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I'm reading Michael Pollan's book 'How to Change Your Mind', which is largely about psychedelic mushrooms. In discussing the biology of the mushrooms, he writes:

'Even if psilocybin in mushrooms began as 'an accident of a metabolic pathway', the fact that it wasn't discarded during the course of the species' evolution suggests it must have offered some benefit.'

I'm wondering if this is actually true. In general, I'm wondering if it is true that traits that do not confer advantage will eventually be weeded out.

Being ignorant of the finer points of evolution/natural selection, I can make arguments both ways. On the one hand, it seems that the intense competition would make investing any resources at all in a trait that was not beneficial a totally losing proposition. Therefore no traits that weren't positively adaptive would survive. On the other hand, there seem to be all kinds of traits that are 'neutral' in fitness terms but which survive anyway. E.g. coccyx, male nipples, appendix, whale legs, etc.

I am not talking about information encoded in the genome, which can be present but not expressed. I am talking about phenotypes, i.e. traits that get expressed in interactions with the environment, such as the psilocybin chemicals in these mushrooms. (Though I suppose unexpressed genetic info could never be selected for or against by natural selection by definition.)

So to put a very fine point on my question: Is it possible/likely that psilocybin mushrooms produce a chemical that happens to engender hallucinations, not because doing so is adaptive, but just incidentally? So that this property would be something like the redness of blood, i.e. not adaptive in itself but just a matter of happenstance?

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Good question. And good analysis. I have little to add! I'll simply provide my own list of thoughts to complement your ideas, which are not mutually exclusive.

The fact that it wasn't discarded during the course of the species' evolution suggests it must have offered some benefit.

This statement is speculative. The key word here is suggests. i can think of several speculative scenarios, of course the list is by no means exhaustive:

  • Traits that are not adaptive can still exist in the organism as vestigial traits. This can be because the trait was recently useful but no more, over evolutionary time scales, and not enough time has passed for the trait to be lost.
  • The trait may also be floating, i.e. has not been selected against, and acts as a neutral trait. It therefore remains as a phenotype. Traits are theoretically unlikely to float for very long periods of time, as I will describe later.
  • Some traits can very indirectly affect other traits. In practice it is often difficult to completely describe or understand which traits are a result, or cause, of other traits.
  • Many traits can also be byproducts of other useful traits. With nipples it might have something to do with early exposure to hormones; developing a way to bypass male nipple formation could be difficult and costly. With psylocibin, it may be a side-effect of a particularly useful biochemistry to the fungus, perhaps metabolic, that is completely unrelated to its neuroactivity in humans. It may be that a biochemical pathway might form psychoactive intermediates or products that are difficult to remove or metabolize, and find themselves in the mushroom co-incidentally.
  • The trait may simply be very useful, but we don't understand why it is useful. Humans often overlook this possibility; for instance, I assume you have not considered that psylocibin may have unknown effects on non-human or even non-vertebrate life.
  • I am not an expert but filamentous fungi sometimes/often have very complicated sexual reproductive strategies. Psylocibin may be maintained through sexual selection, rather than natural selection. This is probably far fetched, but hey- we're speculating about our ignorance.
  • Lastly, but very importantly, all organisms face pressure to survive and replicate. It is expensive to maintain useless features and traits, or to produce excesses, or to overdevelop or harbor chemistry that is not doing anything. Natural selection is ever-active in limiting in which traits are maintained within a population. This I think is the most convincing argument; the principle of economy. This argument fares well in all discussions on biology; life is difficult, and the costs of survival are very important to consider, always. It is expensive to store or maintain constituent chemicals, even if they are not toxic, nor if they have no use for the survival of fungi. It is more economical, and less costly, to lose such traits; selection will favor fungi that save or spend this energy elsewhere. This is a very important point, and I think it is the most salient to understand the quote you provide.

I think it would also be a good idea to study the number of times psylocibin arose. If it occurred ('was invented') multiple times independently, it must have had some functionality for the organism, like wings, or vision. If it occurred only once, one can ask whether the majority of descendant strains has lost it, or whether they maintain the trait. That could also shed some light on whether it is maintained through positive selection. Lastly, psylocibin may be a chemical that allows to explore a very specialist niche of the ecosystem. If few descendant strains contain it, that can mean it is still selected for, though only by fungi that rely on it as a strategy. This would also mean that psilocybin-less fungi would have found no need to maintain it, and may point to the occurrence of negative selection. Hope that makes sense.

Mandatory reading for you on relaxed selection.

tl;dr yes, psylocibin may be maintained by happenstance, though likelier via positive selection, at least in specialist fungi

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    $\begingroup$ Also, a trait may be adaptive in some circumstances, but maladaptive in others. For instance, the sickle cell anemia gene, which protects against malaria (if there is just one copy) but causes serious health problems with two copies, and/or if you live where malaria is not present: sciencedaily.com/releases/2011/04/110428123931.htm $\endgroup$ – jamesqf Jul 18 at 18:02
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S Pr lists a number of reasons that might allow non-adaptive traits to spread. One other that's probably important in some populations is "allelic surfing".

If you imagine a smallish population that suddenly expands (say, starlings in the Americas, or humans in the past few thousand years), the original genes are going to expand no matter what - even useless, or mildly harmful, genes will be carried along on the overall success of the rest of the organism. The most obvious example of this is the founder effect, where populations can carry along irrelevant or harmful effects simply because there were very few founders, and some happened to have red hair or Tay-Sachs Disease; but more subtle effects can be seen whenever populations expand.

Several studies have found strikingly different allele frequencies between continents. This has been mainly interpreted as being due to local adaptation. However, demographic factors can generate similar patterns. Namely, allelic surfing during a population range expansion may increase the frequency of alleles in newly colonised areas. ... We therefore conclude that most of the observed large allele frequency differences between continents result from demography rather than from positive selection.

--Large Allele Frequency Differences between Human Continental Groups are more Likely to have Occurred by Drift During range Expansions than by Selection

... remember that it isn't actually the gene that has the advantage, it is the person who has that gene. Usually the two are linked but not always. ... The difference is that the genes weren't the advantage, the situation was. The frontier people's genes were just in the right place at the right time and so were spread more widely.

--Gene Surfing: The Surprising Genetic Advantage of Being on the Frontier

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