“Intraspecific macroevolution” within domestic dog breeds

| 66 Comments

Several years ago, I saw a fantastic talk at the Evolution meeting about Intraspecific macroevolution: variation of cranial shape in dog breeds. The talk was by Abby Drake, then a grad student, and reported on a huge digital morphometric comparison of the skulls of dogs and many representatives from the order Carnivora (dogs, cats, bears, sea lions, etc.).

Morphometrics basically consists of taking digital photos of e.g. bones from different angles, and then marking the same landmarks on homologous bones across a big group. Then you can quantitatively compare the differences in shape, independent of things like body size. This is a much more sophisticated analysis than is possible with just calipers, where you can only get length, width, etc.

A previous study had noted that the skull variation in dogs was bigger than the variation in the family Canidae, but the incredible result of Drake’s study was that the variation in shape of dog skulls was bigger than the variation in shape across the entire order Carnivora, which is 60 million years old and includes even mostly-aquatic forms.

Drake_Klingenberg_2010_AmNat_dogs_intraspecific_macroevolution_fg3.gif

Figure 3: Principal component (PC) analysis for skull shape in the complete data set. A-C, Plots of the PC scores. D, Shape changes associated with the PC axes. For each PC, the shapes corresponding to the observed extremes in the positive and negative directions are shown as a warped surface of a wolf skull (Wiley et al. 2005).

And most of this morphological variation took only a few hundred years to produce. It is true that some of these weird skulls would not be favored in the wild – Drake notes that natural selection is reduced when your food comes from a can rather than stuff you hunt – and artificial selection is greatly enhanced by selective breeding. But this is strong evidence that (a) there is no problem on the genetic variability end of the equation for the kinds of variability that we see in a mammalian order like Carnivores; rather the constraint is natural selection for a particular niche. If the selective pressure is there, the morphological change can happen very quickly; and (b) lack of time isn’t the issue; if the conditions are right, hundreds or thousands of years can be plenty of time.

I didn’t even notice when this study came out and got a bunch of press in January, probably because I actually had a girlfriend at the time (see, rare events do happen in geologic time!). But this is a study that should be in the back pocket of any creationism opponent. You can see an example of its usage on Cornelius Hunter here; it’s kind of like a surprise sack of a quarterback.

The other thing I like about the conclusion of “intraspecific macroevolution” is that it tweaks a lot of standard tropes that even we scientists have about what is meant by the word “macroevolution.” The minimal definition of macroevolution is “evolution above the species level”, but it has become a catchall term encompassing everything from speciation to lineage-diversification and extinction dynamics to “evolution of ‘higher taxa’” (ack! go read “down with phyla!”) to vaguely defined “large” amounts of change to evo-devo changes in development. These things then all get mixed together in people’s heads, resulting in the erroneous presumption that “‘large’ amounts of change” = lots of speciation events = the origin of some big Linnaean ‘taxon’ = lots of action at the lineage-counting level. As a very rough approximation it might be true that these different things are often linked, but as this study shows, it ain’t always true. We would probably be better off using specific terms for each of these different topics, and not trying to lump them all together under “macroevolution” as if they were all intrinsically connected. Questions like “is macroevolution just the result of repeated rounds of microevolution” have almost no meaning if “macroevolution” refers to all of these different things at once.

References

Abby Grace Drake and Christian Peter Klingenberg

Large‐Scale Diversification of Skull Shape in Domestic Dogs: Disparity and Modularity

Am Nat 2010. Vol. 175, pp. 289-301

DOI: 10.1086/650372

Abstract:

The variation among domestic dog breeds offers a unique opportunity to study large‐scale diversification by microevolutionary mechanisms. We use geometric morphometrics to quantify the diversity of skull shape in 106 breeds of domestic dog, in three wild canid species, and across the order Carnivora. The amount of shape variation among domestic dogs far exceeds that in wild species, and it is comparable to the disparity throughout the Carnivora. The greatest shape distances between dog breeds clearly surpass the maximum divergence between species in the Carnivora. Moreover, domestic dogs occupy a range of novel shapes outside the domain of wild carnivorans. The disparity among companion dogs substantially exceeds that of other classes of breeds, suggesting that relaxed functional demands facilitated diversification. Much of the diversity of dog skull shapes stems from variation between short and elongate skulls and from modularity of the face versus that of the neurocranium. These patterns of integration and modularity apply to variation among individuals and breeds, but they also apply to fluctuating asymmetry, indicating they have a shared developmental basis. These patterns of variation are also found for the wolf and across the Carnivora, suggesting that they existed before the domestication of dogs and are not a result of selective breeding.

Robert K. Wayne (1986). “Cranial Morphology of Domestic and Wild Canids: The Influence of Development on Morphological Change.” Evolution, Vol. 40, No. 2 (Mar., 1986), pp. 243-261 * Stable URL: http://www.jstor.org/stable/2408805

Abstract l The domestic dog varies remarkably in cranial morphology. In fact, the differences in size and proportion between some dog breeds are as great as those between many genera of wild canids. In this study, I compare patterns of intracranial allometry and morphologic diversity between the domestic dog and wild canid species. The results demonstrate that the domestic dog is morphologically distinct from all other canids except its close relatives, the wolf-like canids. Following this, I compare patterns of static and ontogenetic scaling. Data on growth of domestic dogs are presented and used to investigate the developmental mechanisms underlying breed evolution. Apparently, most small breeds are paedomorphic with respect to certain morphologic characters. In dogs and other domestic animals, morphologic diversity among adults seems to depend on that expressed during development.

66 Comments

“if the conditions are right, hundreds or thousands of years can be plenty of time.”

Yup, and I predict it will be a matter of days before the creationists twist this study to claim it proves that the few “kinds” on the Ark could easily be pushed (by God, natch) to fill all the niches with all the different species we see today.

But then, for creationists, the conditions are always right - for lying.

“intraspecific macroevolution”

Cringe. This is an oxymoron. Plus, the morphological differences within this species, large as they are, are not permanent at all. They are easily lost when artificial genetic isolation is relaxed for even a couple of generations. Need data, sloppy terminology.

Hi Ryan! Thanks for the comment, I was attempting to be provocative (obviously). So I’ll continue:

1. Who says these aren’t permanent changes? And, who says that the morphological changes that *do* occur in “regular large scale natural evolution” *are* permanent? In either case what happens morphologically probably depends substantially on the future selective regime, which will either maintain the changes, or it won’t.

2. Re: oxymoron. So, hypothetically, if a major developmental change leading to a “major” morphological change (say, on the level of the differences we typically see between genera or between families) did occur *within* a species, complete with polymorophism within the population for this change which is later fixed by selection – but with no speciation/lineage-splitting event, would this be:

(a) a microevolutionary event, because it was within a species, or

(b) a macroevolutionary event, because the amount of change was on the level of the differences often observed between higher taxa?

Obviously there must be a simple, correct answer, right?

;-)

TR Gregory said:

“intraspecific macroevolution”

They are easily lost when artificial genetic isolation is relaxed for even a couple of generations.

In that sense and in light of our partial Neanderthal ancestry what major changes (morphological or not) might just as easily have been lost when if that genetic isolation was lost for longer? In other words what is the significance of emphasizing the incomplete speciation of the different dog breeds?

Steve said:

Yup, and I predict it will be a matter of days before the creationists twist this study …

Though I may be overly suspicious here, I think your timescale may have been optimistic:

TR Gregory said:

“intraspecific macroevolution”

Cringe. This is an oxymoron.

Fascinating article, NickM. The variations in morphology among dogs are obvious, but that they exceed by proper measures those of the rest of the Carnivora comes as a surprise.

BUT THEY ARE ALL STILL DOGS!

Well, somebody had to say it.

The important thing is not the degree of morphological or even genetic variation. The important thing is genetic discontinuity. Now if all of the types of dogs are still potentially interbreeding, then there may or may not be any significant discontinuities. That would depend on the actual degree of interbreeding, along with mutation rate, population size, epistatic interactions, etc. Given the degree of variation observed, speciation would seem to be a fairly trivial outcome of such processes. This does demonstrate the tremendous power of artificial selection. It should also convince any unbiased observer that natural selection can be a very powerful force as well.

MrG said:

Steve said:

Yup, and I predict it will be a matter of days before the creationists twist this study …

Though I may be overly suspicious here, I think your timescale may have been optimistic:

TR Gregory said:

“intraspecific macroevolution”

Cringe. This is an oxymoron.

Fascinating article, NickM. The variations in morphology among dogs are obvious, but that they exceed by proper measures those of the rest of the Carnivora comes as a surprise.

You are indeed being overly suspicious. Dr. Gregory is an evolutionary biologist who literally wrote the book on genome evolution (full disclosure: I haven’t read it). Definitely not a creationist.

As I read this article about humans making huge changes in the morphological diversity of a companion specie, I could not help but speculate as to how we have guided our OWN morphological changes. Anyone have any thoughts?

I would not care to put money on the long survival of male facial and body hair, for one thing.

TR Gregory said:

“intraspecific macroevolution”

Cringe. This is an oxymoron. Plus, the morphological differences within this species, large as they are, are not permanent at all. They are easily lost when artificial genetic isolation is relaxed for even a couple of generations. Need data, sloppy terminology.

I’m not a biologist (glacial geologist) but “intraspecific macroevolution” looks like a loser to me. Any creationist or ID’er (except a diehard YEC) will immediately dismiss the paper as demonstrating “microevolution” that has no bearing on “macroevolution”, while the YEC will blather on about how rapidly the “kinds” will change to repopulate the earth after Noah’s Flood. To me, it’s just evolution.

The lesson of this paper is that the dog genome is capable of producing more than sufficient variability in body size and morphology in a very short period of time. The variability is severely limited by natural selection in the wild, leading to a much more restricted morphology in wild dogs, and reversion to this type in feral dog communities. The variability is preserved by dog breeders, or even facilitated by them. In the long run, we might even suggest that the dog species has already “evolved” into several subspecies or new species. After all, if a species is defined as a population that interbreds and produces viable offspring, I find it hard to believe that a Chihuahua and a St. Bernard can be defined as the same species.

To me, the utility of this paper is to point out the speed of change in the genome of a single species in situations where the variability can be preserved. Such might be the case after mass extinctions, where lack of competition and the emptying of most ecological niches have led to explosive radiation of mammals in the early Tertiary, of dinosaurs in the early Mesozoic, and of many other organisms. Creationists claim that there is no mechanism for the recoveries after mass extinctions. This paper provides one - normal evolution.

Sorry Nick, but morphometrics is similar the mathematics of body size and shape. While today virtually all morphometric data capture is via digitizing of images, it started with the use of calipers. After one collects the data, and then (hopefully) plots it just to see the amount of dispersion in it, then what is done next is usually some kind of data reduction technique to see if there are any correlations between body size and shape or unseen factors which account for it. What is normally referred to as factor analysis - if it is unrotated - is merely principal component analysis and this is the technique most widely used for data reduction of morphometric data (Stephen Jay Gould has an elegant description of principal components analysis - which if my memory serves, he refers to incorrectly as “factor analysi” - in his “The Mismeasure of Man”.).

Let me just rephrase the first sentence:

Sorry Nick, but morphometrics is simply the mathematics of body size and shape.

John Kwok said:

Sorry Nick, but morphometrics is similar the mathematics of body size and shape. While today virtually all morphometric data capture is via digitizing of images, it started with the use of calipers. After one collects the data, and then (hopefully) plots it just to see the amount of dispersion in it, then what is done next is usually some kind of data reduction technique to see if there are any correlations between body size and shape or unseen factors which account for it. What is normally referred to as factor analysis - if it is unrotated - is merely principal component analysis and this is the technique most widely used for data reduction of morphometric data (Stephen Jay Gould has an elegant description of principal components analysis - which if my memory serves, he refers to incorrectly as “factor analysi” - in his “The Mismeasure of Man”.).

If I were a creationist, I would point out that this is confirmation that “intelligent design”, in the form of human intervention, is capable of producing “macroevolution”.

TomS said:

If I were a creationist, I would point out that this is confirmation that “intelligent design”, in the form of human intervention, is capable of producing “macroevolution”.

Wot of it? Creationists are NEVER at a loss for a snappy answer. The nice thing about baloney is that the cost is extremely low and the supply indefinitely great.

TomS said: If I were a creationist, I would point out that this is confirmation that “intelligent design”, in the form of human intervention, is capable of producing “macroevolution”.

Except that dog breeding occurred long before we could directly manipulate genomes. Dog breeding is therefore not intelligent design, its intelligent selection. The fact is, all the variation you see was produced by nature via either sexual reproductions standard mixing or mutation. We merely decided which variant bred with which.

The fact that intelligent breeding can produce such rapid changes in morphology is, as Nick says, proof that its selection, not availability of variation, that keeps evolution relatively slow.

Of course, if you were a creationist you’d probably ignore any counter-argument posted…

Dogs appear to be one of the most morphologically plastic animals we’ve been able to domesticate. It seems like there’s something unique about their genes to let us change their size, fur, body type, skull shape, and even innate behaviors to such a great degree. (Of course it could just be that we haven’t domesticated rats for anything like the same length of time). I’ve heard that there’s a single gene that’s mostly responsible for the different angle of dog snouts (pointing out, up, or down compared to the rest of the skull), but haven’t looked into that.

Tangentially related, but to me dogs always presented a ready challenge to the conventional definition of “species” anyway, since they interbreed so readily with wolves and coyotes (who also interbreed with each other) and produce fertile offspring.

Wheels said:

Of course it could just be that we haven’t domesticated rats for anything like the same length of time.

Points taken, but I would think that the case. Domestic pigeons get pretty wild, ditto for goldfish – double tails, bubble eyes, even (I recollect) translucent goldfish where you can see their heart beating.

Translucent … try THAT with a dog.

eric said:

Except that dog breeding occurred long before we could directly manipulate genomes. Dog breeding is therefore not intelligent design, its intelligent selection. The fact is, all the variation you see was produced by nature via either sexual reproductions standard mixing or mutation. We merely decided which variant bred with which.

Some of those selections are pretty weird (pekinese for example). As has been noted, I vaguely recall by Darwin himself in terms of pigeons, many of the “sports” of domesticated organisms are just something strange that popped up and breeders ran with.

Also … it is very difficult to say that the domestication of the wolf wasn’t at the wolf’s initiative. Those with a tame inclination were much more inclined to being domesticated than those that weren’t.

Wheels said:

Dogs appear to be one of the most morphologically plastic animals we’ve been able to domesticate.

I suspect that this is what cats think about humans. ;-)

Mike Elzinga said:

I suspect that this is what cats think about humans. ;-)

Actually, SCIENTIFIC AMERICAN did an article on cat descent and domestication that pretty much said cats domesticated US. I ran an outline in my blog, I’ll give links if anyone cares. GIRL GENIUS fans of course think of Krosp, the Emperor of Cats: “I accept your fealty, human!”

MrG said:

Points taken, but I would think that the case. Domestic pigeons get pretty wild, ditto for goldfish – double tails, bubble eyes, even (I recollect) translucent goldfish where you can see their heart beating.

True, good examples. As a counterpoint, domestic cats don’t have nearly as much variety of basic shape built in it seems. Sure you get flat-faced Persians and adorable Scottish Folds, but beyond that cats still basically look like cats. You don’t see cats bred to have limbs like their dorsal fins totally absent, or stumpy badger-hunting cats with high-set, short legs and down-pointing schnauses. I’m not sure this can be fully explained by lack of trying on the part of the sport breeding community.
Humans are so weird, taking perfectly functional wildlife and churning out mutant freaks like some kind of mad science, sometimes for no reason other than to do it. Not besmirching the habit*, just making an observation.


*Although I would like to see an end to breeding programs that cause obvious health problems, like Persians that can’t stop “crying” or bulldogs that can barely breath.

Wheels said:

True, good examples. As a counterpoint, domestic cats don’t have nearly as much variety of basic shape built in it seems.

Yeah, the article discussed that, saying that the genetic variation between cats is roughly like IIRC French and Italians. But this was attributed partly to the fact that, other than mousing, cats aren’t put to much work and so there’s not so much reason to come up with specialized variants. And that’s changing now due to artificial insemination, producing hybrids like the “caracat” (housecat-caracal hybrid).

So the morphological variation in dogs mainly comes down to the fact that they can be put to some new use, uses more apparent and achievable to early breeders that weren’t in this for sports, more than to some kind of easy plasticity built into their genome.

MrG said:

Yeah, the article discussed that, saying that the genetic variation between cats is roughly like IIRC French and Italians. But this was attributed partly to the fact that, other than mousing, cats aren’t put to much work and so there’s not so much reason to come up with specialized variants.

Dogs have masters; cats have staff.

Dogs come when called. Cats tell you to leave a message and they’ll get back to you later.

It seems that this study would also indicate that when we identify different species by fossil evidence alone, we may artificially magnify the differences, and great diversity in one species may be mistaken as many different species. Would this be accurate?

I’m actually dealing with this issue for someone now, ghost-writing and editing a manuscript, but can’t say anything further on that. But you have the right idea:

Jedidiah Palosaari said:

It seems that this study would also indicate that when we identify different species by fossil evidence alone, we may artificially magnify the differences, and great diversity in one species may be mistaken as many different species. Would this be accurate?

Jedidiah Palosaari said: It seems that this study would also indicate that when we identify different species by fossil evidence alone, we may artificially magnify the differences, and great diversity in one species may be mistaken as many different species. Would this be accurate?

Speciation being just the end result of variation, it would be fair to say that it might be dificult to tell the differences between variations in a widely varying species and species that have recently split. With some caveats.

First lets get teh stupid out of the way. You understand that a continuum in morphology is a prediction of common descent with modification, and observing it is a confirmation of the theory of evolution, right? There is no other hypothesis or theory that rationally makes this prediction. ‘Goddidit that way because he wanted to’ certainly doesn’t count…are we agreed?

Okay, second: “by fossil evidence alone” is rarely the case, and even when it is, biologists consider more than just skull morphology. There are many other ways, for instance, to tell a wolf from a dog which make it quite clear which species is which.

Lastly, biologists argue over what counts as a species in the first place. If you consider populations that don’t breed with each other due to behavioral or geographical barriers (rather than biological barriers) to be different species, then of course some different species are going to have extremely similar physical traits (at least at first). So part of the ‘mistakenness’ depends on how you define species. The difficulty of distinguishing ‘close species’ versus ‘wide variations’ is, again, a problem one would predict given descent with modification.

To put that in mathematical terms, sameness of species is not a transitive relation (i.e., A is like B and B is like C does not necessarily imply A is like C).

Nick (Matzke) said:

Hi Ryan! Thanks for the comment, I was attempting to be provocative (obviously). So I’ll continue:

1. Who says these aren’t permanent changes? And, who says that the morphological changes that *do* occur in “regular large scale natural evolution” *are* permanent? In either case what happens morphologically probably depends substantially on the future selective regime, which will either maintain the changes, or it won’t.

2. Re: oxymoron. So, hypothetically, if a major developmental change leading to a “major” morphological change (say, on the level of the differences we typically see between genera or between families) did occur *within* a species, complete with polymorophism within the population for this change which is later fixed by selection – but with no speciation/lineage-splitting event, would this be:

(a) a microevolutionary event, because it was within a species, or

(b) a macroevolutionary event, because the amount of change was on the level of the differences often observed between higher taxa?

Obviously there must be a simple, correct answer, right?

;-)

Hi Nick,

I forgot to come back and check the discussion. Short answers:

1. We know it’s not permanent because dog populations that are not bred selectively revert to mutthood very quickly.

2. An oxymoron because the original and still current definition of “macroevolution” is evolution above the species level. Do you know of any such examples of the case you describe? If not, this seems like a minimally relevant scenario to contemplate.

ps: Who the heck is this Dave C guy who thinks I might be a creationist?!?

:-)

eric said:

Okay, second: “by fossil evidence alone” is rarely the case, and even when it is, biologists consider more than just skull morphology. There are many other ways, for instance, to tell a wolf from a dog which make it quite clear which species is which.

The problem I see there is that, as Gould pointed out, often paleontology is how some teeth mated with other teeth to produce more teeth. Yes, we can get a hell of a lot from teeth. But not as much as if we have the entire skeleton. If our fossils are merely teeth, as they often are, it seems we, at times, would run the risk of conflating species and genera.

Hygaboo Andersen said:

Gee, it’s hard to think of a more rancid combination of arrogance and greed than the evolutionists when it comes to their pathetic, third-rate, peer-reviewed by other evolutionists, so-called literature. Not only do they charge megabucks for 24-hour access to their articles, they also demand you register with them for the privilege of sending them this money! Evolutionists are worse than the pornographers their faith spawns when it comes to their money-grubbing spam machine! Indeed, what is the point in citing this crud knowing Christians will be unable to read and critique it–or is that the whole point?!

By the way, computer models of animals morphing into each other is not proof that it happened in real life! That is all this “research” really seems to amount to.

I think you are unaware of the nature of science. No, that’s not right. You seem to be unaware of basic English definitions. Typically, scientists *do* peer review other scientists. That’s what “peer review” means. That’s what science is. Unless you want to just redefine all of science?

Ohhh! Right. My bad.

But I see you are very anti-capitalism and free market. That of course is your right. I mean, nothing against socialism. Not that there’s anything wrong with that…

But you may also be confused on how to use a credit card and move your finger on the mouse pad to reach over and click. Most of the other Christians get that, I know. You may be just an incredibly stupid Christian.

Jedidiah Palosaari said:

Hygaboo Andersen said:

Gee, it’s hard to think of a more rancid combination of arrogance and greed than the evolutionists when it comes to their pathetic, third-rate, peer-reviewed by other evolutionists, so-called literature. Not only do they charge megabucks for 24-hour access to their articles, they also demand you register with them for the privilege of sending them this money! Evolutionists are worse than the pornographers their faith spawns when it comes to their money-grubbing spam machine! Indeed, what is the point in citing this crud knowing Christians will be unable to read and critique it–or is that the whole point?!

By the way, computer models of animals morphing into each other is not proof that it happened in real life! That is all this “research” really seems to amount to.

I think you are unaware of the nature of science. No, that’s not right. You seem to be unaware of basic English definitions. Typically, scientists *do* peer review other scientists. That’s what “peer review” means. That’s what science is. Unless you want to just redefine all of science?

Ohhh! Right. My bad.

But I see you are very anti-capitalism and free market. That of course is your right. I mean, nothing against socialism. Not that there’s anything wrong with that…

Meh,

All secular political ideologies are nothing but Darwin’s dingleberries. Justice can only be achieved by placing the Gospel at the center of all political discourse.

But you may also be confused on how to use a credit card and move your finger on the mouse pad to reach over and click. Most of the other Christians get that, I know. You may be just an incredibly stupid Christian.

What I am not confused about is having to sign up for spam. I don’t want the moral excrement of evolutionism pollluting my email box!

Hygaboo Andersen said:

Meh,

All secular political ideologies are nothing but Darwin’s dingleberries. Justice can only be achieved by placing the Gospel at the center of all political discourse.

Then I take it you would prefer to live in a country like Afghanistan, Iran or Somalia, where you can be beaten or put to death for not being Godly enough, often without trial?

All the journals are in fact available free to anyone at any academic library (usually found on college campuses) Not every library will have every journal but they are staffed by librarians who know how to get any article you need. The advent of paid online subscriptions is a very recent development( less than 10 years) Before that all article reading was done in librarys. There is no conspiracy to restrict access, you simply need to go to a good library!

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This page contains a single entry by Nick Matzke published on July 29, 2010 7:07 PM.

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