How to study adaptation the proper way

One of the recurring discussions in evolutionary biology is the question of how to test adaptive hypotheses. Creationists often claim (wrongly) that the theory of natural selection is tautological, and so did, at some point, prominent philosopher of science Karl Popper (he later acknowledged that his comment was based on a misunderstanding of the theory, something that creationists strangely neglect to mention whenever they quote him in their favor — see this short essay I wrote about it for Skeptical Inquirer). And then, of course, there is the never ending issue of the quasi-scientific status of evolutionary psychology, precisely because adaptive hypotheses are particularly hard (though not impossible) to test in the case of Homo sapiens (more on this below).

It was therefore with delight that I recently happen to stumble on a paper by Mark Olson and Alfonso Arroyo-Santos entitled “How to study adaptation and why to do it that way: adaptation, just so stories, and circularity,” published in the prestigious Quarterly Review of Biology (pdf freely available here).

The basic argument put forth by Olson and Arroyo-Santos is that “circularity” comes in degrees, from vicious to virtuous, which is why they prefer the term “loopiness,” as in feedback loops between hypotheses and empirical evidence. Perhaps the best way to get what they are saying is to examine a few of their figures.

This one is a summary of the standard adaptationist story about why giraffes have long necks:

If you start with the observed pattern (lower portion of the figure), you will agree that, observationally, modern giraffes have long necks and they feed from tall trees. Based on that, you infer (upper portion of the figure) that the following things were true of the ancestors of modern giraffes: (i) they varied in neck length; (ii) this variation was heritable; (iii) short-neck giraffes had less access to food (functional argument); and (iv) short-neck giraffes, as a consequence of their phenotype, had lower fitness (adaptive argument).

The problem is, up to this point you have absolutely no evidence for any of inferences (i)-(iv) above. Which truly does make your “explanation” a just-so story.

But wait!, say — correctly — Olson and Arroyo-Santos, this can be the beginning of a fecund research program, because you can turn (i)-(iv) into hypotheses to be directly or indirectly tested.

For instance, evidence for (i) may be found in the fossil record; evidence for (ii) in extant populations (which would license the inference, though obviously not prove, that this was the case also in the past); (iii) may be tested directly in extant populations, or indirectly via optimization models; and (iv) is a reasonable conclusion from (i)-(iii), and therefore acceptable in direct proportion to the strength of the evidence in favor of (i)-(iii).

If you ponder the above for a minute you will realize why this shift from vicious circularity to virtuous loopiness is particularly hard to come by in the case of our species, and therefore why evolutionary psychology is, in my book, a quasi-science. Most human behaviors of interest to evolutionary psychologists do not leave fossil records (i); we can estimate their heritability (ii) in only what is called the “broad” sense, but the “narrow” one would be better (see here); while it is possible to link human behaviors with fitness in a modern environment (iii), the point is often made that our ancestral environment, both physical and especially social, was radically different from the current one (which is not the case for giraffes and lots of other organisms); therefore to make inferences about adaptation (iv) is to, say the least, problematic. Evopsych has a tendency to get stuck near the vicious circularity end of Olson and Arroyo-Santos’ continuum.

Here, by contrast, is an example of what virtuous loopiness looks like, in the case of the observation that swimming animals tend to have streamlined bodies, regardless of their taxon and phylogenetic relatedness:

You can appreciate the much more clear distinction between the initial observation of a pattern (lower right), the development of a number of assumptions necessary to explain the pattern (upper right), and three types of empirical evidence that feed into the other two components (left side of the figure).

Let us take a closer look at that last bit. Olson and Arroyo-Santos argue, again, correctly, that there are fundamentally three types of evidence that bear upon any adaptive hypothesis: from the comparative method, from population biology, and from optimality considerations.

The comparative method has to do with contrasting large number of species with different degrees of phylogenetic relatedness. The methodology has been fine tuned decades ago, including the development of sophisticated statistical approaches and the use of computer simulations to assess how well different methods of phylogenetic reconstruction work. This is another area where evopsych suffers, however, since there are very few and widely scattered “close” relatives of our species (no other Homo surviving, a couple of species of chimpanzees and the gorillas, separated from us by several million years of independent evolution).

Population biology is a very broad field at the interface among ecology, evolutionary biology and genetics, again characterized by well honed methods that rely on basic population and quantitative genetic theory. This is where our estimates of population variation (and hence also heritability) come from.

Optimality modeling has to do with applying biomechanical considerations to the study of adaptation, developing quantitative assessments of how well certain biological structures — and their variants — perform their function in response to pertinent environmental stimuli. In the case of the streamlined bodies of fish, marine mammals, and some invertebrates like squids, the pertinent theory comes from hydrodynamics.

The third figure, also from the Olson and Arroyo-Santos paper, explains how the loopiness of adaptive explanations works in the recurring case of discussions about the relative roles of natural selection and developmental constraints:

These two classes of explanations of biological structures are too often, even by biologists, considered to be mutually exclusive, and indeed sort of divide evolutionary biologists from developmental biologists, as well as “externalists” (who favor external causes, like natural selection) from “internalists” (also known as structuralists, who favor internal causes, like developmental constraints).

But Olson and Arroyo-Santos rightly point out that this is yet another case of loopiness: in the figure, they show a typical scattergram that hints at a strong linear correlation between two traits, X and Y (say, body size and antler size in the famous “Irish elk,” see figure at top of post). The typical question is: why do the data points line out that way within the phenotypic space defined by the two variables? Why the empty spaces of unrealized phenotypes (say, of large bodied elks with small antlers, or small bodied ones with very large antlers)?

Each of the two alternative explanations, that the empty spaces are explained by the fact that some morphologies are maladaptive, or that they are developmentally inaccessible (i.e., there is no way for the organism in question to build that phenotype, given its genetic-developmental matrix) are testable by stretching the initial circularity into the same sort of loopiness we’ve seen before. Moreover, the two are not mutually exclusive, since developmental constraints can limit, but not nullify the action of natural selection, and selection in turn may favor a genetic-developmental matrix that precludes the accidental invasion of maladaptive areas of phenotypic space. There are, in fact, many examples in the literature of this sort of analysis, and they represent some of the best achievements of modern evolutionary biology.

Here is how Olson and Arroyo-Santos then conclude their excellent paper:

“Studies of adaptation would necessarily seem to require the sort of loopy reasoning [presented in this paper]. Recognizing how adaptationist explanations are structured in actual practice helps give clarity to problems that have plagued biology, such as debates over tautology/circularity, and resolve false conflicts, such as the mutual scorn that often characterizes the adherents of the comparative, population/quantitative genetics, and optimality approaches. Instead, as providers of complementary sources of direct evidence, no single approach has a monopoly on tests of adaptation. An understanding of the real, loopy structure of evolutionary explanation encourages biologists to discuss truly substantial issues awaiting attention, such as how to identify the population of hypotheses from which to select the ‘best’ explanation, how scientists know the best explanation when they see it, or how best to weave disparate sources of evidence into a single explanation. By accepting that studies of adaptation require multiples types of direct evidence, evolutionary biologists can improve current research practice by designing a compelling and long-overdue integration of comparative, populational, and optimality approaches.”

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Categories: Philosophy of Science

51 replies

  1. We can test suggestions of fitness by modelling possible outcomes, as in the case of the streamlined Marine mammals. But how do we identify developmental constraints? We know that whatever happens must be developmentally possible; for example, it must be developmentally possible for the hind limb bud in developing porpoise embryo to be reabsorbed. But how do we test the suggestion that this or that possible adaptation does not happen because it is developmentally inaccessible?

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  2. Paul,

    There is a number of ways to address the issue of developmental constraints. In some cases we know enough about the genetic machinery and/or the way development unfolds to be able to tell. For instance, we know that any vertebrate that has evolved wings has done it out of its forelimbs, not by adding an additional pair of appendages, so it seems reasonable to conclude that the vertebrate developmental system is incapable of doing so.

    In other cases there is direct evidence coming from experimental manipulation of developing embryos, or from mutation experiments where people have tried to artificially (re-)create a missing area of phenotypic space.

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  3. The account given here of how hypotheses are tested seems sensible, even pretty obvious. The point: “… they prefer the term “loopiness,” as in feedback loops between hypotheses and empirical evidence” could equally be phrased as iterations between models and empirical evidence in a Quine-style web.

    There is nothing here, though, that makes evolutionary psychology necessarily a “quasi-science”. Some of the points mentioned do indeed mean that the science of human behaviour is harder, but that alone doesn’t make the whole of evolutionary psychology “quasi-science”. It would be better to simply focus on whether particular claims made in the field are or are not adequately supported by evidence.

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  4. Coel,

    Setting aside your unnecessary comment about just how trivial all of this is, I made a specific, detailed argument, for why evopsych is a quasi-science. The difficulties aren’t just encountered case by case, which is true in any science. They are systemic, and seemingly unavoidable given the specific situation of Homo sapiens.

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  5. Have I understood you correctly? You don’t believe the evolutionary study of behaviour can ever be scientific because it doesn’t leave any fossil evidence? For all animals or just Hominids? If only for hominids then why the distinction. Presumably you would then not consider the study of the origin of life to be scientific either unless some form of fossil evidence was discovered? Is this right?

    Also, how radically different does an environment have to be before any evolutionary explanation becomes impossible? For example, many animals like sharks have been around for millions of years and I’m sure their environment has changed (maybe even radically). Does that make the study of the behaviour of sharks off limits?

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  6. I would prefer to have a better term than loopy.

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  7. No, Bunsen, you have clearly not understood me correctly at all.

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  8. Massimo,

    I made a specific, detailed argument, for why evopsych is a quasi-science. The difficulties aren’t just encountered case by case, which is true in any science. They are systemic, and seemingly unavoidable given the specific situation of Homo sapiens.

    I’ll make two “evo psych” claims:
    1) The sexual attraction that most men tend to feel towards women is an adaptation (= was selected for in our evolutionary past).
    2) The love that mothers tend to feel towards their young children is an adaptation (= was selected for in our evolutionary past).

    Does anyone seriously think that we have insufficient evidence to make those claims, and thus regard them as “quasi-scientific”? Note that all the difficulties you raised apply to those claims (neither sexual attraction nor maternal love fossilize, etc).

    If we accept those two as sufficiently established as to be likely true, then from there we should indeed evaluate evo-psych claims on their individual merits, rather than blanket dismiss them all.

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  9. Coel,

    You really must have a low opinion of me. Those particular claim are obviously true. You know how we can tell? Because those behaviors are pretty much universal among mammals, which means that the phylogenetic contrast group is huge, and that we can actually test directly those claims in a large number of non-human animals, and therefore easily extend to humans. We also have no reason to believe that the human ancestral environment for those traits was any different than today.

    Now try something more challenging: rape as a secondary sexual adaptation. Or why so many women wear high heels. Or why people work 14 hours days in order to afford a vacation somewhere exotic. That is the stuff of evopsych, not the one you propose.

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  10. ‘Most human behaviors of interest to evolutionary psychologists do not leave fossil records (i); we can estimate their heritability (ii) in only what is called the “broad” sense, but the “narrow” one would be better (see here); while it is possible to link human behaviors with fitness in a modern environment (iii), the point is often made that our ancestral environment, both physical and especially social, was radically different from the current one…’

    This appears to be the core of your argument. I am not sure what a quasi-science is (is it like a pseudo-science?), but I assume it at the very least means not-science.

    So it seems to be you are saying that anything fulfills the above criteria is a quasi-science. Clearly modern homo sapience are no the only ones to fulfill that criteria, correct? It’s not an argument I’ve ever heard before and am quite curious about it, hence the desire to make sure I haven’t misunderstood anything.

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  11. Bunsen,

    As I thought I clearly explained in the OP, those criteria are for a sound evolutionary science. But evopsych fails all three (not just the fossil record), so it is questionable whether it has the same status as run of the mill evolutionary biology, which is what mevopsych supporters claim. Quasi-science is my own term, explained in Nonsense on Stilts.

    As for the origin of life, it’s science, but not evolutionary, it’s more to do with biophysics and biochemistry. And I am very skeptical we will ever arrive at an answer there, because of the lack of historical traces. Even if (and it’s a big if) we should be able to synthesize life in vitro in something like what we think happened 4 billion years ago, we will actually never know because there is no way to check the historical record.

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  12. Massimo,

    But evopsych fails all three (not just the fossil record), so it is questionable whether it has the same status as run of the mill evolutionary biology, …

    But different areas of science will inevitably be easier or harder, and hence have a different degree of reliability or “status”.

    For example, “chemistry of benzene” (where you can create it in a lab and prod it) is going to be way easier than, say, “evolutionary split between humans and chimps”. That is not a basis for calling one a “quasi-science”, it’s just an argument for appropriate caution in the more difficult disciplines, adjusting the strength of claims to the available evidence.

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  13. I think I see. For something to be considered sound evolutionary science it must pass 3 criteria:

    (i) There should exist a fossil record
    (ii) We should be able to estimate heritability of the traits in a ‘narrow’ sense (is there supposed to be a link available when you say ‘see here’ showing what narrow means?)
    (iii) The modern environment should not have diverged too far from the ancestral (decided by the relevant scientific community?)

    Also, my copy of Nonsense on Stilts is at a friends. How exactly is the term quasi-science to be understood?

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  14. Perhaps it would be more accurate in Table 1 to describe the logical prerequisite for the optimality approach as the well-supported generalization that adaptation is the only mechanism thus far proposed that holds any promise as the driver for what optimization we seem to have found.

    A graver objection I think is the description of the optimality approach neglects to mention that population sizes may be indicative of the optimality of adaptation. You can say members of a microspecies are optimally adapted with respect to their local environment. But the tiny population of the species and the extreme narrowness of the habitat suggest that maybe you shouldn’t.

    It seems to me the takeaway is, first, in the end valid adaptationist perspectives need all three approaches. Circularity is to be avoided by references to different kinds of evidence, instead of reverting back to the same facts or arguments. Second, I think the paper is saying Popperism must be rejected. It cloaks this by claiming that in practice Popperism is rejected by working biologists, but I really doubt that’s true. What they write in the conclusions of papers, or say in interviews, or pronounce in popularizations I think is still pretty much, there is no scientific history, scientific method is laboratory experiments, laws of nature do not apply to people(‘s minds,) values are not derived from mundane life, and so on.

    The thing is, Popperism is a reactionary philosophy. Not only do most scientists live in a socially privileged stratum, but they mostly work to transmit culture from the past, or as they seek new knowledge, are mostly working for the rich and powerful, often directly. In that situation, Popperism, like all obscurantism, has an appeal that reaches far beyond mere evidence.

    My impression is the OP means EP is almost science when it calls it “quasiscience,” rather not really science. That seems excessively generous to me. In addition to talk about adaptation to an undescribed EEA (possibly undescribable?) rendering all talk about adaptation moot, EP posits unobserved (maybe unobservable) mental modules with the medieval abandon that shocked William of Ockham, Even as they rely on genetic determinism, they don’t study genes. It is not even clear their assumption that everything was adaptive in the la-la-land of the Pleistocene is testable in any fashion, so they are not even good Popperians, for what little that’s worth. Pseudoscience is the word I’d choose.

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  15. Massimo was too kind to ev psych. He didn’t mention the sexism behind the “man the noble hunter gatherer” and related claims, claims which in turn hinge upon an arbitrary definition of when the EEA was, and why.

    ==

    Massimo is otherwise right to separate the origin of life from the evolution of life. Naturalistic abiogenesis is not only a more sticky wicket, it’s a different wicket.

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  16. Massimo,

    Those particular claim are obviously true. You know how we can tell? Because [explanation snipped for brevity]

    This is in line with my suggestion that some evo psych claims are adequately supported by evidence and thus are scientific.

    Now try something more challenging: rape as a secondary sexual adaptation. Or why so many women wear high heels. […]

    This is again in line with my above position. Some evo psych claims are adequately supported by evidence. Others are not. The sensible thing to do is to evaluate each of them on their merits.

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  17. Coel,

    “different areas of science will inevitably be easier or harder, and hence have a different degree of reliability or “status”.”

    It isn’t a question of easier or harder. It’s the fact that for a whole class of traits — those are are universal among human beings but not found in other mammals, and those that are variable within Homo sapiens — there are huge methodological stumbling blocks. That is a different kind of problem from the normal one of “some things are harder than others.”

    “This is in line with my suggestion that some evo psych claims are adequately supported by evidence and thus are scientific.”

    No. The examples you suggested are not really evopsych, they are human behavioral ecology. While it is true that some evopsychs– given the failure of their research program — are now trying to claim the mantle of behavioral ecology, the latter is an older and better established discipline. The difference between the two, in part, is along the lines just sketched above.

    Bunsen,

    Apologies for my somewhat snappy comment earlier. Long day.

    “For something to be considered sound evolutionary science it must pass 3 criteria”

    Not necessarily all three, but a suitable combination of at least two, as detailed in the article I discuss in the post.

    “How exactly is the term quasi-science to be understood?”

    I don’t know about “exactly,” since I don’t believe complex concepts admit of exact definitions. In NoS I put evopsych near the same area of, say, SETI, though not for the same reasons. They are both fields that are clearly not pseudoscientific, and yet fall short of full fledged disciplines like evolutionary biology, not because they deal with hard things (see Coel), but because their methodology and/or theory suffer from systematic issues.

    Steven,

    I’m not sure what it means to say the “Popperism” (not a philsci term) is an obscurantist ideology. It isn’t an ideology. It was a good attempt to make sense of how science makes progress, as well as of getting around Hume’s problem of induction. It doesn’t work, but it is still a point of reference for the rest of us to do better.

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  18. Good article. I think the idea of predictability is there also. So if one hypothesizes that there was a group of short and long necked giraffes, it is a prediction that one should find in the fossil record evidence for this, making the necessary qualifications.

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  19. Massimo, if instead of general behaviour we looked at cognition. Do you think an evolutionary approach can be used to to study cognitive processes? For example, face recognition or counting.

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  20. “I’m not sure what it means to say the “Popperism” (not a philsci term) is an obscurantist ideology. It isn’t an ideology. It was a good attempt to make sense of how science makes progress, as well as of getting around Hume’s problem of induction. It doesn’t work, but it is still a point of reference for the rest of us to do better.”

    I’m not sure what The Open Society and its Enemies or The Poverty of Historicism or co-founding the Mont Pelerin Society are about, if not ideology. It’s true that Popper was persuaded to come to his senses and concede that it might be possible to do experiments in evolutionary biology, therefore Darwinism is scientific after all…then remain discreetly silent about Darwin’s own work, which has no experiments. Personally I can only think that a philosophy of science that so directly leads to such a conclusion isn’t causing more confusion than enlightenment. That seems a reasonable enough definition of obscurantism to me. Perhaps you feel Popper’s repudiation of the possibility of scientific history must mean he’s a great guy, because that knocks Marxism in the head. But historical sciences aren’t just political history, but cosmology, geology, biology And for that matter economics should overlap with geography and ecology, which both have histories. Caging science in laboratories is a huge price to pay for congenial politics.

    And as for taking inspiration from World 3 or Quantum Theory and the Schism in Physics? Inspiration comes where it comes from, but that does that really mean being neutral about the advocacy of, say, absinthe or LSD?

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  21. Popper’s influence in the philsci with the “Logic of Scientific Discovery” and “Conjectures and Refutations” was huge and undeniable. Dismissing him as an obscurantist ideologue is misleading.

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  22. Coel,

    It is a pity you have never thought to apply this principle to economics, about which you have often been dismissive in the past.

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  23. Hi Coel,

    Does anyone seriously think that we have insufficient evidence to make those claims, and thus regard them as “quasi-scientific”?

    They are things that are obvious even to a non scientist not some discovery of evopsych. Are you seriously suggesting that you can justify an entire specialist field devoted to claims that are obvious even to non-scientists?

    Why don’t you bring up a claim that is not obvious to a non-scientist and show that it is better than mere speculation of the kind we can all do?

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  24. I mean when one of your examples of the success of a field has to be the kind of thing I worked out for myself by the age of 11 (and would have probably worked out earlier if I had felt sexual attraction earlier) it does not really commend that field to me.

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  25. Massimo–

    Very useful essay on a kind of non-viscous explanatory program for evolution. Too bad this was made necessary in part by the mid-19th-century-forward acceptance of predictive-based science as the model of successful science, both neglecting underdeveloped science making bad predictions (the existence of Vulcan after Neptune by Leverrier), and undervaluing the retrodictive explanatory power of a theory as signifying truth-worthiness (Einstein’s elimination of the place for Vulcan by GR, but awaiting the eclipse results for real verification of the theory). Retrodiction still only really gets credit insofar as it is based on time-symmetric theory (so now we say, ok, Einstein’s equations really eliminated Vulcan because they also predicted star-shifts and gravity waves), and since evolution isn’t exactly based on primarily predictive grounds, it’s somehow second-class science. Real science is a many-splendored thing, and there is no single conceptual feature of any science that demarcates what science is, and, contra Popper, no single feature of meta-science that demarcates it either.

    BTW I concur on your evaluation of evolutionary psych, despite the fact that I and an anthropology colleague authored an article in the forthcoming Springer Encyclopedia of such. We just confined our attention to the fact that one cannot draw conclusions from observations about cultural relativism to say anything about the nature of the origins or truth of morality.

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  26. Bunsen,

    “Do you think an evolutionary approach can be used to to study cognitive processes?”

    In a very limited way, I’m afraid. On this I’m with Richard Lewontin (Harvard geneticist, BIG influence on my early career), who once said that it may be interesting to know how cognition evolved, but we just don’t have enough information. Tough luck.

    Steven,

    To begin with, The Open Society and Its Enemies is far from an obscurantist piece of ideological propaganda. One may or may not agree with Popper, but still. Second, it has nothing at all to do wi his philosophy of science, it isn’t derived from it, nor is it connected to it.

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  27. Massimo, I suspect you’re right on a fair amount of the cognitive enterprise. And, I know that Lewontin, like Gould, holds that the “tape of life’ is likely to play differently with each replay.

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  28. I love The Open Society and its Enemies. And important work, I would maintain, and right in many ways though obviously, not all.

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  29. Interesting paper. It doesn’t seem to cover the genomic tests of adaptation which are increasingly applied to human (and other species) phenotypes. These have the possibility, at least, of addressing your evolutionary psychology questions.

    Two examples:

    Polimanti and Gelertner [2017] Widespread signatures of positive selection in common risk alleles associated to autism spectrum disorder

    http://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1006618

    “The same mechanisms that contributed to the evolution of human brain are likely to be involved in the pathogenesis of mental illnesses. Numerous evolutionary hypotheses have been proposed to account for the observation that phenotypic traits with deleterious effects on fitness such as psychotic and mood disorders, have not been removed by natural selection. Risk alleles with large effects on predisposition to mental illness should be under negative selection, at least insofar as they interfere with reproductive fitness. This does appear to be true for rare and de novo mutations strongly associated with psychiatric disorders, but most genetic risk for these disorders is attributable to a polygenic predisposition…

    “Significant positive correlations were observed between Autism Spectrum Disorder GWAS results and Hierarchical Boosting scores for incomplete selection (p = 3.53e−4):..ASD has genetic correlations with several advantageous traits: years of schooling (rg = 0.277, p = 2.9e−13), college completion (rg = 0.339, p = 1e−6), childhood intelligence (rg = 0.425, 5e−5), openness to experience (rg = 0.421, p = 2e−3).

    “…we hypothesize that certain Autism Spectrum Disorder risk alleles were under positive selection during human evolution due to their involvement in neurogenesis and cognitive ability.”

    Table S1 of Field et al [Science 1016] Detection of human adaptation during the past 2000 years presents results for a genomic test of polygenic selection:
    Height, r=0.08 (P=9e-74)
    Female hip size, r=0.02 (P=2e-9)
    Years of education, r=0.01 (P=0.02)

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