Modules and the promise of the evo-devo research program

Since Evolgen recognizes the importance of evo-devo, I’ll return the favor: bioinformatics is going to be critical to the evo-devo research program, which to date has emphasized the “devo” part with much work on model systems, but is going to put increasing demands on comparative molecular information from genomics and bioinformatics to fulfill the promise of the “evo” part. I’m sitting on a plane flying east, and to pass the time I’ve been reading a very nice review of the concept of modularity in evo-devo by Paula Mabee (also a fish developmental biologist, and also working in a small college in a small town in the midwest…but rather deservedly better known than yours truly). In addition to summarizing the importance of the concept of modularity to evolution and development, the paper also does something I always appreciate: it summarizes the key questions that the modern evo-devo research program is working to answer.

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A brief overview of Hox genes

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In previous articles about fly development, I’d gone from the maternal gradient to genes that are expressed in alternating stripes (pair-rule genes), and mentioned some genes (the segment polarity genes) that are expressed in every segment. The end result is the development of a segmented animal: one made up of a repeated series of morphological modules, all the same.

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Building an animal with repeated elements like that is a wonderfully versatile strategy for making an organism larger without making it too much more complicated, but it’s not the whole story. Just repeating the same bits over and over again is a way to make a generic wormlike thing—a tapeworm, for instance—but even tapeworms may need to specialize certain individual segments for specific functions. At its simplest, it may be necessary to modify one end for feeding, and the opposite end for mating. So now, in addition to staking out the tissues of the embryo as belonging to discrete segments, we also need a mechanism that says “build mouthparts here (and not everywhere)”, and “put genitalia here (not over there)”.

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Evo-Devo in NYR Books!

This really is an excellent review of three books in the field of evo-devo—

From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design (amzn/b&n/abe/pwll),

Endless Forms Most Beautiful: The New Science of Evo Devo and the Making of the Animal Kingdom (amzn/b&n/abe/pwll), and

The Plausibility of Life:Resolving Darwin’s Dilemma (amzn/b&n/abe/pwll)—all highly recommended by me and the NY Times. The nice thing about this review, too, is that it gives a short summary of the field and its growing importance.

Evolving spots, again and again

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a–c, The wing spots on male flies of the Drosophila genus. Drosophila tristis (a) and D. elegans (b) have wing spots that have arisen during convergent evolution. Drosophila gunungcola (c) instead evolved from a spotted ancestor. d, Males wave their wings to display the spots during elaborate courtship dances.

It’s all about style. When you’re out and about looking for mates, what tends to draw the eye first are general signals—health and vigor, symmetry, absence of blemishes or injuries, that sort of thing—but then we also look for that special something, that je ne sais quoi, that dash of character and fashionable uniqueness. In humans, we see the pursuit of that elusive element in shifting fashions: hairstyles, clothing, and makeup change season by season in our efforts to stand out and catch the eye in subtle ways that do not distract from the more important signals of beauty and health.

Flies do the same thing, exhibiting genetic traits that draw the attention of the opposite sex, and while nowhere near as flighty as the foibles of human fashion, they do exhibit considerable variability. Changes in body pigmentation, courtship rituals, and pheromones are all affected by sexual selection, but one odd feature in particular is the presence of spots on the wing. Flies flash and vibrate their wings at prospective mates, so the presence or absence of wing spots can be a distinctive species-specific element in their evolution. One curious thing is that wing spots seem to be easy to lose and gain in a fly lineage, and species independently generate very similar pigment spots. What is it about these patterns that makes them simultaneously labile and frequently re-expressed?

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Evolving spots

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Here’s what seems to be a relatively simple problem in evolution. Within the Drosophila genus (and in diverse insects in general), species have evolved patterned spots on their wings, which seem to be important in species-specific courtship. Gompel et al. have been exploring in depth one particular problem, illustrated below: how did a spot-free ancestral fly species acquire that distinctive dark patch near the front tip of the wing in Drosophila biarmipes? Their answer involves dissecting the molecular regulators of pattern in the fly wing, doing comparative sequence analyses and identifying the specific stretches of DNA involved in turning on the pigment pattern, and testing their models experimentally by expressing novel gene constructs in different species of flies.

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Chance and regularity in the development of the fly eye

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What has always attracted me to developmental biology is the ability to see the unfolding of pattern—simplicity becomes complexity in a process made up of small steps, comprehensible physical and chemical interactions that build a series of states leading to a mostly robust conclusion. It’s a bit like Conway’s Game of Life in reverse, where we see the patterns and can manipulate them to some degree, but we don’t know the underlying rules, and that’s our job—to puzzle out how it all works.

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Another fascinating aspect of development is that all the intricate, precise steps are carried out without agency: everything is explained and explainable in terms of local, autonomous interactions. Genes are switched on in response to activation by proteins not conscious action, domains of expression are refined without an interfering hand nudging them along towards a defined goal. It’s teleonomy, not teleology. We see gorgeously regular structures like the insect compound eye to the right arise out of a smear of cells, and there is no magic involved—it’s wonderfully empowering. We don’t throw up our hands and declare a miracle, but instead science gives us the tools to look deeper and work out (with much effort, admittedly) how seeming miracles occur.

One more compelling aspect of development: it’s reliable, but not rigid. Rather than being simply deterministic, development is built up on stochastic processes—ultimately, it’s all chemistry, and cells changing their states are simply ping-ponging through a field of potential interactions to arrive at an equilibrium state probabilistically. When I’d peel open a grasshopper embryo and look at its ganglia, I’d have an excellent idea of what cells I’d find there, and what they’d be doing…but the fine details would vary every time. I can watch a string of neural crest cells in a zebrafish crawl out of the dorsal midline and stream over generally predictable paths to their destinations, but the actions of an individual melanocyte, for instance, are variable and beautiful to see. We developmental biologists get the best of all situations, a generally predictable pattern coupled to and generated by diversity and variation.

One of the best known examples of chance and regularity in development is the compound eye of insects, shown above, which is as lovely and crystalline as a snowflake, yet is visibly assembled from an apparently homogenous field of cells in the embryo. And looking closer, we discover a combination of very tight precision sprinkled with random variation.

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Warring sexes

Both Twisty and Amanda seem a bit weirded out by this news that the fetus can be viewed as a kind of parasite. This story has been around long enough that a lot of us just take it for granted—I wrote about the example of preeclampsia a while back.

There are worse feminist-troubling theories out there, though. In particular, there is the idea of intersexual evolutionary conflict and male-induced harm. In species where there is some level of promiscuity, it can be to the male’s evolutionary advantage to compel his mate to a) invest more effort in his immediate progeny, b) increase her short-term reproduction rate, and c) suppress her ability to mate with other males. After all, his optimal strategy is to flit from female to female, copulate, and put her to work producing his offspring. The female’s preferred strategy, on the other hand, is to take her time, maximize her lifetime reproduction rate, and select the best genetic endowment for her children.

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This sets up a cycle of counter-adaptations in the population. If a male acquires a mutation that increases his fitness at the expense of his mate’s—for instance, if some component of his semen works on her brain to suppress her interest in remating—it will spread through the population due to its positive effect on male fitness, even though it reduces female fitness. Subsequently, a female who acquired a counter-adaptive resistance to the male’s hormonal sabotage would have an advantage, and that gene would spread through the population, reducing male fitness by making them less capable of controlling female reproduction. Then, of course, males could evolve some other sneaky way of maximizing their reproduction rate—vaginal plugs, secretions that make the mated female unattractive to other males, proteins that put her ovaries into overdrive to produce more eggs now at the expense of the female’s long term survival.

It all sounds improbable and dystopian, but all of these mechanisms and more have been observed in that exceptionally promiscuous species, Drosophila. Drosophila seminal fluid has the property of reducing the female’s interest in remating, increasing her rate of egg-laying, and is also mildly toxic. Artificial selection in the lab can produce females that are resistant to the effects, and males that produce more and more potent semen to overcome their resistance, to the point where the line of “super potent” males, when crossed to unselected females, kill their partners with their ejaculations. There is literally a battle of the sexes in these species.

To speak up in my defense, though, not all males are evil exploitive pigs. The logic of this pattern of sexual competitiveness vanishes as species exhibit greater and greater monogamy—if you have only one mate, it is to your advantage to take good care of him or her, because a loss diminishes your reproductive fitness.

Rice WR (2000) Dangerous Liaisons. Proc. Nat. Acad. Sci. USA 97(24):12953-12955.

Rice WR (1996) Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381(6579):189-90.

Snuppy is a real clone!

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Remember Snuppy, the cloned puppy? He’s been living under a cloud for a while now, since one of his creators was Woo-Suk Hwang, the Korean scientist who was found to have faked data and exploited his workers, and there was concern that perhaps the dog cloning experiment was also tainted.

Put those fears to rest. Two groups of researchers have independently analyzed Snuppy and its putative clone parent, and both agree that it is most likely a clone. The nuclear markers between the two were identical, while mitochondrial markers were different—exactly what you’d expect in this kind of clone, and not what you’d see from simple twins, for instance, or if someone had faked the samples.

Parker HG, Kruglyak L, Ostrander EA (2006) DNA analysis of a putative dog clone. Nature 440:E1-E2.

Seoul National University Investigation Committee, Lee JB, Park C (2006) Verification that Snuppy is a clone. Nature 440:E2-E3.

PZ Myers’ Own Original, Cosmic, and Eccentric Analogy for How the Genome Works -OR- High Geekology

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I’m teaching my developmental biology course this afternoon, and I have a slightly peculiar approach to the teaching the subject. One of the difficulties with introducing undergraduates to an immense and complicated topic like development is that there is a continual war between making sure they’re introduced to the all-important details, and stepping back and giving them the big picture of the process. I do this explicitly by dividing my week; Mondays are lecture days where I stand up and talk about Molecule X interacting with Molecule Y in Tissue Z, and we go over textbook stuff. I’m probably going too fast, but I want students to come out of the class having at least heard of Sonic Hedgehog and β-catenin and fasciclins and induction and cis regulatory elements and so forth.

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Life will find a way

Creationists sometimes try to argue that what we consider straightforward, well-demonstrated cytological and genetic events don’t and can’t occur: that you can’t get chromosome rearrangements, or that variations in chromosome number and organization are obstacles to evolution, making discussions of synteny, or the rearrangement of chromosomal material in evolution, an impossibility. These are absurd conclusions, of course—we see evidence of chromosomal variation in people all the time.

For example, A friend sent along (yes, Virginia, there is a secret network of evilutionists busily sharing information with one another) a remarkable case study of a radical chromosome arrangement in a mother and daughter. When you see how these chromosomes are scrambled, you’ll wonder how they ever managed to sort themselves out meiotically to produce viable offspring…but life will find a way.

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