These drugs are just changing the balances of existing pathways in our brains. They aren't creating new pathways. Either they are causing a substance that your body naturally limits to exist in higher quantities or lower quantities, keeping a messenger molecule from being removed as fast as it would be normally, or removed faster than normal.
So I agree with the parent, it is likely we can choose the tradeoffs, maybe needing to avoid predators and scavenge for food is not our priority anymore and we can turn off some of that so we can think more deeply. But chemically I doubt we can improve ourselves without any drawbacks.
But yes, technology in general, physical things, can have a more pure benefit, and we are already reaping the rewards of those benefits. A new macbook pro is likely to make me more productive while not interfering with my sleep :)
Gwern outlines three general ways to work around the Algernon rule:
1. We can live under different conditions than evolution prepared us for
2. We can optimize for different goals than evolution rewarded
3. We can make major/multifactor changes unavailable to an local-maximization algorithm.
Condition two is easiest: caffeine is a sensible response to electric lighting, while staying awake long after dark was largely unhelpful in our evolutionary past.
Condition one is sometimes rewarding: piracetam shows efficacy with choline supplements, because we can massively overload a relatively scarce chemical. Other kludges may exist, like boosting immune response by simulating a summer day/night cycle to signal "safe conditions, energy is cheap now".
Condition three is incredibly hard wrt to the brain. It's obvious for the body - eye surgery can improve on 20/20 vision - but I don't know of any drastic better-than-well interventions for the mind.
You could apply the same logic to Aspirin or any medicine - if reducing swelling was beneficial, why doesn't our body do it for us?
That seems like a misunderstanding of evolution. It's not a master plan driving toward perfection. Our biology is a bag of traits, some of which were useful and some of which just haven't been selected out yet.
Perhaps if you are a runner and you take these seemingly benign medicines to reduce pain and swelling, you end up causing more permanent damage by continuing to run when you should not (I have experienced this).
I think a lot of medicines work by turning off or on processes that are important but inconvenient at the time. Painkillers are probably the best example. We shouldn't take them when we are healthy, it would be dangerous. Other medicines, such as antibiotics, work by killing pathogens directly and don't affect our bodies like the drugs in this discussion.
It's I suppose possible to hit a simple optimization evolution hasn't found yet, but that's rarer than people seem to think. The major examples we have are either things which evolution lacks the tools for (e.g. mechanical prosthetics) or major biological leaps (e.g. your antibiotic example).
The things that look quick and easy like "eat some willow bark extract" have tradeoffs, even when they aren't obvious. Taking 'painkillers' to the extreme - morphine - makes it especially obvious. It's generally a terrible idea unless you've recognized that there's a problem and gotten someone else to take care of keeping you healthy while you're out of commission.
There is one version of this idea that I like though, which is that I doubt that we're built for 8+ hours a day of intense abstract reasoning, which seems to be what the modern information economy demands of those aspiring to a middle class or better existence. The vast bulk of humanity did not earn their daily bread this way for most of human history, so I don't think our brains are adapted for "abstract reasoning above all else."
As an aside, drug use was extremely common among indigenous peoples all across the world. I don't even think this naturalism fallacy supports these particular claims.
It's very useful to recognize when we aren't 'made' for something, because it implies we can get benefits from either avoiding it or supplementing our performance at the task. When we are "made for" a task, like walking for long periods or throwing objects with good aim, it's tough to improve on human baseline. (At least, not without serious side effects. There's a reason drugs to boost strength and physical endurance tend to be risky.)
But that distinction has to be kept separate from a values judgement. As I mentioned in another comment, "reading a good book" is something I'm not evolved to do. That might mean I should be prepared for challenges with the task (e.g. back pain if I sit for too long), but it's unrelated to whether I want to keep doing it.
The 'ancestral environment' stuff is likely to be easy or optimized-for, but that's not the same as being a better way to live.
There shouldn't be any easy way to improve on what evolution tried to do, because evolution would have done it. But there can certainly be ways to optimize for things evolution didn't try to do, like preparing us to do symbolic logic for 40 hours a week or stay up well past dark. And there can be ways to optimize for goals evolution didn't/couldn't reward, like "never having kids and staying healthy until age 90".
I do think there's risk in blurring the moral point with the practical one, though. I'm not particularly evolved for reading books, but it's something I enjoy and I want 'hacks' to do it better - whether that's reading glasses or a cup of coffee. I don't like commuting while tired or being stationary for hours on end, and if I had free choice I'd stop doing those things instead of hacking myself to be better at them.
But in "enhancement" terms, they both count as "doing a thing I wasn't made to do" regardless of whether I want to keep doing them.
It does not follow that evolution would maximize intelligence or performance.
Human intelligence exists as a by-product of many cumulative adaptions for survival.
That's the thing, that's not how it works
The brain didn't evolve to be affected by substances unknown to it, it's plants that evolved substances that have CNS effects. (Though the body did evolve to depend on a lot of external substances - be that calorie and protein sources or vitamins)
Nicotine is literally a pesticide (and yes, people do use it as such in some occasions). Not sure how other substances evolved though (I think caffeine made the coffee seeds travel further)
There's some reason to believe this is literally true - and true in the same sense as the economic rule! In this context, it's been nicknamed the Algernon argument. Gwern (of course) has the canonical writeup.[1]
The short version is: "if some chemical change could make us smarter, why wouldn't it already been in place?" Or, framed differently, "why would the brain evolve to benefit from a chemical it doesn't normally have?" This argument doesn't say cognitive performance enhancement is impossible, only that there has to be some tradeoff for it or we would have evolved it already. If we're going to get rewarding "brain boosts", we need to find tradeoffs that are more appealing than they were historically.
One simple possibility is this one: we can find chemical supplements that let us rearrange when we're performing well, without net gain. Caffeine is an obvious example: it doesn't actually diminish the value of sleep, but postpones the feeling and helps us manipulate our schedules. Amphetamines might be a more extreme case of the same, 'borrowing' energy more generally and paying for it later.
The other dodges are less relevant here, but a fascinating read if you check the article.
[2] https://www.gwern.net/Drug-heuristics