Douglas Futuyma—Evolutionary Ecology and the Question of Constraints

I have wireless access in the lecture hall today, so I’m going to try liveblogging these talks. This may get choppy! What it will lack in editing will be compensated for by more timely and regular updates. I hope. At least I’ll be able to dump something to the site every 40-60 minutes.

He summarizes the idea that there is a wealth of genetic diversity in populations to allow for effective selection. Lack of mutations should not limit a straightforward selection response. This raises a paradox, however: organisms have phylogenetic niche conservatism. Many species are evolutionarily unadventurous. He works on clades of herbivorous insect species that are sticking to the same plant groups since the Miocene.

May be many niches in nature that are unfilled: example: fish-catching bats have only one species. Where are the nocturnal aerial fish-feeders in other environments? Species don’t just liberally fill every possibility.

Futuyma introduces Gould/Eldredge’s concept of stasis. We need to acknowledge the existence of constraints that are limiting factors on evolutionary possibilities.

Genetic constraints:

In some cases, a “character” doesn’t exist — there aren’t genes or developmental pathways that specify it. For example, thoracic bristle number in flies may not be defined by simple genetic programs. Haldane said humans will not evolve into angels because we lack the required genetic diversity in wings or moral character.

Little or no genetic variance in a character or combination of characters. Looked at Ophraella beetles, asking whether genetic predispositions might limit which species of plants they can feed on. Screened for genetic variation; in about half the cases they found no evidence of genetic variation that would allow for expansion into distantly related plant species. Discussed Bradshaw’s work on genostasis in evolution, which found little genetic variance in heavy metal tolerance in grasses, dessication resistance in rainforest flies, locomotor and life history traits in Hyla. Adaptation observed in some fly species may have been facilitated by hybridization, which introduces the needed variation.

Species evolve along lines of genetic least resistance, where variation is present in the population. Other directions may not be easily followed.

Successful genetic change may require correlated change in multiple other traits, so genetic diversity may hinder evolutionary change by making the optimal combinations rare in the population. Demanding simultaneous changes in larval and adult characters, for instance, might limit rates of change.

Major issue: how much evolutionary novelty is due to new mutations vs. recombination of standing variation in a population?

What accounts for stasis? Most adaptive novelties are associated with shifts to new niches. Because of recombination, new constellations of characters are likely to be ephemeral and not appear in the fossil record — we don’t see them because of issues in population structure. Adaptive gene combinations will be diluted by interbreeding with individuals that lack the combination, so novelties are unlikely to spread very far (unless it’s also associated with reproductive isolation).

During the glacial periods, most species did not adapt to new environments — they used habitat tracking to follow favorable environments. Recombination with more abundant ancestral genotypes leads to collaps of population structures that might favor new forms. Subpopulations lose their character when merged with larger populations, so reproductive isolation is important.

Interesting prediction: ought to be more stasis in times of environmental fluctuation, and more expansion of novelties in subpopulations in times of environmental stability.. Adaptation to rapid environmental change may fail, especially if multiple character changes are required, and extinction is not unllkely. Climate change may simply doom many species. Adaptation to other invasive species is also going to be slow. And many adaptations may be unlikely and evolve only rarely.

Once upon a time, biologists like the idea of convergence — that similar populations might arise in similar environments (I’m thinking of Simon Conway Morris here), but communities are dependent on contingency in evolutionary history, and a deterministic, equilibrial view of ecological “communities” can no longer be supported.

We are seeing a major shift in the discipline to the importance of constraint and evolvability, and the origin of variation. History is important. and there’s increasing integration of disciplines to cover micro- and macro-evolution.

Richard Lewontin—Genetic Determination and Adaptation: Two Bad Metaphors

It was a fine evening here in Chicago, with all these superstars of evolutionary biology in attendance. It was also an information-dense evening — I tried to keep up on my little laptop, but I know I missed a lot. Fortunately, I’m not alone: Rob Mitchum and Jeremy Manier were also covering the event, and have a play-by-play available. I’ll just dump what I’ve got here tonight. I do have wi-fi passwords so I can get things up a little more promptly tomorrow and Saturday.

Richard Lewontin opened up with a few deprecatory comments about the religiosity of our surroundings (the talks were given in a chapel) and our purpose, the reverence given to Saint Darwin. He was there to talk about the importance and danger of metaphors, and addressed two of them. The New Testament metaphor of genes make organisms, and the Old Testament metaphor that organisms adapt to the environment.

It’s not true that genes make organisms. Organisms are consequence of interactions between inside and outside, genes and molecules, and the phenotype is not predictable from the genotype. He discussed the classic example of norms of reaction in Achillea, showing growth of clones in different environments. Cloned plants taken from cuttings — so they’re genetically identical — and grown in different environments show different patterns of growth, and, for instance, don’t show a simple relationship between morphology and the elevation at which they’re grown. Another example is bristle number in Drosophila which show similar unpredictable pattern of response to temperature. Another thing to think about: look at the fingerprints on your left and right index fingers. They’re not identical, but they have the same genes and formed in the same environment at the same time. Living organisms are the outcome of developmental and physiological processes influenced four factors: genes, non-genic molecules in the embryo, environment, and random variation.
Biologists have known this for years but have fallen prey to the metaphor of genetic determinism. (He also mentioned another bad metaphor as an aside: the cell as a machine.)

The other bad bad metaphor is the idea that organisms adapt to ecological niches. Organisms do not fit into preexisting niches. You can’t look at “niches” in the environment…there are an infinity of them. The organism determines the niche. A better idea is the concept of niche construction, in which niches change as organisms evolve. Organisms take whats available and integrate it with their biology, and the life activities of organisms determine what is relevant. When did living in water become the niche of the ancestral seal?

Organisms seek out appropriate environments, the idea of microclimate. Put mesic (adapted to environments with a moderate amount of moisture) and xeric (dry or desert) flies in evironments with different zones of humidity, one surprising result is that the xeric flies move most quickly and determinedly to moist areas, more so than mesic flies. It’s not that dry-adapted flies can handle dryness better…it’s that they’re better at finding damp microenvironments.

Lewontin gave several other examples of organisms that respond in sophisticated ways to confound simple interpretations of adaptation: that we all produce shells of altered microenvironments around us by our metabolic activity; that trees can count the number of days of a certain temperature to trigger flowering; that Daphnia measure the rate of environmental change to determine whether to reproduce sexually or asexually; that organisms modulate the statistical properties of their environment by storage.

He suggested that we need to set aside the bad metaphor of adaptation for a less bad metaphor of construction. Unfortunately, this creates a difficult situation for scientists interested in selection, because, for instance, frequency dependent selection means that the addition of new genotypes to the gene pool (which happens constantly) causes fitness to change in unpredictable ways. It’s a game of rock-paper-scissors with a lot more than just three possibilities. He closed by saying that addressing this kind of problem should be the goal of the next generation of evolutionary biologists.

I ♥ sabbaticals

Why? Because Jerry Coyne can mention this amazing conference, I can take a look at the luminaries speaking at it, and decide at the drop of a hat that I’m going. So this weekend, I’ll be spending my Halloween at a major conference on evolution. Yay!

Look forward to lots of liveblogging (I hope…if they have wi-fi in the conference halls. If not, there will be some massive data dumps in the evenings.)

The ups and downs of radio

Yesterday, I got a brief mention of a botch of a radio show on NPR that nattered on about a “deep rift” in atheism, but this morning on MPR you could have heard Richard Dawkins talking about evolution. He got the better gig.

This interview does make clear one difference in strategy between Dawkins and myself. The interviewer tries to hammer him on being less than respectful to religious believers, and Dawkins is always polite and tries his best to downplay the conflict. In a similar situation, I’d simply say, “Yes, I am openly contemptuous of religious belief. You want to make something of it?”

I guess I’m meaner than Dawkins.

Uh-oh! Deep rift, deep rift, DEEP RIFT!

Mismatch of the decade: Thornton vs. Behe

One of my favorite examples of the step-by-step evolution of molecules has been the work coming out of Joe Thornton’s lab on glucocorticoid receptors. It’s marvelous stuff that nails down the changes, nucleotide by nucleotide.

It’s also work that Michael Behe called “piddling”, despite the fact that it directly addresses the claims of irreducible complexity. Have you ever noticed how the creationists will make grand demands (show me how a duck evolved from a crocodile!) and then reject every piece of fossil evidence you might show them because there are still “gaps”? This is the converse of that argument: when you’ve got a system where you can show each tiny molecular/genetic change, they dismiss that as trivial. You really can’t win.

Well, Thornton has been working hard and coming up with more and more details, while Behe is still sitting there, eyes clamped shut and ears stoppered, insisting that IT CAN’T HAPPEN LALALALAALALALALAAAA. Behe threw together some dreck claiming that not only didn’t Thornton’s work demonstrate evolution, but it actually supported Intelligent Design creationism!

Boy, did he make a mistake.

Remember how when the creationists started playing games with his work, it roused Richard Lenski to slap down Conservapædia hard? We’ve got a similar situation here.

Joe Thornton has written a beautiful response to Michael Behe.

Read it. Really. It’s a whole lesson in important principles in evolutionary theory all by itself. It exposes the ignorance of Behe through and through, and demolishes the premises of Behe’s latest foolish book. And it made me feel soooo gooooood.

Jonathan Wells gets everything wrong, again

I was just catching up on a few blogs, and noticed all this stuff I missed about Jonathan Wells’ visit to Oklahoma. And then I read Wells’ version of the event, and just about choked on my sweet mint tea.

The next person–apparently a professor of developmental biology–objected that the film ignored facts showing the unity of life, especially the universality of the genetic code, the remarkable similarity of about 500 housekeeping genes in all living things, the role of HOX genes in building animal body plans, and the similarity of HOX genes in all animal phyla, including sponges. 1Steve began by pointing out that the genetic code is not universal, but the questioner loudly complained that 2he was not answering her questions. I stepped up and pointed out that housekeeping genes are similar in all living things because without them life is not possible. I acknowledged that HOX gene mutations can be quite dramatic (causing a fly to sprout legs from its head in place of antennae, for example), but 3HOX genes become active midway through development, 4long after the body plan is already established. 5They are also remarkably non-specific; for example, if a fly lacks a particular HOX gene and a comparable mouse HOX gene is inserted in its place, the fly develops normal fly parts, not mouse parts. Furthermore, 6the similarity of HOX genes in so many animal phyla is actually a problem for neo-Darwinism: 7If evolutionary changes in body plans are due to changes in genes, and flies have HOX genes similar to those in a horse, why is a fly not a horse? Finally, 8the presence of HOX genes in sponges (which, everyone agrees, appeared in the pre-Cambrian) still leaves unanswered the question of how such complex specified genes evolved in the first place.

The questioner became agitated and shouted out something to the effect that HOX gene duplication explained the increase in information needed for the diversification of animal body plans. 9I replied that duplicating a gene doesn’t increase information content any more than photocopying a paper increases its information content. She obviously wanted to continue the argument, but the moderator took the microphone to someone else.

It blows my mind, man, it blows my freakin’ mind. How can this guy really be this stupid? He has a Ph.D. from UC Berkeley in developmental biology, and he either really doesn’t understand basic ideas in the field, or he’s maliciously misrepresenting them…he’s lying to the audience. He’s describing how he so adroitly fielded questions from the audience, including this one from a professor of developmental biology, who was no doubt agitated by the fact that Wells was feeding the audience steaming balls of rancid horseshit. I can’t blame her. That was an awesomely dishonest/ignorant performance, and Wells is proud of himself. People should be angry at that fraud.

I’ve just pulled out this small, two-paragraph fragment from his longer post, because it’s about all I can bear. I’ve flagged a few things that I’ll explain — the Meyer/Wells tag team really is a pair of smug incompetents.

1The genetic code is universal, and is one of the pieces of evidence for common descent. There are a few variants in the natural world, but they are the exceptions that prove the rule: they are slightly modified versions of the original code that are derived by evolutionary processes. For instance, we can find examples of stop codons in mitochondria that have acquired an amino acid translation. You can read more about natural variation in the genetic code here.

2That’s right, he wasn’t answering her questions. Meyer was apparently bidding for time until the big fat liar next to him could get up a good head of steam.

3This implication that Hox gene expression is irrelevant because it is “late” was a staple of Wells’ book, Icons of Evolution and the Politically Incorrect Guide to Darwinism and Intelligent Design. It’s a sham. The phylotypic stage, when the Hox genes are exhibiting their standard patterns of expression, of humans is at 4-5 weeks (out of 40 weeks), and in zebrafish it’s at 18-24 hours. These are relatively early events. The major landmarks before this period are gastrulation, when major tissue layers are established, and neurulation, when the neural tube forms. Embryos are like elongate slugs with the beginnings of a few tissues before this time.

4What? Patterned Hox gene expression is associated with the establishment of the body plan. Prior to this time, all the embryonic chordate has of a body plan is a couple of specified axes, a notochord, and a dorsal nerve tube. The pharyngula stage/phylotypic stage is the time when Hox gene expression is ordered and active, when organogenesis is ongoing, and when the hallmarks of chordate embryology, like segmental myotomes, a tailbud, and branchial arches are forming.

5Hox genes are not non-specific. They have very specific patterning roles; you can’t substitute abdominal-B for labial, for instance. They can be artificially swapped between individuals of different phyla and still function, which ought, to a rational person, be regarded as evidence of common origin, but they definitely do instigate the assembly of different structures in different species, which is not at all surprising. When you put a mouse gene in a fly, you are transplanting one gene out of the many hundreds of developmental genes needed to build an eye; the eye that is assembled is built of 99% fly genes and 1% (and a very early, general 1%) mouse genes. If it did build a mouse eye in a fly, we’d have to throw out a lot of our understanding of molecular genetics and become Intelligent Design creationists.

Hox genes are initiators or selectors; they are not the embryonic structure itself. Think of it this way: the Hox genes just mark a region of the embryo and tell other genes to get to work. It’s as if you are contracting out the building of a house, and you stand before your subcontractors and tell them to build a wall at some particular place. If you’ve got a team of carpenters, they’ll build one kind of wall; masons will build a different kind.

6No, the similarity of Hox genes is not a problem. It’s an indicator of common descent. It’s evidence for evolution.

7Good god.

Why is a fly not a horse? Because Hox genes are not the blueprint, they are not the totality of developmental events that lead to the development of an organism. You might as well complain that the people building a tarpaper shack down by the railroad tracks are using hammers and nails, while the people building a MacMansion on the lakefront are also using hammers and nails, so shouldn’t their buildings come out the same? Somebody who said that would be universally regarded as a clueless moron. Ditto for a supposed developmental biologist who thinks horses and flies should come out the same because they both have Hox genes.

8You can find homeobox-containing genes in plants. All that sequence is is a common motif that has the property of binding DNA at particular nucleotide sequences. What makes for a Hox gene, specifically, is its organization into a regulated cluster. How such genes and gene clusters could arise is simply trivial in principle, although working out the specific historical details of how it happened is more complex and interesting.

The case of sponges is enlightening, because they show us an early step in the formation of the Hox cluster. Current thinking is that sponges don’t actually have a Hox cluster (the first true Hox genes evolved in cnidarians), they have a Hox-like cluster of what are called NK genes. Apparently, grouping a set of transcription factors into a complex isn’t that uncommon in evolution.

9If you photocopy a paper, the paper doesn’t acquire more information. But if you’ve got two identical twins, A who is holding one copy of the paper, and B who is holding two copies of the same paper, B has somewhat more information. Wells’ analogy is a patent red herring.

The ancestral cnidarian proto-Hox cluster is thought to have contained four Hox genes. Humans have 39 Hox genes organized into four clusters. Which taxon contains more information in its Hox clusters? This is a trick question for Wells; people with normal intelligence, like most of you readers, would have no problem recognizing that 39 is a bigger number than 4. Jonathan Wells seems to have missed that day in his first grade arithmetic class.

It’s appalling, but this is the Discovery Institute’s style: to trot out a couple of crackpots with nice degrees, who then proceed to make crap up while pretending to be all sincere and informed and authoritative. It’s an annoying trick, and I can understand entirely why a few intelligent people with actual knowledge in the audience might find the performance infuriating. I do, too.

Darwinopterus and mosaic, modular evolution

i-e88a953e59c2ce6c5e2ac4568c7f0c36-rb.png

It’s yet another transitional fossil! Are you tired of them yet?

Darwinopterus modularis is a very pretty fossil of a Jurassic pterosaur, which also reveals some interesting modes of evolution; modes that I daresay are indicative of significant processes in development, although this work is not a developmental study (I wish…having some pterosaur embryos would be exciting). Here it is, one gorgeous animal.

i-e79bd89fb0f5aef616672d3d792dcc97-darwinopterus-thumb-400x456-20754.jpeg
(Click for larger image)
Figure 2. Holotype ZMNH M8782 (a,b,e) and referred specimen YH-2000 ( f ) of D. modularis gen. et sp. nov.: (a) cranium and mandibles in the right lateral view, cervicals 1-4 in the dorsal view, scale bar 5cm; (b) details of the dentition in the anterior tip of the rostrum, scale bar 2cm; (c) restoration of the skull, scale bar 5cm; (d) restoration of the right pes in the anterior view, scale bar 2 cm; (e) details of the seventh to ninth caudal vertebrae and bony rods that enclose them, scale bar 0.5 cm; ( f ) complete skeleton seen in the ventral aspect, except for skull which is in the right lateral view, scale bar 5 cm. Abbreviations: a, articular; cr, cranial crest; d, dentary; f, frontal; j, jugal; l, lacrimal; ldt, lateral distal tarsal; m, maxilla; mdt, medial distal tarsal; met, metatarsal; n, nasal; naof, nasoantorbital fenestra; p, parietal; pd, pedal digit; pf, prefrontal; pm, premaxilla; po, postorbital; q, quadrate; qj, quadratojugal; sq, squamosal; ti, tibia.

One important general fact you need to understand to grasp the significance of this specimen: Mesozoic flying reptiles are not all alike! There are two broad groups that can be distinguished by some consistent morphological characters.

The pterosaurs are the older of the two groups, appearing in the late Triassic. They tend to have relatively short skulls with several distinct openings, long cervical (neck) ribs, a short metacarpus (like the palm or sole of the foot), a long tail (with some exceptions), and an expanded flight membrane suspended between the hind limbs, called the cruropatagium. They tend to be small to medium-sized.

The pterodactyls are a more derived group that appear in the late Jurassic. Their skulls are long and low, and have a single large opening in front of the eyes, instead of two. Those neck ribs are gone or reduced, they have a long metacarpus and short tails, and they’ve greatly reduced the cruropatagium. Some of the pterodactyls grew to a huge size.

Here’s a snapshot of their distribution in time and phylogenetic relationships. The pterosaurs are in red, and the pterodactyls are in blue.

i-d0d352c1204413cbd22c1d7a20e1e0b8-pter_phylo-thumb-400x272-20751.jpeg
(Click for larger image)
Time-calibrated phylogeny showing the temporal range of the main pterosaur clades; basal clades in red, pterodactyloids in blue; known ranges of clades indicated by solid bar, inferred ‘ghost’ range by coloured line; footprint symbols indicate approximate age of principal pterosaur track sites based on Lockley et al. (2008); stratigraphic units and age in millions of years based on Gradstein et al. (2005). 1, Preondactylus; 2, Dimorphodontidae; 3, Anurognathidae; 4, Campylognathoididae; 5, Scaphognathinae; 6, Rham- phorhynchinae; 7, Darwinopterus; 8, Boreopterus; 9, Istiodactylidae; 10, Ornithocheiridae; 11, Pteranodon; 12, Nyctosauridae; 13, Pterodactylus; 14, Cycnorhamphus; 15, Ctenochasmatinae; 16, Gnathosaurinae; 17, Germanodactylus; 18, Dsungaripteridae; 19, Lonchodectes; 20, Tapejaridae; 21, Chaoyangopteridae; 22, Thalassodromidae; 23, Azhdarchidae. Abbreviations: M, Mono- fenestrata; P, Pterodactyloidea; T, Pterosauria; ca, caudal vertebral series; cv, cervical vertebral series; mc, metacarpus; na, nasoantorbital fenestra; r, rib; sk, skull; v, fifth pedal digit.

Darwinopterus is in there, too—it’s the small purple box numbered “7”. You can see from this diagram that it is a pterosaur in a very interesting position, just off the branch that gave rise to the pterodactyls. How it got there is interesting, too: it’s basically a pterosaur body with the head of a pterodactyl. Literally. The authors of this work carried out multiple phylogenetic analyses, and if they left the head out of the data, the computer would spit out the conclusion that this was a pterosaur; if they left the body out and just analyzed the skull, the computer would declare it a pterodactyl.

What does this tell us about evolution in general? That it can be modular. The transitional form between two species isn’t necessarily a simple intermediate between the two in all characters, but may be a mosaic: the anatomy may be a mix of pieces that resemble one species more than the other. In this case, what happened in the evolution of the pterodactyls was that first a pterodactyl-like skull evolved in a pterosaur lineage, and that was successful; later, the proto-pterodactyls added the post-cranial specializations. Not everything happened all at once, but stepwise.

i-94819b8301477fb9f96d640f74156a9c-pter_evo-thumb-400x314-20748.jpeg
(Click for larger image)
Schematic restorations of a basal pterosaur (above), Darwinopterus (middle) and a pterodactyloid (below) standardized to the length of the DSV, the arrow indicates direction of evolutionary transformations; modules: skull (red), neck (yellow), body and limbs (monochrome), tail (blue); I, transition phase one; II, transition phase two.

This should be a familiar concept. In pterodactyls, skulls evolved a specialized morphology first, and the body was shaped by evolutionary processes later. We can see a similar principle in operation in the hominid lineage, too, but switched around. We evolved bipedalism first, in species like Ardipithecus and Australopithecus, and the specializations of our skull (to contain that big brain of which we are so proud) came along later.

As I mentioned at the beginning, this is an example of development and evolution in congruence. We do find modularity in developmental process — we have genetic circuits that are expressed in tissue- and region-specific ways in development. We can talk about patterns of gene expression that follow independent programs to build regions of the body, under the control of regional patterning genes like the Hox complex. In that sense, what we see in Darwinopterus is completely unsurprising.

What is interesting, though, is that these modules, which we’re used to seeing within the finer-grained process of development, also retain enough coherence and autonomy to be visible at the level of macroevolutionary change. It caters to my biases that we shouldn’t just pretend that all the details of development are plastic enough to be averaged out, or that the underlying ontogenetic processes will be overwhelmed by the exigencies of environmental factors, like selection. Development matters — it shapes the direction evolution can take.

Lü J, Unwin DM, Jin X, Liu Y, Ji Q (2009) Evidence for modular evolution in a long-tailed pterosaur with a pterodactyloid skull. Proc. R. Soc. B published online 14 October 2009 doi: 10.1098/rspb.2009.1603

I should have mentioned that Darren Naish has a very thorough write-up on Darwinopterus!

My talk at AAI

Josh Timonen has put up a video of my talk at AAI. Tear into it!

One of the things I neglected to say more clearly, but should have, is that what I’m complaining about is the creationists’ blithe conflation of complexity with order. We can build up immense amounts of complexity from nothing but noise, so just babbling about how complicated something is says nothing about the impossibility of its origin from chance events. Order, functionality, and, as Joe Felsenstein defined it, adaptedness are more relevant properties, and we have a natural mechanism for generating those, too. It’s called selection.

Someone over at the RDF also mentioned that he thought the Q&A was really good, too. I agree — I need to learn to shut up more and just get the interactivity going. Maybe my ideal talk would be 5 minutes of raillery and inflammatory incitement, followed by 55 minutes of questions and comments.