Deficiencies in modern evolutionary theory

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This is a post originally made on the old Pharyngula website; I’ll be reposting some of these now and then to bring them aboard the new site.

There are a number of reasons why the current theory of evolution should be regarded as incomplete. The central one is that while “nothing in biology makes sense except in the light of evolution”, some important disciplines within biology, development and physiology, have only been weakly integrated into the theory.

Raff (1996) in his book The Shape of Life(amzn/b&n/abe/pwll) gives some of the historical reasons for the divorce of evolution and development. One is that embryologists were badly burned in the late 19th century by Haeckel, who led them along the long and unproductive detour of the false biogenetic “law”. That was a negative reaction; there was also a positive stimulus, the incentive of Roux’s new Entwicklungsmechanik, a model of experimental study of development that focused exclusively on immediate and proximate causes and effects. Embryology had a Golden Age of experimentation that discouraged any speculation about ultimate causes that just happened to coincide with the time that the Neo-Darwinian Synthesis was being formulated. Another unfortunate instance of focusing at cross-purposes was that the Neo-Darwinian Synthesis was fueled by the incorporation of genetics into evolutionary biology…and at the time, developmental biologists had only the vaguest ideas about how the phenomena they were studying were connected to the genome. It was going to be another 50 years before developmental biology fully embraced genetics.

The evolutionary biologists dismissed the embryologists as irrelevant to the field; furthermore, one of the rare embryologists who tried to address evolutionary concerns, Richard Goldschmidt, was derided as little more than a crackpot. It’s an attitude that persists today. Of course, the problem is mutual: Raff mentions how often he sees talks in developmental genetics that end with a single slide to discuss evolutionary implications, which usually consist of nothing but a sequence comparison between a couple of species. Evolution is richer than that, just as development is much more complex and sophisticated than the irrelevant pigeonhole into which it is squeezed.

In her book, Developmental Plasticity and Evolution(amzn/b&n/abe/pwll), West-Eberhard (2003) titles her first chapter “Gaps and Inconsistencies in Modern Evolutionary Thought”. It summarizes the case she makes in the rest of her 700 page book in 20 pages; I’ll summarize her summary here, and do it even less justice.

She lists 6 general problems in evolutionary biology that could be corrected with a better assimilation of modern developmental biology.

  1. The problem of unimodal adaptation. You can see this in any textbook of population genetics: the effect of selection is to impose a gradual shift in the mode of a pattern of continuous variation. Stabilizing selection chops off both tails of the distribution, directional selection works against one or the other tail, and disruptive selection favors the extremes. This is a useful, productive simplification, but it ignores too much. Organisms are capable of changing their specializations either physiologically, in the form of different behaviors, morphologies, or functional states, developmentally in the form of changing life histories, or behaviorally. Evolution is too often a “theory of adults”, and rather unrealistically inflexible adults at that.
  2. Cohesiveness. There is a long-standing bias in the evolutionary view of development, that of development imposing constraints on the organism. We can see that in the early favor of ideas like canalization, and the later vision of the gene pool as being cohesive and coadapted, which limits the magnitude of change that can be permitted. It’s a view of development as an exclusively conservative force. This is not how modern developmental biologists view the process. The emerging picture is one of flexibility, plasticity, and modularity, where development is an innovative force. Change in developmental genes isn’t destructive—one of the properties of developmental systems is that they readily accommodate novelty.
  3. Proximate and ultimate causation. One of the radical secrets of Darwin’s success was the abstraction of the process away from a remote and unaccessible ultimate teleological cause and to a more approachable set of proximate causes. This has been a good strategy for science in general, and has long been one of the mantras of evolutionary biology. Organisms are selected in the here and now, and not for some advantage many generations down the line. Evolutionary biology seems to have a blind spot, though. The most proximate features that affect the fitness of an organism are a) behavioral, b) physiological, and c) developmental. These are the causes upon which selection can act, yet the focus in evolutionary biology has been on an abstraction at least once removed, genetics.
  4. Continuous vs. discrete change. This is an old problem, and one that had to be resolved in a somewhat unsatisfactory manner in order for Mendelian genetics (an inherently discrete process) to be incorporated into neo-Darwinian thought (where gradualism was all). Many traits can be dealt with effectively by quantitative genetics, and are expressed in a graded form within populations, and these are typically the subject of study by population geneticists. We often see studies of graded phenotypes where we blithely accept that these are driven by underlying sets of graded distributions of genes, such as the studies of Darwin’s finches by the Grants, yet those genes are unidentified. Conversely, the characters that taxonomists use to distinguish species are usually qualitatively distinct are at least abruptly discontinuous. There is a gap in our thinking about these things, a gap that really requires developmental biology. Wouldn’t it be useful to know the molecular mechanisms that regulate beak size in Darwin’s finches?
  5. Problematic metaphors. One painful thing for developmental biologists reading the literature of evolutionary biology is the way development is often reduced to a metaphor, and usually it is a metaphor that minimizes the role of development. West-Eberhard discusses the familiar model of the “epigenetic landscape” by Waddington, which portrays development as a set of grooves worn in a flat table, with the organism as a billiard ball rolling down the deepest series. This is a model that completely obliterates the dynamism inherent in development. Even worse, because it is the current metaphor that seems to have utterly conquered the imaginations of most molecular biologists, is the notion of the “genetic program”. Again, this cripples our view of development by removing the dynamic and replacing it with instructions that are fixed in the genome. This is bad developmental biology, and as we get a clearer picture of the actual contents of the genome, it is becoming obviously bad molecular biology as well.
  6. The genotype-phenotype problem. Listen to how evolutionary explanations are given: they are almost always expressed in the language of genes. Genes, however, are a distant secondary or tertiary cause of evolutionary solutions. Fitness is a collective product of success at different stages of development, of different physiological adaptations, and of extremely labile interactions with the environment. Additionally, a gene alone is rarely traceable as the source of an adaptive state; epigenetic interactions are paramount. We are rarely going to be able to find that a specific allele has a discrete adaptive value. It’s always going to be an allele in a particular genetic background in a particular environment with a particular pattern of expression at particular stages of the life history.

One unfortunate problem with discussing these issues in venues frequented by lay people is, you guessed it, creationism. Any criticism of a theory is seized upon as evidence that the theory is wrong, rather than as a sign of a healthy, growing theory. The Neo-Darwinian Synthesis is not wrong, but neither is it dogma. It was set up roughly 70 years ago with the knowledge that was available at the time, and it is not at all surprising that the explosion of new knowledge, especially in molecular biology, genetics, and developmental biology, means that there are radically different new ideas clamoring to be accommodated in the old framework. The theory is going to change. This isn’t cause for creationists to rejoice, though, because the way it is changing is to become stronger.

Textbook vs. Frontier

The Hwang Woo Suk stem cell research scandal has triggered quite a bit of concerned introspection in the scientific community. Orac has some useful comments on a good article in the NY Times that makes the distinction between “frontier science” and “textbook science”, where much of the current stem cell research is clearly on the frontier.

Much of science at the very frontiers turns out not to be correct. However, the way it is all too often reported in the press is that it is correct. We in science understand the difference between textbook science and the sort of frontier science that makes it into journals like Science. Indeed, we often lament that the very highest tier journals, such as Nature, Science, and Cell, tend to be too enamored of publishing what seems to be “sexy science,” exciting or counterintuitive results that really grab the attention of scientists–in other words “cutting edge” or frontier science. Such journals seem to pride themselves on publishing primarily such work, while more solid, less “sexy” results seem to end up in second-tier journals, which is why they are so widely read and cited.

I would add another factor, though: Hwang Woo Suk’s results were not at all unexpected, did not contradict any accepted scientific concepts, and were dramatic because they represented a methodological breakthrough. In a way, it was almost a “safe” category in which to cheat: lots of people are trying to transform adult cell nuclei into totipotent stem cells, it looks like a problem that’s just going to require a lot of trial-and-error hammering to resolve, and what Dr Hwang did was steal priority on a result he could anticipate would be “replicated” (or more accurately, done for the first time) in short order. This is one of the hardest categories of science to police, I would think. It’s frontier science all right, but it’s only one step beyond the textbook.

Orac’s comments about those sexy hot scientific results that get into the top-ranked journals also applies to weblogs. I’m guilty of the same thing: the articles I tend to summarize here are the ones that push at the edges of what we know, rather than the ones that consolidate what we already knew, which actually represent the majority of what I read. The solid stuff that is packed with gobs of detailed data on expression patterns of a single gene, for instance, is hard to make exciting to a general audience—when the conclusion of a long paper is that Hox1 represses transcription of Pax1/9 in the endoderm, it takes an awful lot of background exposition to try and make that interesting.

For the creationists out there, by the way, most of evolutionary biology is solidly in the “textbook science” category, which is one of the reasons biologists are so baffled about why the general public embraces criticisms of it.

Orsten fossils

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Bredocaris admirabilis

Ooooh, there’s a gorgeous gallery of Orsten fossils online. These are some very pretty SEMs of tiny Cambrian animals, preserved in a kind of rock called Orsten, or stinkstone (apparently, the high sulfur content of the rock makes it smell awful). What are Orsten fossils?

Orsten fossils in the strict sense are spectacular minute secondarily phosphatised (apatitic) fossils, among them many Crustacea of different evolutionary levels, but also other arthropods and nemathelminths. The largest fragments we have do not exceed two mm. Orsten-type fossils, on the other hand, have the great advantage in being three-dimensionally preserved with all surface structures in place and thus easier to interpret than any other fossil material. Orsten fossils are preserved virtually as if they were just critical-point dried extant organisms. Details observable range down to less than 1 µm, and include pores, sensilla and minute secondary bristles on filter setae and denticles. Orsten fossils also give an insight of meiofaunal benthic life at small scale, including preservation larval stages, and hence a life zone inhabited by the earliest metazoan elements of the food chain.

It’s a good browse over there. I think it’s useful to remember that the majority of the fauna of the world both extant and half a billion years ago is and was tiny and unfamiliar.

Department of Provocative Imagery

OK, that settles it. I’m in the wrong research field.

They found breasts moved in a 3D figure of eight and that uncontrolled movement strained fragile tissues and ligaments.

The study suggested as a woman runs a mile, her breasts bounced 135 meters.

The report found each breast moved independently of the body by an average of 9cm for every step taken on the treadmill.

With the average breast weighing between 200 and 300 grams, this movement puts great stress on the breast’s fragile support structure—the outer skin and connective tissues known as Cooper’s ligaments.

I suspect the analysis was…mesmerizing.

The wording was a little unfortunate—I pictured the subject dribbling a pair like basketballs as she runs.

(via Matt Dowling)

Hemichordate evo-devo

Every biology student gets introduced to the chordates with a list of their distinctive characteristics: they have a notochord, a dorsal hollow nerve cord, gill slits, and a post-anal tail. The embryonic stage in which we express all of these features is called the pharyngula stage—it’s often also the only stage at which we have them. We terrestrial vertebrates seal off those pharyngeal openings as we develop, while sea squirts throw away their brains as an adult.

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The chordate phylum has all four of those traits, but there is another extremely interesting phylum that has some of them, the hemichordates. The hemichordates are marine worms that have gill slits and a stub of a tail. They also have a bundle of nerves in the right place to be a dorsal nerve cord, but the latest analyses suggest that it’s not discrete enough to count—they have more of a diffuse nerve net than an actual central nervous system. They don’t really have a notochord, but they do have a stiff array of cells in their proboscis that vaguely resembles one. They really are “half a chordate” in that they only partially express characters that are defining elements of the chordate body plan. Of course, they also have a unique body plan of their own, and are quite lovely animals in their own right. They are a sister phylum to the chordates, and the similarities and differences between us tell us something about our last common ancestor, the ur-deuterostome.

Analyzing morphology is one approach, but this is the age of molecular biology, so digging deeper and comparing genes gives us a sharper picture of relationships. This is also the early days of evo-devo, and an even more revealing way to examine related phyla is to look at patterns of gene regulation—how those genes are turned on and off in space and time during the development of the organism—and see how those relate. Gerhart, Lowe, and Kirschner have done just that in hemichordates, and have results that strengthen the affinities between chordates and hemichordates. (By the way, Gerhart and Kirschner also have a new book out, The Plausibility of Life (amzn/b&n/abe/pwll), which I’ll review as soon as I get the time to finish it.)

[Read more…]

Firefly squid

This is a beautiful little animal with a brief and brilliant life.

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Watasenia scintillans is a small (mantle length,~6 cm; wet weight,~9 g), luminescent deep-sea squid, indigenous to northern Japan. Females carrying fertilized eggs come inshore each spring by the hundreds of millions, even a billion, to lay eggs in Toyama Bay (max. depth, 1200 m) and die, thereupon completing a 1-year life cycle.

Watasenia possesses numerous (~800), minute dermal light organs (photophores) on its ventral side. Other organs are scattered over the head, funnel, mantle, and arms, but none is found on its dorsal side. There are five prominent organs beneath the lower margin of each eye. They all emit a bluish light. A cluster of three tiny black-colored organs (<l mm diam) is located at the tip of each of the fourth pair of arms. They emit brilliant flashes of light which are clearly visible to the unaided eye even in a lighted room. Some of the flashes have a cadence resembling that of a terrestrial firefly flashing at night, and thus the squid is known in Japan as the “firefly squid” or “hotaru-ika.”

A billion die every year as a natural part of their lifecycle; all those glittering little creatures dying profligately—Nature is both exuberant and pitiless, it seems.

Tsuji FI (2005) Role of molecular oxygen in the bioluminescence of the firefly squid, Watasenia scintillans. Biochem Biophys Res Commun. 338(1):250-253.