How to make a snake

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Blogging on Peer-Reviewed Research

First, you start with a lizard.

Really, I’m not joking. Snakes didn’t just appear out of nowhere, nor was there simply some massive cosmic zot of a mutation in some primordial legged ancestor that turned their progeny into slithery limbless serpents. One of the tougher lessons to get across to people is that evolution is not about abrupt transmutations of one form into another, but the gradual accumulation of many changes at the genetic level which are typically buffered and have minimal effects on the phenotype, only rarely expanding into a lineage with a marked difference in morphology.

What this means in a practical sense is that if you take a distinct form of a modern clade, such as the snakes, and you look at a distinctly different form in a related clade, such as the lizards, what you may find is that the differences are resting atop a common suite of genetic changes; that snakes, for instance, are extremes in a range of genetic possibilities that are defined by novel attributes shared by all squamates (squamates being the lizards and snakes together). Lizards are not snakes, but they will have inherited some of the shared genetic differences that enabled snakes to arise from the squamate last common ancestor.

So if you want to know where snakes came from, the right place to start is to look at their nearest cousins, the lizards, and ask what snakes and lizards have in common, that is at the same time different from more distant relatives, like mice, turtles, and people…and then you’ll have an idea of the shared genetic substrate that can make a snake out of a lizard-like early squamate.

Furthermore, one obvious place to look is at the pattern of the Hox genes. Hox genes are primary regulators of the body plan along the length of the animal; they are expressed in overlapping zones that specify morphological regions of the body, such as cervical, thoracic, lumbar, sacral/pelvic, and caudal mesodermal tissues, where, for instance, a thoracic vertebra would have one kind of shape with associated ribs, while lumbar vertebra would have a different shape and no ribs. These identities are set up by which Hox genes are active in the tissue forming the bone. And that’s what makes the Hox genes interesting in this case: where the lizard body plan has a little ribless interruption to form pelvis and hindlimbs, the snake has vertebra and ribs that just keep going and going. There must have been some change in the Hox genes (or their downstream targets) to turn a lizard into a snake.

There are four overlapping sets of Hox genes in tetrapods, named a, b, c, and d. Each set has up to 13 individual genes, where 1 is switched on at the front of the animal and 13 is active way back in the tail. This particular study looked at just the caudal members, 10-13, since those are the genes whose expression patterns straddle the pelvis and so are likely candidates for changes in the evolution of snakes.

Here’s a summary diagram of the morphology and patterns of Hox gene expression in the lizard (left) and snake (right). Let’s see what we can determine about the differences.

nature08789-f4.2.jpg
(Click for larger image)

Evolutionary modifications of the posterior Hox system in the whiptail lizard and corn snake. The positions of Hox expression domains along the paraxial mesoderm of whiptail lizard (32-40 somites, left) and corn snake (255-270 somites, right) are represented by black (Hox13), dark grey (Hox12), light grey (Hox11) and white (Hox10) bars, aligned with coloured schemes of the future vertebral column. Colours indicate the different vertebral regions: yellow, cervical; dark blue, thoracic; light blue, lumbar; green, sacral (in lizard) or cloacal (in snake); red, caudal. Hoxc11 and Hoxc12 were not analysed in the whiptail lizard. Note the absence of Hoxa13 and Hoxd13 from the corn snake mesoderm and the absence of Hoxd12 from the snake genome.


The morphology is revealing: snakes and lizards have the same regions, cervical (yellow), thoracic (blue), sacral (or cloacal in the snake, which lacks pelvic structures in most species) in green, and caudal or tail segments (red). The differences are in quantity — snakes make a lot of ribbed thoracic segments — and detail — snakes don’t make a pelvis, usually, but do have specializations in that corresponding area for excretion and reproduction.

Where it really gets interesting is in the expression patterns of the Hox genes, shown with the bars that illustrate the regions where each Hox gene listed is expressed. They are largely similar in snake and lizard, with boundaries of Hox expression that correspond to transitions in the morphology of vertebrae. But there are revealing exceptions.

Compare a10/c10 in the snake and lizard. In the snake, these two genes have broader expression patterns, reaching up into the thoracic region; in the lizard, they are cut off sharply at the sacral boundary. This is interesting because in other vertebrates, the Hox 10 group is known to have the function of suppressing rib formation. Yet there they are, turned on in the posterior portion of the thorax in the snake, where there are ribs all over the place.

In the snake, then, Hox a10 and c10 have lost a portion of their function — they no longer shut down ribs. What is the purpose of the extended domain of a10/c10 expression? It may not have one. A comparison of the sequences of these genes between various species reveals a detectable absence of signs of selection — the reason these genes happen to be active so far anteriorly is because selection has been relaxed, probably because they’ve lost that morphological effect of shutting down ribs. Those big bars are a consequence of simple sloppiness in a system that can afford a little slack.

The next group of Hox genes, the 11 group, are very similar in their expression patterns in the lizard and the snake, and that reflects their specific roles. The 10 group is largely involved in repression of rib formation, but the 11 group is involved in the development of sacrum-specific structures. In birds, for instance, the Hox 11 genes are known to be involved in the development of the cloaca, a structure shared between birds, snakes, and lizards, so perhaps it isn’t surprising that they aren’t subject to quite as much change.

The 13 group has some notable differences: Hox a13 and d13 are mostly shut off in the snake. This is suggestive. The 13 group of Hox genes are the last genes, at the very end of the animal, and one of their proposed functions is to act as a terminator of patterning — turning on the Hox 13 genes starts the process of shutting down the mesoderm, shrinking the pool of tissue available for making body parts, so removing a repressor of mesoderm may promote longer periods of growth, allowing the snake to extend its length further during embryonic development.

So we see a couple of clear correlates at the molecular level for differences in snake and lizard morphology: rib suppression has been lost in the snake Hox 10 group, and the activity of the snake Hox 13 group has been greatly curtailed, which may be part of the process of enabling greater elongation. What are the similarities between snakes and lizards that are also different from other animals?

This was an interesting surprise. There are some differences in Hox gene organization in the squamates as a whole, shared with both snakes and lizards.

nature08789-f1.2.jpg
(Click for larger image)

Genomic organization of the posterior HoxD cluster. Schematic representation of the posterior HoxD cluster (from Evx2 to Hoxd10) in various vertebrate species. A currently accepted phylogenetic tree is shown on the left. The correct relative sizes of predicted exons (black boxes), introns (white or coloured boxes) and intergenic regions (horizontal thick lines) permit direct comparisons (right). Gene names are shown above each box. Colours indicate either a 1.5-fold to 2.0-fold (blue) or a more than 2.0-fold (red) increase in the size of intronic (coloured boxes) or intergenic (coloured lines) regions, in comparison with the chicken reference. Major CNEs are represented by green vertical lines: light green, CNEs conserved in both mammals and sauropsids; dark green, CNEs lost in the corn snake. Gaps in the genomic sequences are indicated by dotted lines. Transposable elements are indicated with asterisks of different colours (blue for DNA transposons; red for retrotransposons).


That’s a diagram of the structure of the chromosome in the neighborhood of the Hox d10-13 genes in various vertebrates. For instance, look at the human and the turtle: the layout of our Hox d genes is vary similar, with 13-12-11-10 laid out with approximately the same distances between them, and furthermore, there are conserved non-coding elements, most likely important pieces of regulatory DNA, that are illustrated in light yellow-reen and dark green vertical bars, and they are the same, too.

In other words, the genes that stake out the locations of pelvic and tail structures in turtles and people are pretty much the same, using the same regulatory apparatus. It must be why they both have such pretty butts.

But now compare those same genes with the squamates, geckos, anoles, slow-worms, and corn snakes. The differences are huge: something happened in the ancestor of the squamates that released this region of the genome from some otherwise highly conserved constraints. We don’t know what, but in general regulation of the Hox genes is complex and tightly interknit, and this order of animals acquired some other as yet unidentified patterning mechanism that opened up this region of genome for wider experimentation.

When these regions are compared in animals like turtles and people and chickens, the genomes reveal signs of purifying selection — that is, mutations here tend to be unsuccessful, and lead to death, failure to propagate, etc., other horrible fates that mean tinkering here is largely unfavorable to fecundity (which makes sense: who wants a mutation expressed in their groinal bits?). In the squamates, the evidence in the genome does not witness to intense selection for their particular arrangement, but instead, of relaxed selection — they are generally more tolerant of variations in the Hox gene complex in this area. What was found in those enlarged intergenic regions is a greater invasion of degenerate DNA sequences: lots of additional retrotransposons, like LINES and SINES, which are all junk DNA.

So squamates have more junk in the genomic trunk, which is not necessarily expressed as an obvious phenotypic difference, but still means that they can more flexibly accommodate genetic variations in this particular area. Which means, in turn, that they have the potential to produce more radical experiments in morphology, like making a snake. The change in Hox gene regulation in the squamate ancestor did not immediately produce a limbless snake, instead it was an enabling mutation that opened the door to novel variations that did not compromise viability.


Di-Po N, Montoya-Burgos JI, Miller H, Pourquie O, Milinkovitch MC, Duboule D (2010) Changes in Hox genes’ structure and function during the evolution of the squamate body plan. Nature 464:99-103.

86 Comments

There’s another way to make a snake. You take a human and elect that human to public office. It’s much faster than evolution.

Seriously though, I love reading about these kinds of things.

crosspost from pharyngula:

Legless lizard From Wikipedia, the free encyclopedia

Legless lizard may refer to any of several groups of lizards which have independently lost limbs or reduced them to the point of being of no use in locomotion.[1] It is the common name for the family Pygopodidae[2], but often refers to other groups, such as limbless anguids, depending upon the region of the world.[citation needed] These lizards are often distinguishable from snakes on the basis of one or more of the following characteristics: possessing eyelids, possessing external ear openings, lack of broad belly scales, and/or a very long tail (while snakes have a long body and short tail).[1]

Many families of lizards have independently evolved limblessness or greatly reduced limbs (which are presumably non-functional in locomotion), including the following examples:[1]

Anguidae – many limbless species, including genera Ophisaurus and Anguis. Cordylidae – genus Chamaesaura. Pygopodidae – members of the family are named Legless lizards due to their absent forelimbs and greatly reduced hindlimbs.[2] These are small flaps without digits, hence the common name “flap-footed lizards”. Dibamidae – all members of the family are limbless burrowers which are nearly or completely blind. Anniellidae – all members of the family are limbless. Gymnophthalmidae – Many limbless and nearly-limbless species. Scincidae – Many limbless and nearly-limbless species. Gerrhosauridae – Several limbless or reduced-limbed species.

The snakelike morphology has evolved many times. There are whole groups of lizards that have lost their external legs. Called rather imaginatively, the “legless lizards”.

It would be interesting to compare the hox genes of these lizards with those of their ancestral lizard species and with their cousins the snakes.

Great stuff. Someday we will know enough to build a dinosaur.

Couple of quibbles: Lizards are not a clade, as shown by your figure but contra your text, and snakes are nested within them. Fortunately the node your are discussing exists regardless.

And there may be one thing wrong with the tree in your figure; some evidence suggests the the chicken and the turtle should go together. Again, irrelevant to your story, but good to know anyway.

More sampling of lizards and snakes, including various groups of legless lizards, would probably be instructive. Get on it immediately.

PZ Myers said: The differences are huge: something happened in the ancestor of the squamates that released this region of the genome from some otherwise highly conserved constraints.

That would be the bit where God said, “Because thou hast done this, thou art cursed above all cattle, and above every beast of the field; upon thy belly shalt thou go, and dust shalt thou eat all the days of thy life,” or at least, that is what creationists would have us believe ☺

PZ Myers said

(which makes sense: who wants a mutation expressed in their groinal bits?)

Written by a man who knows his trouser-snake is never going to run out of legs? Surely for those with a less than perfect penis, not all mutation is bad.

To me the interesting thing would be to find out what was responsible for removing functional constraints on such a highly conserved mechanism. That might tell us a lot more about hox gene regulation than is presently known. The comparative approach would most likely be the way to get clues about where to look.

Thanks PZ, for another interesting and informative post.

Another vote for less contstraint in the lower chakras. I think it would be awesome to have a baroque dick.

Speaking of squamates, check out Lizards and Snakes Alive at the American Museum of Natural History. I have seen this and it’s really cool.

Paul Burnett said:

PZ got it wrong:

http://grahammercer.com.au/humour/G[…]TheSnake.jpg

Dang! You beat me to it! Being a Larson fan, this cartoon was the first thing I thought of when I saw the title of the post.

John_S said:

Dang! You beat me to it! Being a Larson fan, this cartoon was the first thing I thought of when I saw the title of the post.

Me too. Great minds work alike.

One of the tougher lessons to get across to people is that evolution is not about abrupt transmutations of one form into another, but the gradual accumulation of many changes at the genetic level which are typically buffered and have minimal effects on the phenotype, only rarely expanding into a lineage with a marked difference in morphology.

Do I understand it correctly that (even in a stable environment) evolution is proceeding at a more or less constant speed due to accumulation of mutations, but with little effect on the appearance of the critters in question, because they are already well adapted to the environment?

Maybe the “only” effect of evolution in a stable environment is to increase the genetic diversity of the critters?

Suppose then that there will be a fairly large change in the environment, such as a major food source becoming scarce. This might lead to radiation of species, as new sources need to be found in order to survive. Is this something akin to punctuated equilibrium?

Genetic diversity will help in finding new sources of food, I presume.

Snakes are a very good point to the gain of biblical creationism. They are one of the few creatures with remnant of a previous anatomical existence. Genesis explains why. This is unique despite the evolutionary claim that everything looked like something else endlessly. Yet few have unsed bones to prove it.

Snakes are a kind despite losing their legs and so allows flexibility for creations in explaining diversity. Snakes surely were only one kind off the ark and so spitters and squeezers and egg layers and live birthers (important to me) all are the result of post flood adaptation and show how life can rapidly change.

The legless lizards are not snakes. In fact the leggy snake was probably very different looking then any thing we can now imagine. There is no reason to see a connection between legless lizards and snakes as showing what evolution can do. The lizards are just a variety of lizard. I don’t know if they have anatomical evidence of their leggy previous existence but anyways its still guessing to see them like snakes. It could only be that like form has like details in dna etc. Yet not a trail of heritage.

We have a clear witness in the bible on the origin of the snake. The lizards are just ordinary adaptation.

Cue; blowing tumble-weeds and whistling empty wind: RB has entered the building.

My favourite Gary Larson is god pulling earths out of a cosmic oven and noting that our own planet, as he says, ‘is only half-baked’.

What a wonderful thing it is to have an imagination; but how horrible to see it used as a substitute for reality.

Eric, in a stable population I wouldn’t necessarily say that evolution would result in increased diversity. Mutations are constantly being pumped into the population for sure, and they accumulate at a certain rate, but the population size will ultimately control how many of those neutral mutations can be maintained. This is because drift will randomly eliminate variation from the population every generation. Now the potentially important thing to consider is how long has the population been that size? It takes a fair amount of time for a growing population to see a corresponding increase in genetic diversity, as conservationists well know.

Robert Byers said: Snakes…are one of the few creatures with remnant of a previous anatomical existence.

All living things have a “remnant of a previous anatomical existence.” If you agree that some snakes have remnants of a pelvis, then you must also be aware that some whales have remnants of a pelvis, proving they were once land animals. Right?

This is actually exciting, as it means that whales were on board Noah’s Ark, as land animals with pelvises and legs - and then hyper-evolved into much larger sea creatures in a matter of hours after the Ark landed on a mountain-top in the middle of a desert. Do you see any problems with this hypothesis, Robert?

JGB said:

Eric, in a stable population I wouldn’t necessarily say that evolution would result in increased diversity. Mutations are constantly being pumped into the population for sure, and they accumulate at a certain rate, but the population size will ultimately control how many of those neutral mutations can be maintained. This is because drift will randomly eliminate variation from the population every generation. Now the potentially important thing to consider is how long has the population been that size? It takes a fair amount of time for a growing population to see a corresponding increase in genetic diversity, as conservationists well know.

Am I correct in assuming that you approach the question of populations and alleles from a statistical point of view?

If you do, that approach seems valid to me.

OK, the genetic diversity does not (necessarily) increase in a stable population. Then, what is going on? Does the drift result in new satellite species, thus leaving the original population virtually intact?

The current subject is about snakes. Are snakes outcasts of the “lizard population”?

I hope you forgive my ignorant and partly aggressive questions.

Paul Burnett said:

This is actually exciting, as it means that whales were on board Noah’s Ark, as land animals with pelvises and legs - and then hyper-evolved into much larger sea creatures in a matter of hours after the Ark landed on a mountain-top in the middle of a desert.

I never thought of it before, but you have a point there, Paul. It’s unlikely most cetaceans could have survived a global flood. Very few of them “generalists”, they mostly have specialized diets which would have been grossly disrupted by the vast salinity, temperature and current circulation changes of a flood.

Ironically, the whales most in need of being on the ark are the largest, the huge baleen whales. They’re dependant on not only finding krill, but finding krill in large schools in at predictable points along their migratory path.

Since the krill population would be decimated and scattered by changes in the ocean and the currents, the baleen whales would quickly starve.

Conversely, the Ganges River Dolphin, a small animal which can happily live in fresh, brackish and salt water, and which which has an extremely varied diet (basically, anything it can catch or find), would do nicely. In fact, I would expect it to take the opportunity to migrate widely, in the biosphere now largely devoid of competitors, whcih is why we find it all over the world and…

What was that you say?.….

We don’t find the river dolphin all over the lakes of the planet?

We only find them in a tiny slice of closely-connected rivers in India and south Asia?

Hmmm… now that’s really weird.

Maybe Byers has some explanation for that.

Byers, Ever read the “Just So” stories of Rudyard Kipling? He took his cue from the “How the Snake Lost Its Legs” children’s fable in Genesis.

Defending the snake story in Genesis makes you look just as foolish as you would by defending Kipling’s “How the Elephant Got Its Trunk” or “How the Rhinocerous Got Its Skin.”

Don’t you get that? it seems that there’s a lot that you Just Don’t Get.

The interaction of drift and mutation would be a population who is in fact changing which particular neutral alleles it has, and is therefore evolving, but the changes would only be noticeable on the sequence level.

Drift will only seperate the species if there is a reproductive barrier first, which in effect means that the population is not stable. This can tie into punctuated equilibrium, in that in absence of a significant environmental change we would imagine drift to be causing these genetic changes that do not produce new phenotypes directly. What it can do however is open new doors. A neutral allele is only neutral in that particular environment. Drift is perfectly able to change the population in such a way that it could adapt in a new or different way by selection, whereas earlier that option may not have been possible.

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John Kwok said:

Actually Noah received ample help. Klingon scientists aboard orbiting Klingon Defense Force battlecruisers beamed up the ancestral whales, conducted experiments, and then beamed down the lucky survivors at the end of the flood:

Well, that works for the whales, and I’ve pointed out before that if Noah was the organized type and arranged the ark alphabetically, he would have placed the unicorns in a pen next to the tyrannosaurs. Which would go a long way towards explaining why neither of them apparently made it through the entire cruise…

Actually Noah received ample help. Klingon scientists aboard orbiting Klingon Defense Force battlecruisers beamed up the ancestral whales, conducted experiments, and then beamed down the lucky survivors at the end of the flood:

Yes, why not? Wasn’t there a whale in Star Trek 4? The Klingon researchers were probably dining on whale meat, just like the Japanese whale researchers do today.

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John Kwok said:

I suppose the Klingons didn’t like the unicorns and the tyrannosaurs:

I don’t know about that … what’s Klingon for “good eatin’”?

That would be gagh.

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No, no. The unicorns did NOT die in the Flood, nor were they left off the Ark! They’re referred to NINE times in the KJV, all post-Flood. Byers has one in his cellar, along with his talking snake, talking ass, 4-legged bugs, cud-chewing bunnies, and avian bats.

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John Kwok said:

If PZ was posting at Pharyngula, blog entries as splendid as this one on the evolutionary developmental biological evidence demonstrating how snakes evolved from lizards, I wouldn’t be clamoring for Science Blogs to shut down Pharyngula now, and suggesting that maybe it ought to move to a more suitable online environment like Daily Kos.

Reluctantly, I must concur with the final paragraph from Sheril’s opening statement at her Intersection blog entry. And it isn’t because of any personal animosity I may hold toward PZ or his Pharyngulite Borg Collective. Instead, it is for the very reasons she has stated.

PZ posted this at Pharyngula. Did I mention that I went to a very prestigious high school with a bunch of very famous people, all of whom would agree with me? Oh and Kwok, you owe me a camera.

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Please note that I was not arguing with you, John, I was making fun of you.

one of your fellow Pharyngulites

Please detail the evidence for your assertion that I am a “Pharyngulite”, apart from your usual paranoid “if they’re not with me, they’re against me” mentality.

Your own absurd tribal group think mentality

“If they’re not with me, they’re against me.” Go ahead, tell me I’m acting exactly like a member of the Dishonesty Institute IDiot Borg Drone Collective, you know you want to.

Despite all the self-puffery, name-dropping, and bluster, I see very little evidence that anyone anywhere agrees with you about much of anything, or much cares what you think. The voices in your head may differ.

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PZ, would you kindly relegate these off topic posts (including this ) to the BW?

TIA

dpr

I swear, I’m going to STOP this car! And just wait until your father gets home!

Ye gods and little fishes, yet another Kwokathon.

Is there to be no respite?

Might someone in the PT Administration take appropriate steps?

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This comment has been moved to The Bathroom Wall.

John Kwok said:

Too bad you don’t take seriously the sad fact that one of PZ’s loyal fans posted at Pharyngula a threat…[et efficating cetera]

Sir:

When I read something about “How to make a snake”, I wish to read something about “How to make a snake”. I do not wish to read an entire topic about “The Effulgent Wisdom of John Kwok”.

Perhaps this is the thing that you have persistently, doggedly, unmovingly been unable to comprehend.

I make no pretense of being, magically, the one who can cause you to apprehend the shining truth.

But hope springs eternal.

John, you’re insane.

seek treatment.

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John Kwok said:

IMHO this was the best comment posted over at the Intersection regarding the absurd tribal mentality which you are now displaying. I think you and Ichthyic need to read it again:

Thanks, I prefer to read posts that relate to the topic at hand. If you wish somehow to designate yourself as a serpent, this may have a chance of becomeing germane.

Failing that, it is a silly example of parading oneself center stage having elbowed the legitimate actors aside.

Will SOMEONE GET THE HOOK AND DRAG THIS LOONY OFF THE STAGE, please.

Shebardigan said:

Thanks, I prefer to read posts that relate to the topic at hand.

Especially when someone’s just spamming the same sentence over and over again.

Back on (sort of) topic: are there any good sources on the evolution of snake venom? I’m curious about how the initially non-venomous snakes switched over.

John Kwok will not ever be posting on any of my articles anymore, and his comments will be deleted as soon as I get a chance. Please do not reply to him.

Back on (sort of) topic: are there any good sources on the evolution of snake venom? I’m curious about how the initially non-venomous snakes switched over.

in fact, there was an excellent discussion of the evolution of snake venom on this very site, attended by the person who probably knows more about the subject than anyone on earth.

now if i can just find that thread…

ah:

here was the original release:

http://www.corante.com/loom/archive[…]he_venom.php

here’s the guy (Bryan Fry):

http://venomdoc.com/venomdoc/Venomdoc.html

and here is the discussion on PT, where Dr Fry rips apart an old creationist front-loader type:

http://pandasthumb.org/archives/200[…]ons-and.html

ah, fun times.

ah, pardons, the thread where he rips apart the front loader is a different thread, and I can’t find it any more.

still, that thread i linked to on PT actually has a MUCH better discussion of snake venom.

One of those threads where the comments were far more educational than the original post!

Sweet. Thanks!

It’s not necessarily true that evolution always proceeds in small increments with little effect on phenotype, because small changes in hox genes can produce large phenotype changes on the spot, which will then be slected for if they turn out to be useful (although most will be harmful of course).

You can also get instant speciation in animals which for some reason are prone to chromosomal mutations. Ship rats (Rattus rattus) seem to be especially prone to this, forming non-interbreeding populations with differing chromosome counts, more or less overnight.

Although a large change might be possible in the offspring, if the change is so large as to prevent its carrier from mating, it won’t last.

U mentioned at the beginning of this post said something about speciation being the result of constant rate of mutation. as a matter of fact most studies use this constant rate of mutation assumption without any justification. A brand new study published in Nature ( http://www.nature.com/nature/journa[…]re08630.html ) compared 101 phylogentic trees and found constant rate of mutation model might account for only 8% of the speciation events in those 101 trees..

take home message, dont take everything for granted. Dont get thrilled about exciting ideas so quickly..

get well Moe

I wouldn’t expect the constant rate of mutation to account for speciation, anyway. Speciation occurs when mutations cause two parts of a population to cease routine exchange of genes with each other; that can sometimes take a huge number of mutations, or it might sometimes occur after just a few.

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