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    Burrowing by Way of Genes: Mice provide clues to genetics of behavior
    By Kenrick Vezina | January 23rd 2013 03:52 AM | 13 comments | Print | E-mail | Track Comments
    About Kenrick

    Kenrick Vezina is a science writer and amateur naturalist with expertise in zoology, evolutionary biology, and natural history. He completed his...

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    An oldfield mouse.Our behavior is critically linked to our genetics but the relationship remains murky. Genes, by constructing our brain and nervous system and by regulating our hormones, influence behavior — in humans and in all animals.

    Ironically, the science is the least clear where the connection between genetics and behavior should be, in theory, the most direct — in cases of “hard-wired” behavior such as the construction of beehives or the courtship rituals of some bird species or a human infant’s rooting; behaviors that are common across a species without having to be taught. Instinct.

    Biologist-author Richard Dawkins put forth the highly controversial idea, in his 1982 book The Extended Phenotype, that we should stop assuming that the phenotype — the outward expression of an organism’s genes — end with, for instance, the fur on a beaver’s back. If genes also influence the beaver’s behavior, and therefore its dam construction, we should consider the length of a given beaver’s dam as valid a measurable product of the beaver’s genotype as the length of its tail. This is the extended phenotype.

    Many scientists contest this view. However, in what appears to be a confirmation of some of Dawkins’s theory, a recent paper in Nature demonstrated that a handful of discrete genetic modules are responsible for the burrowing behavior in two closely-related, mice species: oldfield mice and deer mice. The researchers explicitly chose burrows as an extended phenotype; they were working in the intellectual context Dawkins proposed.

    The study, by Harvard zoologist Hopi Hoekstra and her team, has already been reported on in an excellent piece at Ed Yong’s National Geographic blog, Not Exactly Rocket Science. Here’s here’s the study in brief:

    
Captive-bred mice, even those with no previous exposure to sand, demonstrated the same burrow construction behavior as their wild counterparts. This must be a genetically controlled behavior. So the scientists crossed oldfield mice, which build escape tunnels in their burrows, with deer mice, which do not, and end up with an entire generation that built burrows matching that of their oldfield mice parents — including the escape burrow.

    Some of you may recognize in this pattern the simple dominance of Mendelian genetics, except in these crosses we’re not dealing with pea color or shape but the complex behavior of an animal. To push behavioral genetics forward, these researchers dug into the same breeding toolkit that Gregor Mendel used a century-and-a-half ago to found the field.

    The researchers then back-crossed the hybrid mice with deer mice, and analyzed the genotypes of the mice they were working with to identify regions associated with the observed behavioral changes. Ultimately, they came to the conclusion that burrowing behavior is controlled by a remarkably small number of genes packaged into discrete modules. One module, for instance, influences whether or not the mice will build escape tunnels, and just because a given hybrid inherits the module for an escape tunnel (an oldfield mouse trait) does not mean it will make a burrow of the same dimensions as oldfield mice.

    The team’s next step is to narrow identify precisely which genes, rather than regions of DNA, influence borrowing behavior in these mice, and to what extent.

    Aside from linking classical genetics and traditional breeding experiments to modern molecular genetics and behavioral studies, Hoekstra’s work opens a door to a wide range of possibilities, not least of which is addressing the question of how genes influence our own extremely sophisticated behavior. It’s not hard to imagine this study as tugging at strands that connect mouse burrows to beaver dam to, to Gorilla nests, and eventually to whatever genetic impetus allowed mankind to become the greatest builders natural history has ever seen.

    In The Extended Phenotype, Dawkins wrote, “The extended phenotype may not constitute a testable hypothesis in itself, but it so far changes the way we see animals and plants that it may cause us to think of testable hypotheses that we would otherwise never have dreamed of.” Twenty-one years later in 2004 he wrote that, as far as he knew, “nobody had done a genetic study using animal artefacts [sic] as the phenotype.”

    Thirty years later, it was not beavers (one of which sits on the cover of my 1999 edition of The Extended Phenotype) but another rodent that provided the first empirical work suggesting the utility of Dawkins’s idea.

    Reprinted from Genetic Literacy Project GeneTrends: Human newsletter.

    Comments

    Gerhard Adam
    The problem I have with the "extended phenotype" is that it doesn't make any predictions.  It is simply an "after the fact" explanation.  One cannot simply look at a behavior and determine its heritability, so once a behavior is confirmed as being genetically derived, it is simply a phrase that we can attach to it; maybe. 
    Mundus vult decipi
    Rickken
    Perhaps that makes the book more a work of philosophy than science, and that's a completely valid issue, but it seems to me if biologists influenced by the perspective offered are able to come up with novel experiments then the idea has contributed, somehow, to the goals of science.


    And, in this case, the authors of the study themselves framed their work in terms of the extended phenotype. It would seem they were influenced by the ideas of the book to pursue this line of research.

    My point is, I suppose, that I recognize your issue with the idea but am still rather baffled as to why so many in the biology or larger science community take such issue with the idea. I'd love to hear more; I'm sure there's a lot I don't know.

    (Thanks for the first comment on my first post, by the way.)

    Gerhard Adam
    Well, first of all, you're welcome and welcome to the site.

    While I can appreciate the authors of the study perhaps being influenced by the idea of the extended phenotype, I still believe that this line of research would have been pursued regardless of what it was called.  After all, if we are going to attribute instinctive behaviors to genetic influence, then it is only a question of who goes looking before that line of research is pursued.

    I suppose one of the issues that occurs is that there may be a temptation [as is often the case in evolutionary psychology] of where we look at a behavior and suddenly begin to invent all manner of evolutionary and/or genetic explanations for it.

    In truth, one would expect that such specific genetic influences would be quite rare in terms of their pervasiveness.  I expect this is precisely why we see the evolution of nervous systems and larger brains, so that learning from experience becomes a much more secure vehicle of ensuring survival, rather than relying on genetically imprinted behaviors.  So, even at its best, the extended phenotype can only explain a relatively small subset of behaviors that we see.  Then again, is it really an explanation?  Isn't the "extended phenotype" simply a substitute phrase for what we always called "instinctive behavior"?
    Mundus vult decipi
    Rickken
    Thank you!

    "Extended phenotype" is not quite a synonym for "instinctual behavior, though. The concept of an extended phenotype isn't limited to instinctive behaviors. Just the opposite. I think it prompts us to consider the genetic underpinnings of complex behaviors that are not immediately obvious as "instinct."

    It's easy to look at, say, the complex suite of human behavior and chalk it all up to cultural evolution, learning, post-gene factors. But there must be some line that can be drawn from, say, human skyscrapers to human genes. Surely it's a very, very long and complicated line with uncountable other factors having a larger, more direct, more recent effect than a handful of human genes. Perhaps I am putting my own spin on the idea, but my interpretation of the "point" of the extended phenotype isn't to provide an explanatory label so much as to put us in mind of that complicated line that links even the most complex behaviors to something genetic.


    Perhaps this "line" is terribly obvious to those steeped in biology and evolutionary science, so the idea of an extended phenotype just seems redundant. As you said: this research would probably have been pursued regardless of Dawkins's book.
    Gerhard Adam
    But there must be some line that can be drawn from, say, human skyscrapers to human genes. Surely it's a very, very long and complicated line with uncountable other factors having a larger, more direct, more recent effect than a handful of human genes.
    You bring up an excellent point, so let me address it in the manner I see these things.  We often hear about human intellect and how evolution has shaped us which invariably leads many people to look at our modern society.  Yet, I would submit that biological evolution had NOTHING to do with it.  We are not appreciably more intelligent than our ancestors of a few thousand years ago, and I would argue that we probably aren't any more intelligent than our ancestors of 50,000 years ago. 

    Intelligence, in this sense, meaning the innate abilities of the brain.

    In fact, we have hundreds of examples of people all over the planet that have the same intelligence, yet couldn't put a man on the moon.  So what's different?

    My take is that the difference is our extreme division of labor, not our intelligence [i.e. biology].  In other words, we leveraged our intelligence by only requiring each individual contribute a small part to the whole, and this is what allowed us to achieve our modern society.  It's all a matter of social organization. 

    This is a similar argument I use regarding the existence of intelligent life elsewhere in the universe.  The point isn't intelligence, but rather the social organization necessary to even consider a space trip and the means/infrastructure necessary to consolidate all the required skills and resources to put it together.

    This isn't a function of biology, but rather social/cultural evolution. 

    Now if you want to argue that genetics played a role in our cooperative nature, which ultimately lead to this type of organization, you could certainly try, but you'd have a tough time explaining why it hasn't occurred in numerous other societies.  In fact, there are some studies indicating that perhaps human intelligence has peaked or is even declining, which would be supported by this idea, since our social organization, has effectively enabled us to behave like a massively parallel processing system, where individual brainpower isn't as important as the cooperative effort.

    http://www.science20.com/gerhard_adam/why_arent_we_smarter-85388
    Mundus vult decipi
    Rickken
    Well this won't be as interesting, but let me start off by emphatically agreeing with you as far as the important of social and cultural evolution goes for the success of mankind. Heck, it's the topic of of a book I would very much like to write, making more or less all of the points you make here.
    My only point of contention is that, for us to get to the point where cultural evolution could take off, we needed to achieve certain milestones in biological evolution. This will be where to look for the more direct parallels between what's going on in this mouse study and with human evolution. To say that biological evolution has "nothing" to do with human success would seem an overstatement.

    I know the "line" I'm talking about is probably clearest at some point earlier in our development a a species. I don't mean to discount the other factors that lead to humans on the moon or their importance, simply to point out that this line must logically exist in some form (however hazy) and this mouse study, as I said, seems to tug at it.
    Gerhard Adam
    To say that biological evolution has "nothing" to do with human success would seem an overstatement.
    Actually, I don't think so, because we have the evidence all around us.  We have modern people living all manner of lifestyles ranging from aboriginal hunter-gatherers, to those of us living in modern society.  My point is that evolution didn't stop for humans, yet we have this vast chasm separating the two.  Without a particular accident of culture that motivated our particular social organization, we could just as readily have remained hunter-gatherers, or some other variation [as many of the Native Americans were even a few generations ago]. 

    If we want to argue about a genetic component, then we would have to explain that kind of cultural difference in our present history.  So, genetically, I can accept the idea that we have a certain propensity for cooperation, which is undoubtedly linked even further back to more primitive primates.  However, I'm not prepared to go much beyond that, because there is no evidence to suggest that there is any basis for presuming that one particular culture exists because of genetic influence.
    Mundus vult decipi
    Steve Davis
    Kenrick, thanks for providing a link to my criticism of The Extended Phenotype.
    Unfortunately, nothing you have presented convinces me to recant.
    Allow me a few comments.
    "Genes, by constructing our brain and nervous system..."
     Genes do not do that.
    Construction of such complex structures is an activity of a living entity; genes are not alive.
    "If genes also influence the beaver’s behavior, and therefore its dam construction, we should consider the length of a given beaver’s dam as valid a measurable product of the beaver’s genotype as the length of its tail."
     Not so. A beaver, like a human, will build where it can, not where it wishes. It's dam will therefore be a product of the local environment as much as the industry of the individual builder.
    "Captive-bred mice, even those with no previous exposure to sand, demonstrated the same burrow construction behavior as their wild counterparts. This must be a genetically controlled behavior."
    Not so.
    Just as the beaver dam is influenced by the local environment, and by the physical features of the beaver, so it is with burrowing mice. The behaviour is influenced in part by genes, but it is simply not correct to say that it is a "genetically controlled behaviour." All traits, including behaviours, are products of the phenotype, not the genes. Mice will burrow (presumably for protection or nesting) according to the nature of the material in which they burrow, and the nature of their physical features, eg, size, strength of claws etc.
    If mice burrowing is genetically controlled, you must also assume that rabbit burrowing is genetically controlled behaviour. And if so, they will burrow regardless of other factors. But they do not. Rabbits in tropical regions do not burrow, although they are identical to burrowing rabbits.
    Behaviours are products of phenotypes and environments.  
    Rickken
    Thankfully, I wasn't trying to convince you to recant. But you do make some excellent points, and I want to respond as best I can.
    Construction of such complex structures is an activity of a living entity; genes are not alive.

    You're right, genes are not what constructs, in an active sense, the nervous system. This is really, I think, a case of imprecise word choice on my part. Would "genes influence the construction" be an acceptable way of phrasing it? Same with genetically controlled. What if I said the behavior was "relatively highly heritable."


    With regard to your second two criticisms, here's where I become stumped. It seems we're disagreeing more about semantics than about facts, because we both agree that behaviors are the product of phenotypes interacting with the environment.

    What, then, is the connection between genotype and phenotype? If, on some level, the genes provide the instructions for the construction of an organism, including the phenotype which creates traits through interaction with the environment, would the genes not be essential to the existence of the behavior? I don't mean to discount the importance of mice as an organism; I actually find myself generally lamenting a perceived shift away from appreciating the importance of the whole organism (read: phenotype with influence from environment) in biology. But it seems without the genes you couldn't have the mouse and therefore couldn't have the behavior. So I'm more than happy to cede that "controlled" is not the right word, but there also seems to be a necessary and important role for genetics.

    Why, then, not call it the "extended phenotype" and acknowledge that once we've extended the phenotype this far out into the world environmental factors such as the presence of absence of sand will have a much more direct and immediate effect on behavior and artefacts of behavior than genes. I may now be making my OWN version of Dawkins's argument, but he's welcome to show up and defend whatever he had in mind whenever he likes.
    Steve Davis
    Kenrick : "Would "genes influence the construction" be an acceptable way of phrasing it?"
    Certainly!
    "What if I said the behavior was "relatively highly heritable.""
    Yes, but it's important to not lose sight of the fact that there's a lot more to behaviours than inherited traits.
    "...we both agree that behaviors are the product of phenotypes interacting with the environment. What, then, is the connection between genotype and phenotype?"
    A good question, but one that was avoided by Dawkins. His focus was genes, not the genome. There is a huge difference between the two. 
    If, on some level, the genes provide the instructions for the construction of an organism, including the phenotype which creates traits through interaction with the environment, would the genes not be essential to the existence of the behavior?
    But they don't provide the instructions.
    And this is where word meanings become so important and word usage needs to be precise.
    It's the genome, operating as the "heart" of the primary level of life - the cell - that instructs for construction.
    The genome is not, as the gene-centrics assume, just a collection of genes that come together and work for their own ends.
    A gene is not even an entity in itself!
    It is a portion of a molecule, and even that definition is debatable.
    "But it seems without the genes you couldn't have the mouse and therefore couldn't have the behavior."
     True, but as Gerhard has pointed out in previous discussions on this matter, if you wish to be so reductionist as to consider the gene to have primary importance in evolution, or in this case, behaviours, then why not go all the way and talk of the importance of carbon? We would not have behaviours without carbon, so carbon must be the most important factor! Does that make sense?
    Of course not, and so it is for genes.
    "Why, then, not call it the "extended phenotype" and..."
    Because Dawkins was not talking about phenotypes at all, despite the title of the book.
    His focus was genes, his aim was to establish genes as the most significant feature of life and evolution.

    But let's look at the genome again.
    There's a couple of reasons why gene-centrics avoid discussion of the genome, preferring to focus on genes.
    One is that the genome is a hive of cooperation, non-stop cooperation in fact, while gene-centrism is all about presenting selfishness as the principal driver of life.
    The other is that if they discuss the genome, they have to discuss life itself, a topic that they cannot handle.
    "I actually find myself generally lamenting a perceived shift away from appreciating the importance of the whole organism (read: phenotype with influence from environment) in biology."
    That's good! Go with your instincts!
    Gerhard Adam
    Would "genes influence the construction" be an acceptable way of phrasing it? Same with genetically controlled. What if I said the behavior was "relatively highly heritable."
    Here's the problem.  Genes aren't always expressed [as in epigenetics], and even those genes that are, will produce wildly different results based on all manner of variables regarding the regulatory mechanisms.  So, even invoking genes already creates difficulties. 

    With only a few percentage points separating mice from chimps from humans, you can see that genes tell us little or nothing about these differences.  It is genetic expression that is the important piece.

    As for the high heritability, I think you have a problem. Heritability is only relevant when one considers differences in a population.  Then one can examine whether those differences are influenced primarily by genetics or by the environment.  High heritability means that there are large differences in behavior caused by genes that can be selected for.  I don't see it.  It's generally considered a truism that people are the same all over the world, which indicates that behavior is NOT highly variable [and therefore not heritable] and consequently behavior is fundamentally fixed in the population with differences being accounted for by the environment [i.e. nurture].
    What, then, is the connection between genotype and phenotype?
    Difficult if not impossible to assess.  In other words, no matter what gene I point to, you can tell me little about the phenotype that will actually get produced.  You can tell me what it SHOULD do, but not what it will do.  You don't know anything about how it will be expressed, if it will be expressed, or how much it varies based on regulatory controls.
    ...would the genes not be essential to the existence of the behavior?
    Why should they be?  Are genes necessary to be a marathon runner, or are they only necessary to produce the muscles attached to the bones?  I may have the genes of an Arnold Schwarzenegger, but if I don't actually get to the gym to lift weights, then that will remain completely unknown.  With something like behavior, the problem is even more nebulous, because you would have to demonstrate that behavior is something that is absolutely dependent on a particular genetic expression [this may work for escape tunnels, but no so much for skyscrapers].  It is insufficient to presume that because the genes regulate the creation of the brain and nervous system, that [by default] they must also be credited with behavior.
    But it seems without the genes you couldn't have the mouse and therefore couldn't have the behavior. So I'm more than happy to cede that "controlled" is not the right word, but there also seems to be a necessary and important role for genetics.
    True, as far as it goes, but not accurate.  A mouse will have a brain, heart, stomach, etc. which consists of cells which all  have exactly the same genes, yet they all look different and perform different functions.  How is that unless genes are not absolute?  More specifically you couldn't have the mouse if the materials to produce the proteins didn't exist.  Wherever you want to draw the line, there is clearly something that you could point to and claim that it is absolutely critical for the creation of the mouse.  However, that would be incorrect without all the elements, not only being present, but also working together as required.  After all, what separates a live mouse from a dead one, is the maintenance of these processes, otherwise the 2nd law of thermodynamics kicks in and your entropy increases to its maximum [i.e. death].

    An interesting book for you to read is Evolution in Four Dimensions, Eva Jablonka and Marion Lamb.  There's an excellent section that describes the problem of genes and phenotypes by giving an example of a world [i.e. in this thought experiment] of where all these different animals exist and yet they all have exactly the same genes.  Their point being that the phenotype is determined by epigenetics and the expression of the genes, while the genes themselves only provide general information.  As mentioned previously, it is the regulatory parts that determine how a gene actually manifests.

    BTW, this doesn't even consider an even more interesting factor, which is the microbiota that each animals is dependent on.  Talk about an extended phenotype ... :)
    Mundus vult decipi
    Recommend two books:

    The Flexible Phenotype, by Piers Thiesma (sp?)
    and
    The Plausibility of LIfe, by John Gerhart.

    Gerhard Adam
    The Plausibility of Life is a great book!
    Mundus vult decipi