The proximate–ultimate distinction and evolutionary developmental biology

frog developmentWhat is the relationship between developmental and evolutionary biology? This apparently simple question (aren’t developmental systems the result of evolution?) has been controversial for more than half a century, which strongly hints at the possibility that the question isn’t just a scientific one (though it is that too), but also has inescapable philosophical dimensions.

My colleague Raphael Scholl and I published a paper on this very topic a couple of years ago in the journal Biology and Philosophy, and I think it is worth revisiting some of our arguments and conclusions.

The influential biologist Ernst Mayr argued back in 1961 that biology, despite its seeming unity, is made up of at least two fields that differ in their choice of, and approach to, research problems. On the one hand, he recognized a discipline of functional biology, of which he wrote:

“The functional biologist is vitally concerned with the operation and interaction of structural elements, from molecules up to organs and whole individuals. His ever-repeated question is ‘How?’”

Then he contrasted this with the interests of the evolutionary biologist:

“His basic question is ‘Why?’. […] To find the causes for the existing characteristics, and particularly adaptations, of organisms is the main preoccupation of the evolutionary biologist.”

Mayr could be read as distinguishing between ‘‘how’’ and ‘‘why’’ questions; between causes acting in the past and causes acting in the present; between different types of causes; or between scientific disciplines.

For Mayr, functional biology is concerned with ‘‘the operation and interaction of structural elements,’’ whereas evolutionary biology studies ‘‘the causes for the existing characteristics’’, ‘‘the reasons for this diversity [of the organic world] as well as the pathway by which it has been achieved’’ or ‘‘the forces that bring about changes in faunas and floras.’’ He then assigns the label ‘‘proximate’’ to the former and ‘‘ultimate’’ to the latter. He specifies the ultimate causes further:

“These are causes that have a history and that have been incorporated into the system through many thousands of generations of natural selection.”

Back in 1961, Mayr used to proximate-ultimate distinction to argue for the continued relevance of organismic biology in the face of molecular approaches. Later on, however, in the 1980s, he began to deploy the distinction against evolutionary developmental biology:

“The suggestion that it is the task of the Darwinians to explain development […] makes it evident that [critics of the Modern Synthesis] are unaware of the important difference between proximate and ultimate causations […]. Expressed in modern terminology, ultimate causations (largely natural selection) are those involved in the assembling of new genetic programmes, and proximate causations those that deal with the decoding of the genetic programme during ontogeny and subsequent life.”

The proximate-ultimate distinction, then, is claimed to give rise to an explanatory asymmetry: evolutionary causes explain how the genetic programs underlying functional causes have changed across generations. But there is no comparable reverse relationship — functional causes are of no relevance to evolutionary causes.

In recent years there have been interesting criticisms moved against Mayr’s neat distinction of causes in biology. The most salient critiques are by R. Amundson (2005) and by K.N. Leland and collaborators.

Since natural selection invariably operates on developmental processes, Amundsen has argued that any account of an evolutionary transition is causally incomplete so long as it does not include the relevant developmental processes: “In order to achieve a modification in adult form, evolution must modify the embryological processes responsible for that form. Therefore an understanding of evolution requires an understanding of development.”

Raphael and I, however, argue that Amundson’s critique fails to offer a reason why developmental processes in particular should be of interest to evolutionary biology. On the criterion of causal completeness, we might also ask for a biochemical-evolutionary synthesis (since biochemistry is both continuously operating in organisms and changed by selection) or indeed a physiological-evolutionary synthesis. Some might argue that these are indeed needed, but we think it is possible to give good reasons why development in particular is of interest to evolutionists.

More promising at first sight is the critique of Mayr by Laland and colleagues who argue that the proximate-ultimate distinction ignores certain prevalent types of reciprocal causation: “In reciprocal processes, ultimate explanations must include an account of the sources of selection (as these are modified by the evolutionary process) as well as the causes of the phenotypes subject to selection.”

These authors’ paradigmatic case is niche construction, where selection creates organisms which alter their environment and thus, in turn, alter selection pressures. Laland et al. regard Mayr’s view as one of linear causation, where a series of genotypes are successively adapted to static selection pressures. In niche construction, however, there is a phenotype-mediated alteration of the selective environment, and thus reciprocal causation.

However, the criterion of reciprocal causation fails to pick out all the cases of interest, and only those. On the one hand, reciprocal causation is again too inclusive since it is ever present. On the other hand, reciprocal causation is not sufficiently inclusive: there are phenomena that are of great theoretical interest to developmental evolutionists but that are not neatly captured as instances of reciprocal causation.

Our thesis, which we defend in detail in the paper, is that it is a mistake to think about the proximate-ultimate distinction in terms of allegedly omitted biological causes. It is much more fruitful to think in terms of abstraction in causal explanations: the issue is not whether certain types of causation (e.g., between genotype and phenotype, or between phenotype and selective environment) exist, but whether these causal paths carry much weight in the explanations we give. We should not ask: Is there causation between genotype and phenotype? Of course there is. Or: Is there causation between phenotype and environment? Again, of course there is. We should ask instead what motivates the foregrounding or backgrounding of some parts of a complete causal account of any given evolutionary transition. The key concern is not causal relevance, in other words, but rather explanatory salience.

Mayr considered natural selection to be the main force in evolutionary explanations. Thus, he foregrounded selection and abstracted development, although both are uncontroversially part of a complete causal account of evolutionary transitions. The key question, then, becomes: Under what circumstances can selection be taken to be the main explanatory force in evolutionary explanations?

Raphael and I maintain that two issues have become conflated in this debate. The first issue is the proximate-ultimate distinction, which does not necessarily imply an explanatory asymmetry between evolution and development. We think a ‘‘lean version’’ of the distinction should be maintained, since it separates research agendas that are indeed concerned with different aspects of causation in nature: proximate questions about biological mechanisms are different from ultimate questions about the evolutionary processes that have produced these same mechanisms. Proximate and ultimate causes answer different contrastive questions. The proximate questions asks why this bird flies south in contrast to another, otherwise identical bird that lacks the same neural mechanism. The ultimate question asks why these birds fly south in contrast to another population of birds with a different history of natural selection.

The second issue is the claim that developmental mechanisms carry no force in evolutionary explanations. This is only true in cases where biological variation is isotropic (i.e., does not have preferential direction, no “developmental constraints,” to use Stephen Jay Gould’s phrase), and this empirical assumption is independent of the lean version of the distinction. On the assumption of isotropic variation, developmental mechanisms are indeed nothing but gory mechanistic detail in evolutionary explanations. When variation is not isotropic (and, it turns out empirically, it often isn’t), however, developmental causes do carry explanatory force in evolutionary transitions — and our lean version of the distinction is entirely compatible with this possibility. The task of proponents of the “evo-devo” (evolution of development) approach, then, has always been to argue not against the proximate-ultimate distinction, but against the generality of the isotropy assumption — to argue that some evolutionary explanations require us to foreground developmental mechanisms.

In summary, Raphael and I argue that the critiques of ‘‘causal completeness’’ and ‘‘reciprocal causation’’ of the proximate-ultimate distinction mentioned above fail because they do not reliably pick out those aspects of individual evolutionary episodes which are of interest to developmental evolutionists or experts in niche construction. Instead, the proper framing of the question concerns explanatory abstractions in causal models: under what circumstances is it appropriate for explanatory purposes to foreground or background certain aspects of the complete causal account of any given evolutionary transition? Ernst Mayr abstracted from developmental causes because he assumed isotropy of variation. In cases where this assumption is not warranted, however, developmental causes carry explanatory force and must be included. In other cases, interactions between the phenotype and the environment may carry particular explanatory force. This approach permits us a charitable reading of Mayr, whose focus on development-less natural selection can be seen as a special case where variation is isotropic. In the half-century since Mayr’s discussion of the proximate–ultimate distinction, it has become apparent that the isotropy assumption does not hold generally. Thus, developmental causes can carry explanatory force in both the proximate and the ultimate domain.

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Categories: Massimo's Technical Stuff, Philosophy of Science

22 replies

  1. Thanks for this piece. You clearly delineate the issues involved in attempting to answer the opening question, especially for someone like me who knows next to nothing on this matter, and, in so doing, help to sensitize the general reader to its importance and its implications.

    One thing that would be of further help to me and that could perhaps be covered in the commentary are some examples to illustrate your conclusion: “Thus, developmental causes can carry explanatory force in both the proximate and the ultimate domain.”

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  2. I need to think about this some more (not today though), but it is important to have this conversation. First, biologists can do biology without thinking about evolution, but should not forget that evolution is the unifying concept of the field. Second, reciprocal causation is a key step forward; it dispels the myth of organisms being pawns (not prawns) of the “environment”. The addition of development and physiology make evolution more dynamic. Having a fuller understanding of genetics and genotype-phenotype interactions is also important. I was reading some historical papers by Gregory Radick on views of WFR Weldon and the incorporation of a more inclusive view of genetics – more on the lines of that used in quantitive genetics – into undergraduate courses. Any way lots to think about.

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  3. Nice article, but difficult for the layman to get. I can’t see how you could ever disentangle development from evolution – they seem to be entwined in so many important ways.

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  4. Thomas Jones. I think an example and one that is still interestingly contentious is the development of the eye. I was taught, unambiguously, that eyes had developed independently several times. Today, I understand, it is thought that at least some common developmental pathways are involved in all cases and this is, in some sense, a constraint that natural selection has to work alongside?

    It is tricky and can depend, to some extent anyway, on what you count as an ‘eye’.

    I am not even sure what the current consensus is as a matter of fact. It is not as simple as I was originally taught for sure. What one used to be told was that, since the advantages of an eye are pretty obvious and significant, Natural Selection had just worked the same magic several times on the basic undifferentiated ‘clay’ of life, producing analogous results in each case. The “Universal Acid” you might say working on raw matter.

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  5. Ed Yong has nice article on eye evolution in last month’s National Geographic.
    http://ngm.nationalgeographic.com/2016/02/evolution-of-eyes-text

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  6. Massimo,

    Interesting article; but it is one of the more technical articles I’ve read from you here, so it will take some time to digest. I’m with Thomas Jones here, that more concrete examples would help.

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  7. Agreed this is one for the experts. Biology doesn’t frame easily.

    One point about complexity is that it does seem to cycle with simplicity, per Gould’s “punctuated equilibrium.” Life expands by filling out ever more refined niches and grows ever more complex, but resets when these structure collapse, leaving residual complex states to then propagate.

    Which means lots of the record is erased.

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  8. Thomas et al.,

    yes, sorry, the article is a bit hard to chew, but that was part of the point. Occasionally, I like to give people a taste of what actual philosophical literature looks like, as opposed to the facile caricature provided these days by a certain number of scientists of which I’ve talked ad nauseam in the past…

    Anyway, yes, examples. In the paper Raphael and I actually examine in detail two instances of fuzzy boundary between evolutionary and developmental biology: digital reduction in amphibians and the origin of pigment patterns in Drosophila.

    From the paper, about the first example:

    “The empirical study presented by Alberch and Gale consists of comparisons within and among two orders of amphibians: plethodontid salamanders and anuran frogs. The trait of interest is loss of phalanges in the extremities. In short, the authors are able to show that the pattern of phalangeal loss is similar in species belonging to the same order, but different among orders. They further show that different morphologies within the same order can be reproduced experimentally by varying a single developmental parameter: size (= number of cells) in the limb bud, which can be manipulated by the (reversible) application of colchicine to the developing limb bud. For example, treatment of the limb bud of the salamander Ambystoma mexicanum with colchicine results in the loss of various phalanges in such a way as to mimic the (normal) morphology of the related species Hemidactylium scutatum … [this kind of] examples illustrate a general methodology for demonstrating the need to foreground developmental processes in evolutionary models. What is not produced is evidence related to optimality—either evidence that a given feature is non-optimal or that some other structure would be optimal. What is produced is evidence that the feature under investigation (adult limb morphology) is a function of a developmental factor (limb bud size), and that the existing adult limb morphology can thus be interpreted as a side-effect of selection on body size alone. Such causal claims can be supported by experimental data which demonstrate the relevant developmental relationships. Any additional explanations of the foot morphology by natural selection are not so much ‘‘disproved’’ as made redundant.”

    That is: in these cases it is developmental constraints, not natural selection, that do most of the explanatory work. Hence the need for – sometimes – taking development into account when producing evolutionary explanations.

    Robin,

    “I can’t see how you could ever disentangle development from evolution – they seem to be entwined in so many important ways.”

    Yes, they are. But what Raphael and I show is that sometimes development can, indeed, be moved to the background, because it doesn’t really play a major role in evolutionary explanations (which is what Mayr argued), while at other times (see example above) it is necessary, since without it one is left with just-so adaptive stories.

    Tudor,

    “I was taught, unambiguously, that eyes had developed independently several times. Today, I understand, it is thought that at least some common developmental pathways are involved in all cases and this is, in some sense, a constraint that natural selection has to work alongside?”

    Right, the same goes, for instance, for the evolution of a fusiform body in fast swimming animals. Likely, squids evolved it independently of fish, but it isn’t as clear that so did marine cetaceans, since they are vertebrates, and share a very similar set of developmental features with fish.

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  9. Massimo,

    “Such causal claims can be supported by experimental data which demonstrate the relevant developmental relationships. Any additional explanations of the foot morphology by natural selection are not so much ‘‘disproved’’ as made redundant.””

    Isn’t this an expression of “nature vs. nurture,” with development as nature and natural selection as nurture?

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  10. brodix,

    “Isn’t this an expression of “nature vs. nurture,” with development as nature and natural selection as nurture?”

    Not exactly, though the nature-nurture debate has some bearing here. Development is the result of interactions between genes and environments — where the latter are not just the external thing, but also the environment internal to an organism, e.g., created by surrounding cells and tissues.

    And of course natural selection does result in the alteration of gene frequencies, but within an environmentally specific context. Change the environment and the selective pressures will change or even disappear or reverse themselves.

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  11. Massimo,

    “And of course natural selection does result in the alteration of gene frequencies, but within an environmentally specific context.”

    So it’s still that outward organic force, encountering resistance, responding to it, incorporating feedback, then repeated and folded through endless numbers of times, through tens and hundreds of millions of generations, but still the basic dichotomy of force and resistance?

    Not trying to simplify it, because for the professional, the devil is in the details, just trying to see if the pattern applies.

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  12. Yes, a good read!

    I wonder if length of time over which we can pick out correlations between objects is a useful way to think. So correlations in lifestyle or physical form of organisms separated by many generations can be genetic, but also reflect continuing stability of environment. The environmental stability does not reflect a causal chain from E1 to EN, rather “ultimate” geology etc. The connection between genotypes from generation to generation does seem directly causal, though “pruned” by selection.

    By contrast, “proximate” causation involved in organismal homeostasis and behavioural adaption to environment is over short time periods.

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  13. brodix,

    “So it’s still that outward organic force, encountering resistance, responding to it, incorporating feedback, then repeated and folded through endless numbers of times, through tens and hundreds of millions of generations, but still the basic dichotomy of force and resistance?”

    Uhm, not sure how to translate that language into something a biologist would recognize, so I’ll have to say maybe.

    …,

    “By contrast, “proximate” causation involved in organismal homeostasis and behavioural adaption to environment is over short time periods”

    yes, but the important point is that the distinction between proximate and ultimate causation isn’t dichotomous, but rather a continuum.

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  14. To riff on your comment on Gould, prior developmental issues constrain, or channel into certain pathways, likely future development (barring a massive, and massively lucky set of genetic mutations), Massimo? And from there, evolutionary development’s natural “conservatism” takes over?

    Hence, the need for ultimate vs proximate to be no more than “lean.”

    (And, obviously, this is the place where the role of epigenetics, still being investigated, comes into play as well.)

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  15. Massimo,

    I think Niko Tinbergen had a useful conception of the proximate-ultimate continuum. His view was that there are four categories of explanation of a given behavior. Going from proximate to ultimate they are causation, development, function and evolution. All four can yield valid explanations of why a behavior occurs; it just depends on what questions you’re interested in. For anyone interested in behavior and evolution, Tinbergen is a good place to start.

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  16. August: ” . . . there are four categories of explanation of a given behavior. Going from proximate to ultimate they are causation, development, function and evolution. All four can yield valid explanations of why a behavior occurs; it just depends on what questions you’re interested in.”

    Some clarification needed . . . So, if I go to an opthamologist and he runs some standardized tests on the basis of which he concludes that my vision is either functional or dysfunctional depending on whether it meets or exceeds some standards, he is addressing a given behavior? This is confusing to me.

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  17. Massimo,

    I certainly agree there is an enormous gap between the experts and the general public, so I’m just trying to pick out some points to see patterns I might understand and see if they make any sense to you.

    “For Mayr, functional biology is concerned with ‘‘the operation and interaction of structural elements,’’ whereas evolutionary biology studies ‘‘the causes for the existing characteristics’’, ‘‘the reasons for this diversity [of the organic world] as well as the pathway by which it has been achieved’’ or ‘‘the forces that bring about changes in faunas and floras.’’”

    The distinction seems to be between the historical narrative and the present state.

    “More promising at first sight is the critique of Mayr by Laland and colleagues who argue that the proximate-ultimate distinction ignores certain prevalent types of reciprocal causation: “In reciprocal processes, ultimate explanations must include an account of the sources of selection (as these are modified by the evolutionary process) as well as the causes of the phenotypes subject to selection.”

    These authors’ paradigmatic case is niche construction, where selection creates organisms which alter their environment and thus, in turn, alter selection pressures. Laland et al. regard Mayr’s view as one of linear causation, where a series of genotypes are successively adapted to static selection pressures. In niche construction, however, there is a phenotype-mediated alteration of the selective environment, and thus reciprocal causation.”

    The point I see as important to this relationship is time as the narrative effect, versus the present state as a physical process, in which thermodynamics is as important than temporal cause and effect. Given the high and low pressures of the organism relating to its environment both push and pull in cyclical and reciprocal actions, which do not model into the historical narrative, other than as a layering effect, as time is physically reductionistic.

    Hopefully this makes some sense. Not only has the day been a mess, but lost electricity and what I’d first written.

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  18. Thomas,

    Sorry, I should have explained more. Tinbergen was an ethologist (as was I, in part of my working career) and thus interested in the evolution of behavior in animals. I’m not sure that functional or dysfunctional vision would be classed as behavior, but in general these categories should work for most biological characteristics.

    In visual perception, if I’m interested in proximate causation, I’d be looking at how light interacts with rods and cones and the resultant neural pathways that lead to sensation. A bit less proximate, I’d look at the development of the visual system and try to determine how visual sensations come about through the development of the eye and visual pathways during maturation. Less proximate would be determining the function, to the animal, of the visual system (although with such a centrally important system I wouldn’t expect there to be one simple function). Finally, I could try to determine how the system evolved through time. Any of these explanations could be an answer to the question of why do I see things that are put in front of me.

    These classes of explanation are more clearly seen in looking at behavior more traditionally studied by ethologists (or behavioral ecologists). For example, when looking at courtship and agonistic displays in various species. Similarly, the same approaches could be used to investigate animal coloration, although in this case causation and development would be hard to disentangle.

    I hope I haven’t misunderstood your question.

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  19. August, some good thoughts.

    Two analogies might help elucidate Massimo further.

    One, per what I’ve said before on volition and other things, is that “proximate” and “ultimate” are not two disjunct polarities, but two ends of a sliding scale.

    Another is, to use photography, that one is more of a wide-angle lens and the other more of a telephoto lens.

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  20. Thanks, August. That’s very kind of you and much more than one might expect. Yes, it’s helpful. The use of word behavior caught my eye, so to speak. I’m afraid my concerns come much later in this chain of explanation. Chicken and egg stuff and “why” some question is even posed in a particular way, as opposed to “how” it is answered. The why seems sometimes inextricably inexplicable with the how being proposed as a substitute without acknowledging it as such. I have concerns with this matter, whether it’s constructed as proximate to ultimate or vice versa.

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  21. Massimo,

    I guess I better specify that, in that evolutionary biology is what has occurred over time, while developmental biology which occurs in the present state.

    So the linear causality is the why, while the reciprocal/cyclical/feedback relationship of entities and environments in the present, is the how.

    “sometimes development can, indeed, be moved to the background, because it doesn’t really play a major role in evolutionary explanations (which is what Mayr argued), while at other times (see example above) it is necessary, since without it one is left with just-so adaptive stories.”

    So development is distilled into the resulting effect, thus causality and “can, indeed, be moved to the background.”

    “without it one is left with just-so adaptive stories.””

    Aka, rationalizations, as linear narratives are imposed onto far more complex events.

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  22. Michael, thanks for the link on Ed’s piece. Fascinating, and updates my knowledge. It’s bookmarked.

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