless, especially not when they’re that slow.

His first essay is an exercise in rationalizing away how he could propose this obstacle to evolution while not having the slightest idea how to measure it. His second essay is an exercise in demonstrating that he doesn’t understand basic biology. He has gussied it up with brightly colored diagrams of cell pedigrees that he purports illustrate the problem, but I think are actually more intended to distract and confuse and make you think he’s actually thought deeply about the subject.

Here’s the gist of his conceptual difficulty: he can’t imagine how the first metazoan got from a crude colonial state, where it’s just a mass of identical cells clumped together, to a state in which regions are consistently specialized for specific functional roles, with the simplest example of an animal that contains only two cell types, a mass of somatic cells that take care of feeding and motility, and a smaller mass of germ cells that do the job of reproduction. Why, that would require a whole series of mutations that selection can’t possibly explain! How could selection possibly create a cell that contains a series of instructions to build a cell type that isn’t going to reproduce?

I’m wishing that Nelson hadn’t chosen to focus on biology. If only he were a creationist philosopher of physics, he’d be the one asking, “magnets, how do they work?” and somebody else would get the job of correcting him.

Nelson summarizes the problem as, at the minimum in the simplest possible metazoan, a three step sequence. First, cells have to divide and stick together; second, they have to have a way to make daughter cells differ from one another; and third, there has to be inheritance of that differentiated state in sublineages. He claims that in none of these steps can selection be involved; this complex process had to evolve independently of any selective effects.

That’s nonsense. The first metazoan already had all the tools needed to build these steps, honed by a billion years or more of selection in single-celled organisms. All three of his steps are found in bacteria.

Step one is simply cell adhesion. Step two is gene regulation. Step three is epigenetics. That’s it. These aren’t glorious novelties invented by the first animals, they inherited this toolkit from their ancestors. Bacteria have been sticking together for billions of years, and they’ve been responding to their local environment by shifting patterns of gene expression for just as long. A bacterium in a sugar-rich environment vs. a bacterium in a sugar-poor environment will make long term changes in gene activity that can persist for a few generations using exactly the same mechanisms as an animal embryo sets up germ and somatic tissues; has Nelson never heard of Jacob and Monod?

Nelson’s argument goes beyond pure ignorance, however. He also recruits Lewis Wolpert to his side, which is remarkable. Wolpert is a brilliant and influential developmental biologist who shaped many of our ideas about differentiation, pattern formation, and evolution. He cites Wolpert as postulating as serious problems for evolution the origin of the egg, and in particular implying that Wolpert sees metazoan evolution as violating a principle. Here’s what Nelson says about a particular paper Wolpert wrote.

Evolutionary developmental biologist Lewis Wolpert — whom no one, even in his wildest delirium, would ever mistake for an ID theorist — had long critiqued the scenario on functional grounds, using what he called “the continuity principle.” (1994) The continuity principle requires that any change occurring in an evolutionary transformation be biologically possible, that is, viable and stably heritable in the next generation.

Whoa — eminent anti-creationist scientist critiques an evolutionary explanation! I’m sure this must make you wonder, familiar as you are with creationist tactics, what Wolpert actually said. Judge for yourself, here’s the abstract for Wolpert’s paper, does it sound like he’s on Nelson’s side at all?

A scenario for the evolution of a simple spherical multicellular organism from a single eukaryotic cell is proposed. Its evolution is based on environmentally induced alterations in the cell cycle, which then, by the Baldwin effect, become autonomous. Further patterning of this primitive organism–a Blastaea, could again involve environmentally induced signals like contact with the substratum, which could then become autonomous, by, perhaps, cytoplasmic localization and asymmetric cell division. Generating differences between cells based on positional information is probably very primitive, and is well conserved; its relation to asymmetric cell division is still unclear. Differentiation of new cell types can arise from non equivalence and gene duplication. Periodicity also evolved very early on. The origin of gastrulation may be related to mechanisms of feeding. The embryo may be evolutionarily privileged and this may facilitate the evolution of novel forms. Larvae are secondarily derived and direct development is the primitive condition as required by the continuity principle.

This is a paper in which Wolpert explains how multicellularity could have evolved, directly answering the questions Nelson raised with his supposedly problematic three steps. How did Paul Nelson miss that?

But wait! There’s more Wolpert abuse!

Nelson has found a paper by Wolpert in which he points out a serious problem in a particular evolutionary strategy, and Nelson, apparently primed by a selective reading of science papers for the magic words “problem”, “difficulty”, “impossible”, or “unlikely” has seized upon it as another instance of Eminent Scientist Critiquing Evolution.

What mechanism is coordinating gene expression among all the members of the colony, such that only one cell lineage will evolve to carry the complete instruction set required to specify the form of the whole? How are mutations — occurring in all individual cells of the colony — transmitted to the next generation? If individual cells continue to reproduce via normal fission, or budding, notes Wolpert, “cell lineages [will be] mutating in all sorts of directions in genetic space.” (2002, 745) Given such genetic chaos, he argues, “we consider it practically impossible” for the collection of cells to “yet retain the ability to evolve into viable new forms.”

Sounds dreadful. I give up, I guess evolution must actually be impossible.

Hang on, though, maybe we should read Wolpert’s paper first. And there what you discover is a story that you would not have expected from Nelson’s peculiarly distorted coverage. It’s a short paper where the authors consider alternative reproduction strategies: not all animals go through a single-cell stage in reproduction, you know. Some, like hydra, reproduce by budding, where a small collection of cells, not just one egg or sperm cell, splits off to form an independent organism. Wolpert is considering which solution is more advantageous for evolution, going through a single-cell bottleneck or through a larger population that would reduce the dangers of mutations? And that’s where Wolpert’s criticisms lie: the asexual budding solution is the focus of his critique, and which is where Nelson draws his quotes highlighting the difficulty of evolution.

In a hydra-like organism that only reproduces by asexual budding, it is impossible to evolve significant changes. There is no way that the genes in the huge number of cells involved in budding can change at the same time, and mutations in individual cells mean that they no longer share the behavioural rules of the majority. It is only through a coherent developmental programme, with all cells possessing the same genes, that organisms can evolve, and this requires an egg.

Huh. So Wolpert is arguing that development from a multicellular propagule is much less evolutionarily flexible than evolution from a single-celled egg. His thesis is explaining why we develop from eggs, not that our evolution is unlikely.

We consider it practically impossible to have many asexual, differentiated cell lineages mutating in all sorts of directions in genetic space and yet retain the ability to evolve into viable new forms. This may not be completely impossible but, taking the broad view in evolutionary terms, organisms that develop from an egg would displace those that do not.

Dang, Paul Nelson. You should be smart enough to know that you don’t quotemine claims from the science literature in an argument with someone who has actually read that literature.

Jesse Bering responds

I was not kind in my assessment of Jesse Bering’s story about the evolutionary psychology of homophobia. He was quite irate with me and several other people who pointed out the tattered fabric of his evidence. Now he has gone scurrying back to the author of the study he described, Gordon Gallup, and gotten his take in a rather tendentious interview. Between the two of them, unfortunately, they still can’t manage to address anyou of our criticisms. It’s a very weird conversation: here’s how he handles me.

One common complaint lodged against evolutionary psychology is that its methods, which typically do not track the claimed fitness benefit, are inadequate for testing its hypotheses. PZ Myers, in surveying your homophobia studies, writes:

They know nothing about heritability, they’ve shown nothing about differential survival or fecundity … Is this to be the fate of evolutionary psychology, that it shrivels away into irrelevancy as its proponents overhype (sic) feeble, pathetic data sets?

Myers is, of course, notorious for such over-the-top statements—like the Jim Bakker of New Atheists, a caricature of sweat, histrionics and stage glitter, he sees religious conspiracies as often as evangelicals see the Devil.

Oh, man, glitter! I just knew I’d been forgetting something for my stage show.

Despite that useful bit of information, however, it’s dodging the issue with irrelevancies. I did not accuse Gallup or Bering of committing some religious conspiracy, nor did I even mention religion in my complaint. I said there was no evidence to back up their claims that homophobia conferred a fitness benefit, or even that it was a heritable trait. I know, expecting evidence of an evolutionary psychologist may be a sign of hysteria, and certainly is over-the-top, but I would expect that a reply to shoot me down would be the presentation of evidence to show I was wrong.

They don’t do that.

Instead, Gallup mentions a series of papers he’s published that have nothing to do with homophobia. For instance, he claims that they’ve “shown that a person’s voice is also related to fitness.” But they haven’t! I looked at the paper: it’s another self-reporting exercise in which they determined that people perceive women’s voices as more or less attractive in different stages of their menstrual cycle. Again, there is no attempt to examine inheritance, or whether this perception actually affects survival or fecundity…so we’re right back at my original complaint.

I’m not even going to touch Bering’s unwarranted moral indignation at the idea that Gallup might be a homophobe, which is not only irrelevant but wasn’t even suggested by any of his critics, or his silly conclusion that he’ll do anything to understand why gay men and women are bullied and murdered around the world…as if all of his critics are somehow just fine with the oppression of homosexuals.

Again, Jeremy Yoder has another solid response to the nonsense.

Much fuss about nothing at all

Jesse Bering disappointed me recently. He started off another evolutionary psychology story with this warning.

Consider this a warning: the theory I’m about to describe is likely to boil untold liters of blood and prompt mountains of angry fists to clench in revolt. It’s the best–the kindest–of you out there likely to get the most upset, too. I’d like to think of myself as being in that category, at least, and these are the types of visceral, illogical reactions I admittedly experienced in my initial reading of this theory. But that’s just the non-scientist in me flaring up, which, on occasion, it embarrassingly does. Otherwise, I must say upfront, the theory makes a considerable deal of sense to me.

Oh, boy. I love the throb of adrenaline coursing through my bloodstream. So I read further, expecting fierce data and challenging ideas.

They weren’t there. The hypothesis is rather bold — it’s the idea that homophobia is actually adaptive — but there’s no substance there. It turns out the data is all dueling surveys of people’s views about gay people. “Meh,” I said, and unclenched my fists and dabbed at the blood that was going to squirt out my eyes and damped down the fires that had just begun to flare up from the sparks crackling from my fingertips. That isn’t even interesting. They know nothing about heritability, they’ve shown nothing about differential survival or fecundity, they haven’t even tried to sort out cultural biases from biology. Is this to be the fate of evolutionary psychology, that it shrivels away into irrelevancy as its proponents overhype feeble, pathetic data sets?

I couldn’t even muster the enthusiasm to spit contemptuously, but fortunately, Jeremy Yoder has taken on the subject and nicely dismantled the exaggerations and fallacies. Go read that.

Brachiopods: another piece in the puzzle of eye evolution

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About 600 million years ago, or a little more, there was a population of small wormlike creatures that were the forebears of all modern bilaterian animals. They were small, soft-bodied, and simple, not much more than a jellyfish in structure, and they lived by crawling sluglike over the soft muck of the sea bottom. We have no fossils of them, and no direct picture of their form, but we know a surprising amount about them because we can infer the nature of their genes.

These animals would have been the predecessors of flies and squid, cats and starfish, and what we can do is look at the genes that these diverse modern animals have, and those that are held in common we all inherited together from that distant ancestor. So we know that flies and cats both have hearts that are initiated in early development by the same genes, nkx2.5 and tinman, and infer that our common ancestor had a heart induced by those genes…and that it was only a simple muscular tube. We know that modern animals all have a body plan demarcated by expression of Hox genes, containing muscles expressing myoD, so it’s reasonable to deduce that our last common ancestor had a muscular and longitudinally patterned body. And all of us have anterior eyes demarcated by early expression of pax6, as did our ancient many-times-great grandparent worm.

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We do not have fossils of these small, soft organisms, but that’s no obstacle to picturing them. You just have to see the world like a modern molecular or developmental biologist. One of the graphical conceits of the Matrix movies was that the hero could see the hidden mathematical structure of the world, which was visualized as green streams of symbols flowing over everything. We aspire to the same understanding of the structure of life, only what we see are patterns of genetic circuity, shared modules that are whirring away throughout development to produce the forms we see with our eyes; and also, unfortunately, we currently only see these patterns spottily and murkily. There is no developmental biologist with the power of Neo yet, but give us a few decades.

There’s another thing we know about these ancient ancestors: they had two kinds of eyes. ciliary and rhabomeric. Your eyes contain ciliary photoreceptors; they have a particular cellular structure, and they use a recognizable form of opsin. A squid has a distinctly different kind of photoreceptor, called rhabdomeric, with a different cell structure and a different form of opsin. We humans also have some rhabdomeric receptors tucked away in our retinas, while invertebrates have ciliary receptors as well, so we know the common ancestor had both.

Now this ancestral population eventually split into two great tribes, the protostomes, which includes squid and flies, and the deuterostomes, which includes cats and starfish. It should be an obvious indication of the general state of that ancestor that it represents all that those four diverse animals have in common. It also tells us that while that ancestor had eyes, they were almost certainly very simple, and could have been nothing more than a patch of light-sensitive cells, or perhaps even single cells, as we see in some larval eyes.

What we think happened at this division is that both tribes took the primitive eyes and specialized them independently. Each group evolved under similar constraints: they needed directionally-sensitive eyes that could tell what direction a source of illumination was coming from (and these would eventually form true image-forming eyes), and they also needed sensors to detect general light levels — is it day or night, are we in the open or under a rock? Think of it like a camera system: there is a part that gets all the attention, the lens and image-forming chip, but there’s also a light meter that senses ambient light levels.

The two tribes made different choices, though. The protostomes pulled the rhabdomeric photoreceptor out of their toolbox, and used that to make the camera; they used the ciliary photoreceptor to make their light meter. The deuterostomes (actually, just us chordates) instead used the ciliary photoreceptor for their camera, and the rhabdomeric photoreceptor for the light meter. It’s the same ancestral toolkit, but we’ve just specialized in different ways.

At least, that’s the general model we’ve been exploring. A new discovery at the Kewalo Marine Laboratory, one of the premiere labs for evo-devo research, has made the interpretation a little more complex.

That discovery is that brachiopod larvae, which are protostomes, have been found to have directionally sensitive eyes…which are ciliary. A protostome should have directionally sensitive eyes that are rhabdomeric. How interesting!

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Brightfield microscopy of a Terebratalia transversa larva, with red eye spots visible in the apical lobe (black arrows). (A) Dorsal view. (B) Lateral view.

In addition to being ciliary in structure, these eyes express ciliary opsin. They are also true cerebral eyes, also expressing pax6 and having a nervous connection to the central nervous system.

Notice what is going on here: a protostome is building a camera, and unlike all the other protostomes we’ve observed, it’s pulled a ciliary photoreceptor out of its pocket to make it. This is a surprise, but it doesn’t upset any theories too much — it just means we need to explore a couple of alternative explanations. We don’t have answers to resolve these hypotheses yet — we need more data and experiments — but it’ll be fun to watch the work roll onward.

One explanation is illustrated in A, below. The initial animal state was to build directional, cerebral eyes using rhabdomeric photoreceptors. The vertebrates are oddballs who swapped in ciliary receptors instead, while these larval eyes in brachiopods are major peculiarities, an evolutionary novelty which resembles a cerebral eye, but is actually non-homologous. This seems unlikely to me; there are multiple elements of the eye circuitry at work in these eyes, and if they’re using the same gene circuitry, we ought to recognize them as homologous at the molecular level…the only one that counts.

The second explanation in B is that all of these cerebral eyes are homologous, but that the receptor type is more plastic than we thought — it’s relatively easy to switch on the ciliary module vs. the rhabodmeric module, so we would expect to see multiple flip-flops in the evolutionary record.

If we accept that it’s easy to switch receptor type, though, then why assume that the last common ancestor had a directional, cerebral eye that was rhabdomeric? It could have been ciliary, which is also a more parsimonious explanation, because it requires only one switch of types in the protostomes, shown in C.

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(Click for larger image)
Alternative hypothesis on the evolution of photoreceptor deployment in cerebral eyes. Schematic representation of three hypotheses accounting for the deployment of ciliary photoreceptors in the cerebral eyes of Terebratalia and vertebrates, versus rhabdomeric photoreceptors in Platynereis and other protostomes. (A) Deployment of rhabdomeric photoreceptors as the ancestral state in cerebral eyes, with the larval eyes of Terebratalia, containing ciliary photoreceptors, representing an evolutionary novelty. The deployment of ciliary photoreceptors is the result of a substitution (with ciliary photoreceptors having replaced rhabdomeric photoreceptors in the cerebral eyes) early in the chordate lineage. (B) Larval eyes in Terebratalia are homologous to the cerebral eyes in other protostomes, but ciliary photoreceptors have been substituted for rhabdomeric photoreceptors, as in the vertebrates. (C) Ciliary photoreceptors in cerebral eyes represent the ancestral condition, inherited by Terebratalia and vertebrates. Deployment of rhabdomeric photoreceptors in the cerebral eyes of Platynereis and other protostomes are the result of substitution events.

Whichever hypothesis pans out, though, the important message is that photoreceptor type is a more evolutionarily labile choice than previously thought. What I want to see is more research into photoreceptor development in more exotic invertebrates — that’s where we’ll learn more about our evolutionary history.

I have to mention a couple of other cool features of this paper. If you ever want to see a minimalist directional eye, here it is: the larval eye sensor of brachiopods consists of two cells, a lens cell that actually does the job of light detection, and a pigment cell that acts as a shade, preventing light from one direction from striking the lens cell. That’s all it takes.

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I lied! That isn’t a minimal directional eye at all: here it is.

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This rather blew my mind. The brachiopod gastrula senses light. The figure above is of a very early stage in development, when the organism is little more than a couple of sheets of cells with no organs at all, only tisses in the process of forming up into rough structures. It definitely has no brain, no nervous tissue at all, and no eyes…and there it is, that dark blue smear is a region selectively expressing ciliary opsin as if it were a retina. Furthermore, when tested behaviorally (mind blown again…behavior, in a gastrula), populations in a light box show a statistical tendency to drift into the light. Presumably, light stimulation of the opsin is coupled to the activity of cilia used for motility in the outer epithelium of the embryo.

Amazing. It suggests how eyes evolved in multicellular organisms, as well — initially, it was just localized general expression of light-sensitive molecules coupled directly to motors in the skin, no brain required.

Passamaneck Y, Furchheim N, Hejnol A, Martindale MQ, Lüter C (2011) Ciliary photoreceptors in the cerebral eyes of a protostome larva. EvoDevo, 2:6.

Soon to appear on a thousand herpetologist’s doors

xkcd digs into cladistics.

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Unfortunately, his cladogram is wrong. Mammals should also be a subset of the reptiles, so the herpetologists should be demanding that all other amniotes be absorbed into their more inclusive field of tetrapod biology.

At least, until the ichthyologists show up and point out that we’re all just weird dry land-walking fish.

Just to clear this up, I hope, here’s a modified version of a cladistic diagram to show what herps are:

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So if you want to avoid the sins of polyphyly or paraphyly, you must include birds and mammals in the herps. Of course, the alternative is to not care about the abstractions, and recognize that there are plenty of people already specializing in mammals and birds, so someone has to pay attention to all the otherwise neglected classes.

How to tell you’re arguing with an idiot

There are some useful tells. My favorite has the been the classic quotemine, where creationists quote one sentence of Darwin’s — “To suppose that the eye, with all its inimitable contrivances for adjusting the focus to different distances, for admitting different amounts of light, and for the correction of spherical and chromatic aberration, could have been formed by natural selection, seems, I freely confess, absurd in the highest possible degree” — to claim that Darwin was stumped by the evolution of the eye. As everyone who has read the Origin knows, what he was doing there was setting up a rhetorical question, which he then followed by three pages of detailed description of exactly how such an eye could have evolved. When you hear some creationist say “absurd in the highest possible degree,” you know right away that they haven’t read the book.

There’s another great example, though, that’s an even better demonstration of your opponent’s illiteracy. That is when someone cites The Selfish Gene and then goes on to rail against the horrors of evilution and the way it encourages people to be righteous bastards who kill and steal and rape their way to dominance. They haven’t read the book! All they’ve done is scanned a three word title and leapt to a series of absurd conclusions! (Yeah, Mary Midgley, I’m givin’ you the squinky eye.)

Ken MacLeod exposes the inanity of this claim in some detail. It really is astoundingly common for people to expound on how Richard Dawkins was arguing for the rightness of Thatcherism or whatever reactionary conservative policy they think he was endorsing, and get the whole story completely wrong — it really is a great tell. Unfortunately, it seems to expose left wing idiocy more than that of the right, but only because I think the righties make the same invalid assumptions, but since they like that error, they tend not to criticize.

Evolve a car

Looking for a nice demonstration of genetic algorithms? Here’s a simulation that takes randomized connected collections of polygons and wheels and scores them for their ability to traverse a rugged 2D landscape. I tried it last night, and it gave me an assortment of very bad vehicles: for example, a lot of them were just polygonal lumps that fell flat and sat there, while some had an odd wheel here and there, but also pointy bits that acted as brakes, or wheels that pointed upward at the sky and did nothing at all. So I just left it running and went to bed.

This morning, I’ve got strange vehicles running races on my computer screen. Unsurprising, but still kind of cool.

I have annoyed Jesse Bering

That’s what I do, after all. I strongly criticized his uncritical analysis of a set of rape-related evolutionary psychology studies, and now he responds with a rebuttal. It’s not a very good rebuttal, but I highly recommend his second paragraph in which he lists a good collection of links to several people who also ripped into his article. That part is excellent!

But then let’s get into the part where he argues with me.

P.Z. Myers is not, of course, the undisputed public ambassador of his discipline (although I’ve no doubt he sees himself as such), and by no means does the following apply to all biologists, or even all those who are critical of evolutionary psychology. But Myers’ affect-laden views regarding evolutionary psychology do represent those of at least a significant and vocal minority.

Not an auspicious start to accuse me of regarding myself as “the undisputed public ambassador of” biology, which certainly isn’t the case. This is a blog written by a professor in a small town in rural Minnesota. I’m kind of aware of exactly what it is, and lack the airs Bering wants to assign to me. But then, this isn’t surprising, since most of his following arguments rely on telling me what I intended, and he also gets that wrong. Except this little bit, where he does get the overall objections right.

Critics are particularly irritated by the fact that evolutionary psychologists do not test for genetic inheritance of the very traits they argue are adaptive but instead rely on behavioral or self-report measures to evaluate their theories. They also believe that evolutionary psychologists take too many story-telling liberties in reconstructing the ancestral past, since we can never know for certain what life was like hundreds of thousands of years ago, when such traits would have, theoretically, been favored by natural selection. (This is a point also stressed by Rennie in his critique of my Slate essay.) According to Myers, the whole messy endeavor, therefore, “is a teetering pyramid of stacked ‘couldas’ and guesses that it woulda had an influence on evolution.”

This is actually a reasonable summary of my general disagreements with evolutionary psychology. They are quite fond of inventing evolutionary stories about phenomena that don’t even have an iota of evidence for being genetic, and can come up with truly awesome causal accounts for even the most trivial observations.

He picks out one of my objections to argue why the evolutionary psychology crowd can’t do one of the experiments I didn’t suggest doing, which is a little odd, but OK.

In his post, Myers uses my discussion of the evolution of the human penis as a prime example of the sloppy work being done in the study of evolution and human behavior. He pillories psychologist Gordon Gallup’s famous “dildo study,” which suggests that the distinctive mushroom-capped shape of the penis might serve to scoop a competitor’s semen out of the vagina. (I described this work at long, intimate length in two prior articles in Scientific American.) Myers calls this penis study “tripe” because Gallup and his colleagues failed to show how variations in penis shape within a population–and variations in how the penis is used for coital thrusting–directly affect fertilization rates. Instead, the researchers relied on dildos of different designs, surveys of college students’ detailing their sexual behaviors, and a batch of artificial semen.

Now, I can only assume that Myers has not had to face a university human-research ethics committee in the past several decades. If he had, he would realize that his suggested empirical approach would be unilaterally rejected by these conservative bureaucratic gatekeepers. Does Myers really believe that these seasoned investigators wouldn’t rather have done the full experiment he describes–if only they lived in a less prudish and libellous university world? The fact of the matter is that research psychologists studying human sexuality are hamstrung by necessary ethical constraints when designing their studies. Perhaps Myers would be happy enough to allow investigators into his bedroom to examine the precise depth and vigor to which he plunges into his wife’s vaginal canal after they’ve been separated for a week, but most couples would be a tad more reticent. Gallup’s dildo study, and his related work on penis evolution, offered an ingenious–ingenious–way to get around some very real practical and ethical limitations. Is it perfect? No. Again, the perfect study, conceptually speaking, is often the least ethical one, at least as deemed by research ethics committees. But was it driven by clear, testable, evolutionary hypotheses? Yes. And it offered useful information that was otherwise unknown.

Telling me that they can’t do an experiment that I didn’t suggest doing doesn’t really undermine anything I said. I’m perfectly aware of the ethical limitations of human research, which is one reason why I work on animal models. The problem is that what I actually offered as shortcomings of the work wasn’t their failure to wire up my genitals, but this:

They don’t have any evidence that this behavior actually affects the fertilization rate of one partner’s sperm over another, they don’t have any indication of morphological differences in human populations that make some individuals better semen-scoopers, they don’t have any evidence that this behavior has had a differential effect in human history.

Those are the criteria I would expect to see met in order to discuss this issue as an evolutionary problem; what Bering’s sources were studying were mechanical and physiological aspects of some plumbing (which can be interesting!), and then tacking on unwarranted conclusions about evolutionary history. In fact, I don’t see how Bering’s strange and unexecutable experiment of logging the details of my personal sexual behavior would even touch my evolutionary objections.

He also skips over another relevant point I emphasized. I read the research papers he cited. These were studies that had him “riveted, and convinced”, but when I looked at, for instance, the study that found an increase in women’s handgrip strength during ovulation, the paper itself mentioned that there were many other studies that showed no variation in strength over the menstrual cycle. Which is it? Do you just pick the result that favors your interpretation?

Jerry Coyne has a summary of reactions, too, and mentions several instances where the papers aren’t as clear in their support of the evo-psych hypotheses as is claimed. These are very noisy data that sometimes support and sometimes contradict their claims, and it seems that whatever result they pluck out of the mess, it’s always in support of some purported evolutionarily significant effect on behavior or physiology.

As I said in my previous article, I think the general claim of evolutionary psychology, that our current behavior has been shaped by our biological history, is true. I think much of the research in the field is damaging to their thesis, though, not because it demonstrates the opposite, but because it flits over tiny details, like monthly variations in how a woman moves her hips or how she feels about men, and pretends that they’re all examples of the power of natural selection in sculpting a genome that encodes every pelvic wobble and every nerve impulse. It’s become a kind of modern ornithomancy, where each dip and swirl and change in direction of a flight of birds is interpreted as directly connected to the fate of nations. I remain unconvinced.

The evolution of rape?

There are days when I simply cannot bear the entire field of evolutionary psychology: it’s so deeply tainted with bad research and a lack of rigor. And that makes me uncomfortable, because the fundamental premise, that our behaviors are a product of our history, is self-evidently true. It’s just that researchers in this field couple an acceptance of that premise to a deep assumption of adaptive teleology, the very thing that they should be evaluating, and produce some of the most awesomely trivial drivel.

I’ve just finished reading an article titled “Darwin’s Rape Whistle: Have women evolved to protect themselves from sexual assault?“, and it’s everything I despise about evolutionary psychology. It’s nothing but sloppy thinking and poor science propped up by a conviction that plausibility is sufficient support for certainty.

I could fulminate for a few hours over this crap, but fortunately Jerry Coyne has calmly criticized the mess, so I’ll just make a few points.

The story is that women have evolved specific adaptive responses to the threat of rape. In support of this conclusion, the author cites various studies that claim to show that ovulating women show stronger handgrip strength (the better to fight off men who want to assault their eggs with sperm), that ovulating women are more suspicious of men, that ovulating women are more likely to avoid risky behaviors, and that ovulating white women become more fearful of black men. I’m unimpressed. All of the studies involve small numbers, typically of college students at American universities (and even more narrowly, of psychology students), and all involve responses to highly subjective stimuli. When you examine the literature cited in these papers, you discover that different investigators get different results — the handgrip study even admits up front that there are conflicting results, with other papers finding no differences in performance across the menstrual cycle. None test anything to do with inheritance, none try (or even can) look at the genetic basis of the behaviors they are studying. Yet somehow evolutionary psychologists conclude that “women may have been selected during human evolution to behave in ways that reduce the likelihood of conception as a consequence of rape.”

Another way to look at it is that they are hypothesizing that women are more likely to behave in ways that invite physical attack and brutal abuse when they aren’t ovulating. That is a remarkable assertion. It also carries the strange implication that the consequences of rape can be measured by the likelihood of immediate fertilization, rather than by the toll of physical injury and emotional trauma, a peculiar thing for psychologists to neglect. Wouldn’t it make more sense to have a general hypothesis that people, men and women, who can avoid violence at any time in their life, are more likely to be reproductively successful and thereby pass on their genes to subsequent generations? That’s all they’re saying, essentially, and the straining to sex it up by tying globally useful behaviors to reproductive cycles is unconvincing.

And of course they’re looking at culturally conditioned behaviors and responses in a narrow subset of the modern human population. How likely is it that a close-knit tribe of 30 hunter-gatherers has a serious problem with rape? Wouldn’t the nature of the culture be of far greater effect in determining the frequency of pregnancy due to rape than variations in handgrip strength or variations in fearfulness in women?

Then many of the studies that are described with such enthusiastic certainty as having definitive results turn out to be subjective, pointless messes. For instance, Jesse Bering concludes that sperm competition had to have been a very significant factor in our profligately promiscuous ancestors, and that the shape of the human penis has been selected specifically for a function in extracting competitor’s sperm from the vaginal canal. Unfortunately, when you look at the actual research cited for this semen-scooping function, it’s underwhelming.

To test this hypothesis, Gallup, Burch, Zappieri, Parvez, Stockwell, and Davis (2003) simulated sexual encounters using artificial models and measured the magnitude of artificial semen displacement as a function of phallus configuration, depth of thrusting, and semen viscosity. The displacement of simulated semen was robust across different prosthetic phalluses, different artificial vaginas, different semen recipes, and different semen viscosities. The magnitude of semen displacement was directly proportional to the depth of thrusting and inversely proportional to semen viscosity. By manipulating different characteristics of artificial phalluses, the coronal ridge and frenulum were identified as key
morphological features involved in mediating the semen displacement effect.

Under conditions that raise the possibility of females engaging in extra-pair copulations (i.e., periods of separation from their partner, allegations of female infidelity), Gallup et al. (2003) also found that males appear to modify the use of their penis in ways that are consistent with the displacement hypothesis. Based on anonymous surveys of over 600 college students, many sexually active males and females reported deeper and more vigorous thrusting when in-pair sex occurred
under conditions related to an increased likelihood of female infidelity.

Got that? They have studies that show that a piston displaces fluids more effectively in proportion to the depth of movement, and that college students report that when they suspect their partner of infidelity, they screw harder. They don’t have any evidence that this behavior actually affects the fertilization rate of one partner’s sperm over another, they don’t have any indication of morphological differences in human populations that make some individuals better semen-scoopers, they don’t have any evidence that this behavior has had a differential effect in human history. It’s all a teetering pyramid of stacked “couldas” and guesses that it woulda had an influence on evolution, if there were any variation and heritable factors involved in this function.

Whenever I see this kind of tripe from evolutionary psychologists, I reflexively reach for a counter-example, and recommend that everyone read one excellent book: The Case of the Female Orgasm: Bias in the Science of Evolution, by Elisabeth Lloyd. It’s a wonderful example of solid, rigorous, scientific thinking about an evolutionary phenomenon. Lloyd analyzes a score of adaptive just-so stories about the female orgasm, carefully scrutinizing the evidence for each, and discovers that the substance is wanting. Too often investigators start with the assumption that a feature absolutely must have been selected for, or it wouldn’t be there, and then contrive elaborate rationalizations for processes that could have favored its preservation in our ancestry…and the aura of plausibility is then sufficient to conclude that it must be so, even in the absence of any supporting evidence, and sometimes even in the face of contradictory evidence.

I should reread it now — if nothing else, to wash that nasty tincture of evolutionary psychology out of my brain.