Ep 155: The Selecting Organism (with Pim Edelaar)

How can organismal choices drive adaptive evolution? Can plasticity act as a kind of selection?

In this episode, we talk with Pim Edelaar, professor in the Department of Molecular Biology and Biochemical Engineering at the University Pablo de Olavide, Spain. He’s also the author of the new book The Selective Organism: An Expanded Theory of Adaptive Evolution. In the book, Pim proposes that in addition to natural selection there might be a “second driver” of adaptive evolution. We discuss the book with Pim, explore how non-genetic inheritance and plasticity underpin the theory, and talk about what implications this expanded perspective has for research. If after listening to the episode you’re interested in reading The Selective Organism, the digital version is free to download.

Cover art by Brianna Longo

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Marty Martin 0:04
Howdy, Cam. I want to start today with some trivia. What's probably the most quoted line about evolution in movie history?

Cameron Ghalambor 0:11
That's a pretty easy one. "Life finds a way".

Marty Martin 0:15
Ooh, damn, that's impressive. You knew right away. But to be precise, the line is "Life uh finds a way," classic awkward Jeff Goldblum style, with Goldblum playing the chaos theorist Dr. Ian Malcolm in Jurassic Park.

Cameron Ghalambor 0:28
Yes, and it's a line evolutionary biologists have been saying for years. And a quick refresher for those few of you out there who may have not seen the movie or who have forgotten about it. In Jurassic Park, the park's geneticists thought they had found a way to keep dinosaurs from breeding. They only cloned females, so no males, no eggs, no problems.

Marty Martin 0:48
Uh yeah, we all know how that plan worked out. So Malcolm's quote is basically him making fun of the park's scientists. Malcolm saying that if natural selection has the right stuff to work with, evolution or life will find a way.

Cameron Ghalambor 1:01
Yeah, and when most of us hear this, we might think "finding a way" means, given some genetic variation for a trait, selection acting on that trait, and enough time, almost anything's possible. Clearly, making baby dinosaurs is a reproductive advantage over making no dinosaurs. So as soon as one female Dilaphosaurus could lay eggs. Her offspring would dominate the population.

Marty Martin 1:24
Darwin via Dilophosaurus.

Cameron Ghalambor 1:26
Yep, Darwin via Dilaphosaurus.

Marty Martin 1:28
Except that's not really what happened. Remember? Later in the movie, Sam Neill's character, Alan Grant, he finds hatched eggs out in the park, and he eventually works out how that happened. But it wasn't the female dinos in the park evolving the ability to breed without males. Some female dinos just changed their sex.

Cameron Ghalambor 1:48
That's right. The park's engineers spliced frog DNA into dinosaur DNA, not realizing that some frogs can change sex when there's no males around.

Marty Martin 1:59
Well, can they? I remember hearing that part of the movie and immediately thinking, "Wait a minute, there aren't any frogs that can change sex.

Cameron Ghalambor 2:06
Mostly true. The frog story, I think, is a bit shaky, but plenty of fish and other animals are plastic in their ability to do this. Pull the big male out of a group of blue-headed wrasses, for instance, and the largest female will turn into a male within days.

Marty Martin 2:21
Okay, fine. Frogs, fish, close enough, I guess. But here's my point: despite how memorable that quote is, Malcolm got it wrong. I think he shouldn't have said that life finds a way. He should have said that life chooses a way.

Cameron Ghalambor 2:35
Ah, choose a way. Wait, that's starting to sound a little Lamarckian to me. The dinosaurs didn't have to decide whether or not to become male; they just did it. Perhaps in response to some environmental cue.

Marty Martin 2:47
Fine, they didn't think through the pluses and the minuses per se, like we do when we decide what we want for dinner. But they did evaluate their options given the cues they experienced, then stayed female or switched to male. That's what the wrasses do. They watch the other fish, and when the big male disappears and they're the largest female left, she switches. That might not be a choice in the traditional sense, but it's definitely not natural selection acting on existing variation, which is what "finds" sounds like.

Cameron Ghalambor 3:15
Okay, I see where you're going. Since Darwin, adaptive evolution has needed three ingredients: variation, inheritance, and selection. Plasticity, meaning organisms changing their behavior, physiology, or other phenotypes, has been often filed under non-heritable variation. It's the menu. Natural selection, by contrast, decides what gets ordered, and plasticity generates variation on the menu. But I think where you're suggesting is that plasticity in dinosaur sex could be viewed as a form of selection rather than variation. If females are choosing their sex, they're doing the sorting that natural selection would otherwise have to do.

Marty Martin 3:54
Well, yeah, but that's not my idea. I do like it. It's one of the main ideas of our guest today, who argues that organisms choosing among options is a second driver of adaptive evolution alongside natural selection. And these aren't just ideas. He has data.

Cameron Ghalambor 4:11
Okay, fine, but here's where I immediately want to push back. First, I'm not sure calling plasticity selection is accurate or does anything. To me, it just describes how well an individual is tracking its local optimum, but we can come back to that later. Second, if we look at the Jurassic Park example, sex switching evolved, let's say, in frogs or fish, but for under completely different circumstances. So even if I go with your point that life is choosing, something has to build the mechanisms that allow for the detection of the environmental cues and thus the choosing. So, isn't choice a product of selection also?

Marty Martin 4:50
Okay, fair, all great questions, but I'm going to let our guest today, Pim Edelaar, answer them. Pim is a professor in the Department of Molecular Biology and Biochemical. Engineering at the Universidad Pablo de Olavide in Sevilla, Spain. His lab studies matching habitat choice in grasshoppers, zebra finches, tree sparrows, and fruit flies using field experiments, lab work, and even simulation models.

Cameron Ghalambor 5:14
And his new book, "The Selective Organism: An Expanded Theory of Adaptive Evolution" just came out from Oxford University Press. On the show today we talk about that book and Pim's exceptional approach to making complex and important points about adaptive evolution.

Marty Martin 5:30
Yeah, unlike other efforts to extend the modern synthesis in evolutionary biology, the merger of genetic concepts of inheritance with Darwin's tenets of evolution by natural selection, Pim makes a systematic and formal argument. So instead of just asserting that theory needs to change, he carefully explains the problem and possible ways forward.

Cameron Ghalambor 5:49
Please don't hear what Marty is saying to mean that the book is full of complex math. It's very much not. It's a carefully structured set of ideas built around the Price equation, but it's also incredibly approachable and a really fun read.

Marty Martin 6:02
So let's hear from Pim.

Cameron Ghalambor 6:04
Let's hear from Pim.

Marty Martin 6:05
I'm Marty Martin,

Cameron Ghalambor 6:06
And I'm Cameron Ghalambor.

Marty Martin 6:07
And this is Big Biology.

Marty Martin 6:20
Pim Edelaar, welcome to Big Biology.

Pim Edelaar 6:21
Thank you for having me.

Marty Martin 6:23
So every good theory starts with something that doesn't really fit a mold, and for you, it was grasshoppers ending up on the right colored dirt. Tell us about the research, that sort of research, and why solving that problem about habitat choice forced you to go after evolutionary theory itself instead of just writing a nice natural history paper and then moving on. Was it that experience that led to this new book, the Selective Organism and Expanded Theory of Adaptive Evolution?

Pim Edelaar 6:46
Yes, to a large extent it was. But there's actually a history to that grasshopper work. So I did a postdoc with Craig Bateman. So I could have I could have used that as an example in the book, but that's his works, and I prefer to use my own work: species of bird that lives across the Northern Hemisphere that specializes on seeds of conifers. And it turns out that instead of there being, let's say, one crossbill in North America, there's actually several types, perhaps even several species. One of them is actually officially recently described as a different species, because they're specializing on different resources, no, on different types of conifers. And the weird thing is is that we didn't really understand well how that was possible because they have overlapping geographical distributions, and there isn't really a good explanation, theoretical explanation of how that would be possible because normally interbreeding would prevent them from splitting up, and then one hypothesis was is that they're choosing their resources and their their habitats, where to breed, depending on their characteristics, on their on their bill size in this case. So that was a hypothesis that we thought could explain speciation, and if anything is evolution is speciation, right? So, so we see their speciation. We don't have a good theory to really explain that. We have a hypothesis, a working hypothesis, but it's impossible to not totally impossible, but it's hard to study in crossbills.

Pim Edelaar 8:17
So then, being back in Spain, I came across a paper on grasshoppers, which suggested that they also choose their habitat based on their characteristics, their color in this case, and they choose a substrate to perch on in order to maintain crypsis, which is good for their survival. And that kind of separates individuals also in space into locally adapted populations, and local adaptation is sort of an evolutionary process, and it also suggested that there could be, even reproductive isolation occurring because of that. So, I decided to take that system and do the experimental test that we couldn't do on the crossbills. And fortunately, that worked out. Now the hypothesis was confirmed, so that was that was super nice. That kind of gave me some insight in what was going on, but it suggested that you could have speciation happening because of organisms choosing their environment, and that is not something that we consider with standard evolutionary theory, you know. Normally we say organisms are just moving, and then the environment selects on the individuals, and that creates divergence and maybe reproductive isolation. So there was this other kind of mechanism that suggested it could cause local adaptation and even speciation, but it wasn't really part of standard theory, and that was the thing that bothered me for well, for quite a while. Maybe too long. Maybe I could have figured it out before. And I discussed it in the book why it was so hard because I really had to look at several aspects of the process. But I realized that with a different perspective, it. does make sense. And this different perspective is really what I want to convey in the book layout. And then I realized, and that was sort of a revelation that came with time, is that this different perspective doesn't just explain this one funny type of habitat choice and the consequence of that, but you can actually apply it to other biological phenomena too. And I thought, oh that is interesting for other people too, right? So then let's write a book about that because I'm not talking to just a few people that are interested in grasshoppers or, or habitat choice. I'm talking to almost all biologists, potentially.

Cameron Ghalambor 10:37
Yeah. So we want to jump into the ideas of the book, but you know, I've read many of your papers over the years, and you know, I'm a big fan of your research. But the first thing that I noticed as I started reading the book was your writing style was a little bit different than you know your typical papers. There seemed to be a very methodical sort of...what was going on in your head as you were writing you you really described the thought process behind the ideas. And I was curious, was that something that you decided to do consciously or did it sort of come about as part of the process of getting the ideas out on paper and and and writing the book?

Pim Edelaar 11:30
I think there's both, or even several. But one of the things that I really thought about hard is maybe even the structure of the book, and I was thinking what I'm trying to convey might be uncomfortable to people, might be a big change of their usual way of thinking, and it's really hard to change people's perspectives. So how do you achieve that? And as I also write in the epilogue, you could argue that that, sort of, evolutionary theory is at an adaptive peak, on or near an adaptive peak, no? It's clearly doing very well. Now it has lots of application in real life. It explains a lot. So in that sense, you know, we're fine. What I suggested or had in mind, and other people too, is that there might be other perspectives that you could see as other adaptive peaks, and maybe those adaptive peaks might even be higher, no, might even be better. But how do you get there? To go from one adaptive peak to another, you have to cross an adaptive valley, and that normally doesn't happen, no. There's resistance into crossing these valleys. So what I set out to do, and hopefully succeeded, is to sort of take the reader by the hand and make small steps, explain everything in a very didactical way, maybe overly simplistic for for the taste of some people, but at least really go through the thought process, go through the the argument, step by step, and at every step along the way, person can say, you know, do I do agree with this? Do I still understand this? Yes, go ahead. And then at the end, after this path of of small steps, we arrive in a different position at the end of the book, where I kind of pull everything together, where this new perspective is then developed, and then hopefully the reader sort of looks back and says, "Oh wow, we did this small, or we did this yeah this walk step by step. It was, you know, comfortable. I agree with every step, but now when I look back, oof, look how much I've traveled, and the view is very different from this adaptive peak. No, the perspective that I dig because I, you know, I agree with all the small steps that we take is very different. But it, but it's where we arrived, and I came along willingly, and it was an easy walk in the end. That's sort of the style I wanted to use, and then the way to do that is yeah is a much more friendly conversational style. I personally don't really like dry scientific papers, no. If someone puts in an anecdote or even a joke, I really appreciate that. So I took I took the liberty of you know this is a book that I wrote that I didn't have to deal with with reviewers basically telling me it had to be this way or co-authors that had different opinions, so I kind of chose my own style in a friendly way and just to keep everyone on board and perhaps even a little bit entertained. So I have anecdotes, I have you know, personal views and whatnot.

Marty Martin 14:39
It came off that way. I mean, it was genuinely a pleasure to read, and as you know sort of describing your thought processes, yeah, it almost read like listening to a podcast, as if you were giving a podcast where you're systematically talking someone through complicated ideas. I mean, your treatment of the Price equation was exceptional and but clear. We'll come back to some of that, but but. I thought that not just the sort of familiarity in the language and the sort of way that you were trying to coach someone through the ideas, but the systematic way that you did it too, it made those ideas... I mean, I'm sort of a fan of many of them. I didn't need to be convinced from for a lot of what you're saying, but I could see that. Like, take for example, you write about this at the end, the extended evolutionary synthesis. Many of the ideas sort of put forward by the proponents of that framework, which we talked a ton about on the show, you know, there's been a lot of pushback, and a lot of people have said it's not necessarily that I disagree. It's the kind of way that that's done. It's like you know, these ideas are shaking the foundations of evolution. Well, I mean, is that necessary? Is that true? And you, you sort of just didn't even get into that kind of a space. You just walked people through the sort of step by step idea, and I really appreciated that. So I got to ask, was that treatment at all derived from what happened with this extended evolutionary synthesis, and that for some people it was so off putting, even though some of the ideas were solid?

Pim Edelaar 15:30
Yeah. So some of the things that I've read and also people mentioned is that, and I agree with a lot of the viewpoints and things that people in the extended evolutionary senses have said. I agree to a large extent, but the way it is presented is not always convincing. It's quite verbal. It is to some extent disconnected. So it's not clear that this is a complete treatment. Some people have spoken about it as a laundry list of desires, no, of things that should be integrated into evolutionary theory, but without really a solid explanation of how or why.

Pim Edelaar 16:45
And so, in my treatise, what I've done is sort of go to basic concepts and sort of use a logic derivation to say, "Okay, how can we think about this concept, and is there maybe an expanded way of thinking about these concepts? And if we do that, then where does the logic take us?" So I've sort of done a systematic review from the basis to see where it leads us. That's still kind of a verbal exploration, but at least it's systematic. And I think it's something that could be repeated by people, no. There's a method to it to some extent. Then, additionally, but more towards the end of the book, I've used some mathematical backing up of my conclusions, because that's another way that some people, no, respond to arguments. For some people, an anecdote or the real biology or a verbal argument is totally convincing. I don't know if you know this joke about theoretical biologists. There was one in the audience, and he responded at the end of a talk. He says, "It's great that you show that this works in practice, but does it work in theory? And what I wanted to also include in the book is is sort of an undercurrent of mathematical support, saying, "Okay, these are the verbal arguments, but this is how it plays out mathematically using the Price equation," because there is also a group of people that need that kind of support to see what's going on and to and to evaluate the argument. So, in that sense, I'm using different types of argumentation for different types of people.

Cameron Ghalambor 18:23
Yeah. So, so Pim, you know, when you were writing, did you? I mean, obviously, your the book is going to be of interest to practicing evolutionary biologists, ecologists. But were you sort of, did you have a particular audience in mind as you were writing was you know were you thinking kind of more general or did you have a particular particular audience in mind as you were writing?

Pim Edelaar 18:51
This was a struggle with the reviewers of the proposal, so I sent the proposal to the publisher, Oxford University Press, and I got I think eight reviews, and one of them is now what's the intended audience. And I had the intention to sort of serve everyone from hardcore evolutionary biologists up to interested non-scientists, and everybody of the reviews push back on that. They say that just doesn't work. Now you can't popularize science before you've done the science, so your audience should be much more the in-crowd, the evolutionary biologists, the ecologists, etc. I've taken that at heart, that advice, but I think I've only managed to do so partially, because I still hope that at least interested people that know something with biologists, or maybe I don't know, an economist, or a medical doctor, you know, a researcher, perhaps, could still follow the argument. They could still take something with it. And so in that sense, that the book is maybe a bit of a hybrid between you know talking to our own people, but with the doors open to a broader audience. I think it's definitely suitable also for graduate students because of this conversational style. I think it could be a really good piece of material for a literature, you know, for book discussion also because it's sort of an extended essay in a way. It's sort of building up the story. So yeah, I think you picked up on that. It's like it's not totally clear that it's really a target audience because it is both for the mathematicians, it is for practicing evolution biologists, it is for people with an interest in evolution biology, and especially because I go back to really basic concepts, even if people don't know anything about evolution and biology, they may actually be able to read the book, start from the beginning, and and follow much of the argument.

Marty Martin 20:55
Yeah, I mean, again, I thought it was fantastic. It feels so much like how we try to put together this podcast, where you know we hope that lots of different kinds of minds listen to it, and yet we know that the majority of our listeners are going to be professional biologists, given the nature of the topics and the material and things. So, yeah, it really resonated. So, all right, let's turn to the book. You open by asking, "Why fix something that isn't broken? So, let's first talk about what you see as being broken. You know, assuming that you do enough at least to write a book about it, and broken with the current views on adaptive evolution. What are you plainly? What are you trying to fix?

Pim Edelaar 21:33
Actually, I don't think anything is broken. No, evolution biology is wildly successful, really explains a lot and has lots of very useful applications. Think of I don't know understanding the evolution of resistance to antibiotics or how it's applied in animal breeding and agriculture, no. Clearly it has massive success there. So in that sense, it totally works. What I argue in the book, and other people have done that too, is that the framework that we currently use explains a lot, but maybe not everything. Maybe not, or or in this specific case, not sort of the adaptive divergence of these crossbills and these grasshoppers. We need something else. So, and I've used that phrase also in the book. If all you have is a hammer now as a tool, then you see all problems as a nail, and you will treat them as a nail. And that's fine because often problems are nails or could be treated as a nail, but some problems are just not no. And if you say yeah, well, then we just don't see those other problems, therefore, and that's not a problem, then you know there isn't nothing wrong.

Pim Edelaar 22:46
But I'm arguing, and or at least I think that there are some topics that we just cannot address with the standard theory. And one of them is, for example, cultural evolution, no. That's a field of research that I think is is has a long history as you know it's respectable. But if evolution is defined, as is done by many people, as a change in allele frequencies, then cultural evolution is a misnomer, no. By definition, it's an oxymoron. However, we know that it exists, and we know that in some cases it has strong evolutionary effects. It can even cause, again, speciation, so clearly it is relevant, but it doesn't really fit nicely in sort of the standard theory. So, is the thought then maybe we need to expand this standard theory, add something to it, such that these other phenomena like cultural evolution can be included, and this habitat choice can be included? So that's my sort of identification of what's the problem is that we can do a lot with standard theory, but not everything. So let's see if there is something, another perspective, that is able to explain more, no, a more holistic, more integrative perspective, and that's the exercise in the book.

Cameron Ghalambor 24:12
Yeah. So so let's let's jump into kind of your what what you're offering and what you're proposing. And so, you know, I think one thing that I really liked about the book was how you started off essentially taking the standard views on variation, inheritance, and selection, and then rather than I guess extending, I think using your words expanding our understanding of these terms. So, and this maybe, you know. a challenge, but can you summarize how you've expanded the standard theory and what are the main, you know, bullet points or take homes that that you think are the main main things that that the reader should take away from the book? And then we can discuss more in detail, but just kind of give your your broad overview.

Pim Edelaar 25:11
Sure, sure, sure, sure. Yeah, yeah, yeah. So I use those three concepts: variation, selection, and inheritance, which are almost always used in all basic textbooks as sort of the elements of adaptive evolution, and I go through them one by one, and I say, "Okay, is our biological interpretation of these concepts as we typically do them? Is is that is that complete, or is there maybe something else?"

Pim Edelaar 25:41
And for variation, I argue that we should see the environment as something that is even more under the control of organisms than we typically already do. Again, we can go into detail, maybe later, but I kind of add our interpretation of what is called the extended phenotype. You know, that's sort of the traits that are expressed outside the organism, so I suggest that there is an expansion that has been overlooked, and that is that's useful, and thereby it would be a complete interpretation. For the inheritance part, typically we think about genetic inheritance, but when you think about cultural evolution, for example, and also other phenomena like epigenetic inheritance, we know that inheritance or transmission from parents to offspring can also be non-genetic, no, there can be hormones transmitted and nutrients and and entire habitats and whatnot. So again, also there I say, okay, what if we expand the concept of inheritance to also include non-genetic inheritance.

Pim Edelaar 26:41
And then for selection, and I'm sure we'll talk about that a little bit more because I think that's where the greatest novelty perhaps is. I suggest there's a second type of selection that we haven't recognized, and again, I use the Price equation to sort of deduce that that is not only a logical or or necessary, better said, way of looking at selection, but also then probably the complete perspective of selection. Having these sort of expanded interpretations of these concepts, I then pull those together and I say, okay, how are those interacting to create and change the evolutionary process? And I use a specific technique called causal modeling, which manages, I think, in a nice way both visually appealing but also mathematically tractable. What are the consequences of these expansions for the evolutionary process? And what comes out is that many of the consequences of these expansions are actually known now. People already have worked on that, given names for that, terms for that, which is a nice confirmation that these expansions kind of you know make sense and are already supported by yeah by ongoing research. But there's another thing that drops out, which I call a second driver of adaptive evolution, which is sort of the logical consequence of these logical expansions of these concepts, which then explains a lot of this additional biology that otherwise doesn't really fit nicely in the standard theory. So, I would say that is the main message of the book that by using the concepts in a broader sense, more complete sense, a better way, I might even argue, we gain the ability to explain biological phenomena that otherwise are not easy to understand. So yeah, that's sort of the main message of the book.

Marty Martin 28:39
That's impressive. I mean, we worried Cam and I when we were coming up with questions that we could ask you such a broad one and get a concise answer like you just gave. So I really really appreciate that. But we let's go ahead and dig into some of the pieces. So these second drivers or this second driver of adaptive evolution, two of the critical components you've sort of alluded to- let's start with non-genetic inheritance because I think, and maybe this is just my own bias. I think that's the simpler one because it's been around as an idea for a little bit longer, because I think the skepticism there has largely been how long these things endure relative to genes. So, I mean, there are systems that have spoken to that, but what's the sort of take home that you want to leave the listener with?

Pim Edelaar 29:30
That's a that's a broad question, actually, because because 10,

Marty Martin 29:33
Pim, you're the one that wrote this expansive book. This is your fault.

Pim Edelaar 29:37
No, no, no, no. Let me just throw out a couple. So, one of them is non-genetic inheritance. For some people, that is just evolutionarily irrelevant because they define evolution as genetic change. So anything that's non-genetic is automatically, sort of, not included in that theory, and that's respectable. I'm not saying that that's wrong, but it is a limited view of what's happening in real life, because what is happening in real life that in some cases organisms do transmit for many generations, and that can be dozens of generations, and in some cases in C. elegans, for example, no, the famous nematode, even infinite. Maybe that's the nicest example to discuss, no. These nematodes when they're exposed to stress in the environment that could be high temperature or specific types of food or or viruses that attack them, they produce RNAs to with that, which help the individual to cope with stress, no, to to maintain homeostasis or or whatnot. Phenotypic plasticity. We know that exists, they have that. But wouldn't it be cool if a parent could pass on these adaptations that it acquired during life to its offspring, such that when the offspring is born, they are already adapted to this environment? Lo and behold, that's exactly what they do. They are able to transmit the RNA that they produce, the specific RNAs that they produce to deal with these stressors, into the eggs that they produce, and the offspring are already born such that their gene regulation is how it's supposed to be to deal with this environment. And there's a whole biochemical machinery that enables these RNAs to be produced, to be transmitted to the eggs, to be upregulated in the offspring, such that it will be passed on to grand offspring and grand grand offspring, etc. That's been studied and understood. So clearly, there's a whole machinery in this organism that has evolved to enable this non-genetic inheritance and thereby promote the adaptation of, you know, many generations to come.

Pim Edelaar 31:51
It's true that sometimes that is unstable, so it's not the same as a genetic variant that in principle is continues infinite until it mutates, and you could say okay then it died, but people have also argued that that's not a problem of non-genetic inheritance. That's actually the advantage of non-genetic inheritance. That also means that if you want to get rid of a certain trait, that's also possible, no. So it is a system that sort of sits nicely between very fast individual level developmental adaptation, no, within a generation versus relatively slow genetic adaptation across generations and and this non-genetic inheritance can kind of deal with environmental changes that are in-between, that are maybe only lasting for a couple of generations, so you need to be relatively quick to deal with that because genetic adaptation would be too slow. But you don't. You also can't deal with it, or you may not want to just deal with it with developmental plasticity, because then every generation has to start from scratch. If you already prime your offspring with, you know, the traits that they need, then that's probably the adaptive thing to do. So in that sense, this non-genetic inheritance sort of sits in between these other types of adaptation that we already taken on board very much in standard theory, and so it's an addition of the ways that organisms can adapt.

Cameron Ghalambor 33:20
Yeah, and well, and this will this might be a this is going to be a theme of some of the questions that I have for you, but you know I totally agree with that. But at the same time, you know, there's also many examples where the offspring experience environments that are different from those of the parent, and so you know, we can think of this type of non-genetic inheritance as always being beneficial or adaptive. But in some cases, you know, the parents may not be doing their offspring a favor if they bias them towards, you know, being adapted to a particular set of conditions that the offspring do not experience. So, how do you see that as kind of falling into this into the selective organism? You know that sometimes there may be mistakes.

Pim Edelaar 34:14
Yes, and and as you say, sometimes, no, environments cannot be predicted or are not, yeah cannot be predicted by the parents, and then to sort of bias or transmit traits to your offspring may not be the right thing to do. So there's actually a nice study in the same C. elegans where they have manipulated the reliability of the environment or or the predictability, I should say, of the environment. So whether or not the environment of the offspring resembles the parental environment, and what they saw is that when the environments of the offspring were actually opposite to the environment of the parents, is that this capacity to prime their offspring was actually selected against. So the nematodes actually evolved. Or de-evolved the ability to transmit traits non-genetically. So that's actually a really nice experimental study showing that non-genetic inheritance is sort of an evolved capacity to deal with and yeah with relatively predictable environments, which totally fits the standard theory actually. So yeah, this capacity to transmit traits is something that's just predicted by standard Darwinian theory. If you want to see it like that.

Cameron Ghalambor 35:26
Right, right, okay, yeah. So okay, so now the follow up. So the second kind of aspect of. the second driver of adaptive evolution that's working alongside non-genetic inheritance is adaptive plasticity, in your argument. So one thing that you kind of spend some time talking about is that there's many ways an organism can be plastic, and I think maybe in the same way with the way that you were describing the way that non-genetic inheritance can evolve. There's also a sorting process akin to selection that sort of favors the sort of realized plastic response that is tracking the highest fitness. So that kind of sorting process, I'm wondering if first you can kind of provide an example because I think compared to sort of maybe a traditional way of thinking about developmental plasticity, this is a little bit in how we think about the realized plastic response. So can you can you talk about that a little bit and how that is working alongside of this non-genetic inheritance?

Pim Edelaar 36:39
Yeah. So maybe let's backtrack a little bit. One experiment that I often do in my talks is that I ask the audience if we have a population, let's say a population of marbles, and and and I will promise I will come back to your question at the end of this. But imagine we have a population of marbles that differ in color, no, from white to black, and some are gray, dark gray, pale gray, whatnot. How could you, or how could that population, better said, how could that population of marbles change its average darkness? No, you can calculate the average darkness of the population if you just give numbers to how dark they are, and you can calculate the mean. How could we change the mean of a population of marbles that vary in darkness. And then I ask the audience to come up with suggestions of how that could be done. So now you are two guinea pigs here, and see how far we get. And actually, if you come up with a way that I hadn't thought of, the whole book falls apart. So the pressure is also on me, but so far that hasn't happened. So I'm pretty confident that it that it won't happen. For example, that way you can the population can become paler, right?

Cameron Ghalambor 37:51
And are these marbles akin to a sessile marine organism that is broadcasting its marbles randomly into the environment, and they just they just settle wherever they settle. Or can the marbles are the marbles capable of making decisions and rolling around? There's more complications here.

Marty Martin 38:15
Well, you can get rid of one of the colors of marbles, right? Although the black ones are gone.

Pim Edelaar 38:20
Yeah, completely right. Okay, I interpret it as you're suggesting that maybe some marbles leave or some marbles would arrive. No, depending on their color, is that what you're maybe getting at?

Cameron Ghalambor 38:32
Well, I'm just wondering if the relationship between the marble and the environment is something that is there like a random covariance, or is there something more more something more systematic?

Pim Edelaar 38:46
No, well in this case there is actually no environment. It's just a population of marbles. No, this is a theoretical example. But so Marty said okay, maybe some marble snow are taken out of the population because of the color, I guess you could also argue maybe some are added because of the color, right? What else could happen with the marbles to change the average color?

Cameron Ghalambor 39:08
Akin to selection is, I guess that would be the first example.

Pim Edelaar 39:12
Uh huh. Yeah.

Marty Martin 39:13
Are you going to allow the marbles to change? Can they become lighter or darker? The individuals.

Pim Edelaar 39:18
Fine by me. Do you want to do that?

Marty Martin 39:20
Okay. Well, I just wasn't sure if that was getting too much into Cam's sort of dispersing marbles idea.

Pim Edelaar 39:26
No, no, no. I think it's getting into Cam's topic of plasticity, right? So sure, marbles could change color. What else? What else could happen to change the average color of a population of entities?

Cameron Ghalambor 39:39
There could be stochasticity in the environment, and some just disappear by random, and you change the color just by chance.

Pim Edelaar 39:47
Yeah, sure, but that's still either adding or subtracting, or let's say removing or changing the traits. No, any anything else?

Cameron Ghalambor 39:56
Well, I you know I'm thinking about it like you know in a Hardy-Weinberg kind of context, right? So you can have drift, you can have selection, you can have gene flow, you could have assortative mating. Some of those processes could be random, or they could be non-random.

Pim Edelaar 40:11
Yeah. I would argue that in all cases, you have sort of two fundamental things that are happening. You're either changing the quantity of your elements based on the characteristics that they have, so you're adding or removing, or you're changing the characteristics of these entities, no, and leaving the quantity intact. So making marbles darker or paler. And that's actually what the Price equation is also saying- for any kind of change in the average trait value, you either have something akin, as Cam was saying to selection, or you have trait changes. And so what I'm arguing is okay. This sort of adding and subtracting, yeah, that's what natural selection is in a way doing, no, individuals that don't do well, they may not survive, or they reproduce less. So, so that sort of goes into that process. And that other process of trait change. There's a lot of biology that that that adds to that, but that can change the the mean of a population, and we don't really have a term for all of that biology, that can be that can be trial and error learning, that can be phenotypic plasticity, that can be the choice of your habitat. All of that is sort of change of the traits of organism. And I've discussed with people how do we call that, because I see that as a form of selection, no, I see that as something that organisms do, where they choose out of a set of options that they have, they choose certain realizations and not others. So there's a big scope for traits to be developed. Everything is possible. A marble could be from white to black, but if for some reason it's advantageous to be darker, then the marble developmentally could become darker.

Pim Edelaar 42:08
My argument is that that's not just a phenomenon that changes the variation that's available for natural selection to act upon. I'm actually arguing that no, this is actually to some extent, a type of selection that's enacted by the organism, no, it has a set of options available, and only a subset is realized. So clearly, that's something systematic happening here. That could be conscious because an organism is comparing different behaviors and realizes that one behavior is better than another. But it can be totally innate, driven by some molecular reaction or no. Like a bacteria can decide to metabolize one substrate versus another just based on relative concentrations. So there's nothing cognitive happening there. It's just a chain of events. Nonetheless, the bacterium is making a choice. Is no, there is a subset of options realized versus not. And I'm saying, if an organism has a lot of options and it only realizes a subset there, then that creates a systematic bias in the traits that the organism will have. That's how they can adapt, and that we know, or we understand as a form of plasticity. The cool thing is, if those choices are then transmitted to the next generation, then suddenly those choices become evolutionarily relevant. That's sort of how the second driver originates by combining this other type of selection that an organism does with this other type of inheritance that exists. If those two sort of combine, then we, I wouldn't say magically, but really it has nice consequences. We can have adaptation being transmitted from the generation that is adapting to the off-brand generation, but not because of natural selection, but because of the choices that organisms make, and hence the title of the book, right? The selective organism, because the organism is here replacing natural selection as the driving engine.

Marty Martin 44:16
Okay. Well, well, this is where it gets very gnarly, and I mean, controversial. And initially, when I was reading the book about halfway through, I was struggling with your. It seemed like almost two uses of adaptive plasticity, because in one sense, there's conventional adaptive plasticity that, you know, the environment releases phenotypic variation, and there's differences in genotypes and sort of adaptedness of that variation, traditional kinds of ways of thinking about it. But you're also making a subtle twist. This is the trickiness of adaptation as a concept, because within generations, individuals are different in their disposition to like make these choices among sets of options, and so there's like this within generation, among individual adaptation that's happening. And then there's the more conventional adaptive. But then the last thing that you said is that for this adaptive plasticity via choice to happen, it's not just that the choice is made, it's that the choice is transmitted. That's mind blowing and tricky. But some people might say that some of that is circular. Is there something else that, I mean, do you have an example that you can share about how choice gets transmitted in sort of a different than conventional way thinking about adaptive plasticity?

Pim Edelaar 45:36
I guess I would use the nematodes again, no. They have the capacity to produce a whole array of different RNAs. Some deal with viral infection. Some deal with specific nutrients. Some may deal with temperature change, you know, those are produced to regulate their expression of their genes. So they can express all these RNAs, but given the environmental conditions, they don't. They will express some, and they will not express others. So there is some sort of choice made by the organism. Again, not conscious, but you know, through all these reactional mechanisms, that happens. That, in principle, is sort of classical adaptive plasticity, and that is evolutionarily not very relevant, other than that it changes maybe natural selection pressures that the individuals are exposed to. Just you know, suddenly the variation is different, so obviously, the outcome of the natural selection process would be different. So in that sense, plasticity is relevant because the outcome will be changed. But it's not an inherently different process.

Pim Edelaar 46:40
However, these RNAs that they choose to produce in response to the environment can be transmitted to the next generation. So then, suddenly, we can say, okay, if the trait that we're interested in is resistance or you know resistance to stress, if that's the trait that we're looking at, then suddenly we see that the plasticity in one generation creates lasting adaptation across generations, no, creates a change in the characteristics of the population. So yes, suddenly development becomes evolutionarily relevant when it hooks up with non-genetic inheritance. That's sort of the magic combination that has to happen, which for a long time was thought to not happen, no. Meyer said, no, it was the achievement of the young science of genetics of showing that soft inheritance didn't exist. Nowadays we have so many studies showing that that's actually not true. That there is this transmission of acquired traits across generations. So, if we come back to your initial question, so sort of what needs to be fixed, one of them is the empirical evidence for non-genetic inheritance is overwhelming, but we're not really taking that on board in a very neat way, in a very organized way.

Cameron Ghalambor 48:04
Well, I wanted to follow up on that a little bit because you mentioned the Price equation and the Price equation plays a fairly prominent role in the book as a way of introducing and expanding these terms into the standard theory. And so maybe for the listeners, you could first kind of just give a brief description of what the Price equation is, and then how you modify the how you modified the equation to incorporate this sort of second driver of adaptive evolution.

Pim Edelaar 48:46
Yeah, so the Price equation was developed some 50 years ago as a way to describe trait change in the most general way. So it's not a predictive equation. It's not something that you plug in measurements and then a prediction comes out. It's really a way of tracking everything that is relevant. It is a mathematical description of the general process of trait change. And why is that relevant? It kind of helps us, as I said, to keep track of everything. No, there are cases where maybe there is natural selection and a trait is heritable, and yet there is no evolutionary response. Like how is that possible? If you then take the Price equation and you kind of put the numbers on all the elements of the Price equation, then you realize "Ah okay there was a part that I hadn't taken into account, and that explains why the net evolution response is actually zero". So it's sort of a bookkeeping exercise. As I said, it's been around for 50 years. By now, I think there's broad consensus that this equation is sort of a very good description of trait change in general ways.

Pim Edelaar 50:04
And so I use that equation, and that actually isn't my idea at all. I should credit other people, Bill Reich, and especially Jun Otsuka, who have shown how we can use the Price equation in combination with causal modeling to understand evolution. Maybe it's a nice anecdote to tell here, so when I was still dealing with habitat choice and whatnot, I came across his paper, and I was totally blown away. I thought, "Oh my God, this is such a nice approach to understand different phenomena". He had epigenetics in there. I think he had something with cultural evolution, something in this construction, and he showed how you can use causal modeling in the combination with the Price equation to make sense of what's happening here. But those were sort of case studies, and I was looking at those, and I thought, but these can be combined in a general model, and that was something I was kind of after already. So merely wrote to him. He's a, I should say, he's a philosopher of science working in Japan. So I said, I think we can make a general model of this. What do you think? He said, "Oof, yeah, maybe, but not over Skype. That doesn't work." I said, "I'll come to you straight away. He said, "Okay, come. And so I went, and he said, "Look, I'm a philosopher of science. I really don't know if this is going to work because I normally don't work with other people, and I've never worked with an empiricist. But let's give it a try." So I was there for two weeks. Every day we went over part of the arguments. He explained me how causal modeling worked. I told him more about biology, and after a week, we had a general model. We had a vision of how all his examples, plus the stuff that I was working on, could be explained by sort of a single, a more expanded causal model. And then he said, "And now what? Because you're here for another week." I said, "Well, let's start writing the manuscript." So after a week, we had a well-developed draft, and he said: "I am totally blown away. I've never been so productive." So, and that turned into a paper that we published in Biological Reviews, which is kind of the basis of the book, but it's not as nicely developed. It's systematic, but the book is much more systematic in its argumentation and scope also.

Pim Edelaar 52:23
But so the Price equation in that sense is sort of an anchor for a lot of the argumentation and scope also. And as I said, yeah, it basically some people find it very complex, but my argument it is just composed of these two main elements that you can either change the frequency of elements based on the characteristics, or you can change the characteristics of the elements, keeping the frequency as it is. Those are sort of the only two ways that a population can change. And then, to me, it makes total sense that you have to look at those two components always and with the same intensity. And when I go through these sort of basic concepts of can we expand them? I also every time take the Price equation and say, what does the Price equation or how can the Price equation help us to sort of keep this broad and complete focus? And yeah, it's super helpful for that.

Cameron Ghalambor 53:13
So, so Pim, the Price equation describes the change in the trait value from one generation to the next, and it does that by having two parts. There's the covariance between fitness and the trait, and then there's the sort of transmission bias that's associated with it. And I see how it's very convenient in in the context that you're talking about, but but for a lot of people, the the multivariate version of the breeder's equation, the Lande-Arnold equation, is another commonly used model to describe how the trait changes from one generation to the next. And the whole time I was reading and looking at the, you know, math and and the way that you sort of were expanding on on the Price equation, I kept thinking to myself, could this be applied in the Lande-Arnold equation? Because I don't know that it can. And I'm curious if that's something you thought about, or by introducing the sort of G-matrix, the genetic variance covariance matrix, does that make incorporating these ideas more complicated?

Pim Edelaar 54:32
The Breeder's equation and and also the multivariate Lande-Arnold equation, they are or can be derived from the Price equation, but you have to make simplifying assumptions, and what does that mean? You have to throw out some of the biology. That often works, but as I mentioned before, sometimes it doesn't. Sometimes, if you just have the components of, for example, the Breeder's equation, you would predict an evolutionary response, and I have in the book the example of the evolution of of laying date, where you know people have studied at what time in the year do do birds lay their eggs, and birds that lay earlier have more offspring, so there's natural selection on on laying date. They've also looked at parent offspring similarity. It's there, so laying date is heritable, yet they lay their eggs at the same date year after year. There is no evolution of laying date, and why not? Because the Breeder's equation is, as I said, a simplification of the Price equation, and there's other parts of the price equation that have been thrown out that have been neglected. And if you would look at those, then you realize why there's no evolution of laying date, and so the answer to the question is the Breeder's equation is maybe not the best way to look at adaptive evolution. It is, yeah, it is a simplification that has been very useful, is very useful, but sort of misses some of the biology. And so again, following sort of the argument of the book by not having sort of the full picture of what's going on, you are often right, but sometimes you're not. And if the sometimes not bothers you, then we need a broader view, no, to take that into account. Glass, the glass is half full. Now you can say, well, but we're right, I don't know, 90% of the times. You know, that's amazing. It is amazing. But if you're interested in the other 10% yeah, then that's where the hard work needs to be done.

Marty Martin 56:36
Yeah. So you know, this is difficult. This is difficult stuff, and you've done an incredibly impressive job explaining the complexity. I'm going to encourage everybody that's listening to read the book. You know, if you're enjoying this, you're going to get a lot from it. But let me try to sharpen up this adaptive plasticity idea again. Back to an example. Can you tell us about the tree sparrow study that your group did? I think that really is a sort of nice juxtaposition of how you want us to think about adaptive plasticity versus tradition.

Pim Edelaar 57:04
Yeah, so that's actually an experiment that we did, kind of coming back to this crossbill study that I mentioned, no, where we suggested that if birds choose where to breed based on is the food in that area, good for them or not? Do they have access to this food? And can then cause a divergence of populations? So what we did was what I think is a is a neat experiment. We had feeders in a forest where wild sparrows were able to to use them, but not all the feeders. We had feeders that only opened if a bird carried what we call a transponder on their leg, no, it's a little, tiny little device that sort of emits a signal that the antenna of the feeder would detect, and they could say, ah, this is a sparrow from one group or from another group. I, as a feeder, only give access to sparrows from group one, or I am a feeder that only gives access to sparrow from group two. And those feeders we put in two different places in the forest. We had a bunch of feeders that gave access to sparrows of group one in one part of the forest, and feeders that gave access to sparrows of group two in the other part of the forest. The sparrows are going around in the forest, and they realize I'm a sparrow of group one. I can feed in this part of the forest. And the sparrows of group two would quickly realize I can only feed in this other part of the forest. So the logical thing that the sparrows would do is go and, no, feed where they have access, and then nest where they have access to this food, and that's indeed what they do. So what we saw is that based on ecological performance, no, do I have access to food or not? Sparrows would choose where they live.

Pim Edelaar 58:49
So what's the plasticity here? What I argue is that a trait of interest here is the area where they breed. That's sort of the thing that they were choosing. Why is that relevant? Because depending on where you breed, also has an effect with whom you breed. Because if both males and females are choosing where to breed, when it's time to reproduce, with whom are they going to reproduce? With the other sparrow that's sitting next to them. So what you get there is strong assortative mating. That's indeed what we found—strong assortative mating for the type of food that you can eat and the type of habitat in the end where you're reproducing to such an extent that we had two populations that were almost completely composed of individuals of the same type, no, there were there were there was almost complete reproductive isolation between individuals of one type or another type. And you could say that these transponders, what we kind of did, it suggests that you could see them as birds with maybe large bills or small bills being able to eat on large seeds or small seeds, as in with the crossbills or with the Darwin's finches. So we kind of mimicked in a technological way, a manipulation of the phenotypic characteristics, the ecological characteristics, and the environment. And then what you see is that the organisms, yeah, they diverge in space, create local adaptation, reproductive isolation arises. And that was the pattern that we want to explain. And it also suggests that then the offspring is going to be pre-adapted because they would inherit, normally, the characteristics of the parents because there's assortative mating, so the chicks would have big bills or small bills too, and they're born in areas with the resource that they need. So that's an example of where this choice of habitat is then transmitted to the next generation because the offspring is already born in that habitat, no. So what evolves there is really the environment in which they live. So that's sort of the novel perspective here is that to understand how, what we call matching habitat choice, is evolutionarily relevant, the trait to look at is the habitat that they use, and that's the thing that diverges, and that's the trait that is transmitted to the next to the next generation.

Cameron Ghalambor 1:01:07
Okay, so Pim, I have to follow up here about. So I have two questions. So there's a little bit of I think confusion for me in the terminology, and maybe you can help clarify it for me. So the example you just gave I think is a very nice intuitive one, and but I think where I where the confusion sets in is that in the book you equate the adaptive plasticity with selection, and this is what gets incorporated into the Price equation. But for me, there's the, you know, the distribution of phenotypes that are tracking some local fitness optimum, and so they either do a good job or a bad job. If they're doing a good job, it's adaptive, and so this tracking of local optima through choice or any other form of plasticity versus calling plasticity selection, to me, I struggled with kind of putting those together, and so how should I be thinking about it?

Pim Edelaar 1:02:27
So it's not that I equate plasticity with selection, but I suggest that we could also look at it as a form of selection. So depending on your question, depending on the system, you don't have to do that, of course. If you're interested in adaptive plasticity, sort of the within generation tracking of developmental plasticity, it's business as usual. Like there's nothing wrong with that. That absolutely works. What I'm suggesting is, if we want to understand how maybe some of those developmental changes are transmitted across generations, and how that sort of fits in evolutionary theory, then maybe looking at plasticity as a type of selection, that could be helpful, because if we do, then you know this and that conclusion comes out. So I don't know if that answers your question. It's not that you have to change your perspective on plasticity-it's more broadening it out and using this perspective or that perspective based on what the topic at hand is.

Cameron Ghalambor 1:03:32
Okay. Next time we see each other, we'll talk more about that over a beer. Okay, but then there's a second follow-up question I have, which is you acknowledge in the book that plasticity can be neutral or sometimes maladaptive, but you don't spend a lot of time engaging with those ideas and discussing them. And and and for me, you know, I think about that a lot because to me the the way in which plasticity shifts the distribution of phenotypes, you know, is directly influencing the the strength of selection, and so, you know, maybe the most familiar example for people is is the Bogart effect, which you also talk about. Like, if if you can behaviorally thermoregulate and keep your body temperature in sort of the the right optimum, then selection on changing your physiology is very weak, because you are able to just you know manage to stay within what is probably more like stabilizing selection rather than directional selection because you're you're matching the phenotype to the environment. But, you know, there there's increasing examples where organisms, especially when they encounter new environments, don't exhibit adaptive plasticity probably because selection hasn't had an opportunity to act on it. And in those cases the mismatch between the phenotype and the local optimum is much greater, which generates really strong selection. And so either that speeds up adaptation and evolution because you're experiencing very strong selection, or if the selection is too strong, you know that maybe the populations go extinct because it's too much of a mismatch. But then when you expanded on on the Price equation, what I had trouble understanding was so if like through the Bogart effect, adaptive plasticity by definition is reducing the strength of directional selection, how adaptive plasticity could actually, because you you argue that it could speed up evolutionary change, and I think the the difference is that when I use the term adaptation, I'm thinking of it as being a product of natural selection. And I think when you say adaptation, you're saying that it doesn't have to be by natural selection; it can just result in populations that are diverged and locally adapted just through their own behavior. Is that a fair way of reconciling those views?

Pim Edelaar 1:06:23
If you say adaptation is only through natural selection, then I would say okay, yes, in the book, I make an argument that that's yeah a limited perspective. For me, adaptation is if we look at sort of the the cross generation aspect of it, is that organisms just do better, no, over time, ecologically, like they they just have a better performance they reproduce at a higher rate. Plasticity can, as you said, can be a factor in that because it changes the variation that is available to natural selection. So the outcome then of natural selection is going to be changed. How can it speed up or how can it improve adaptation? It is through this ability to transmit the traits that have been plastically developed across generations. That's sort of an independent contributor to adaptation. There is an interaction between the two, no, if plasticity is already dealing with the challenge that an organism is exposed to, then natural selection, the scope for natural selection, basically reduces or may even even evaporate, no. If we go back to the marbles, what is the adaptive thing to do for marbles to be darker? If all the marbles become dark, then there is no need to eliminate the white marbles because they're just not there anymore, no. And so there is this maybe even a yeah a balance between the two that natural selection is sort of dealing with the things that that plasticity couldn't solve yet.

Cameron Ghalambor 1:07:57
But I want to push back a little bit on that because like you focus a lot on the capacity for organisms to choose and exhibit adaptive plasticity in the way that they interact with their environments. But I guess you didn't spend as much time talking about the way in which the environment alters heritable variation, and so, you know, under some environmental conditions, heritability there can be a lot of phenotypic variation and very little underlying heritable variation. So, if we focus only on the plastic component of the phenotype and the way in which variation is being generated, at the same time that the heritable component may be very small, how do how should we envision then evolutionary change occurring? I mean, is it is it simply, maybe in your thinking, that we move away from just quantifying genetic change over time, like changes in allele frequency. Is that the simple answer?

Pim Edelaar 1:09:09
Yeah so I think there's two different components here. One is that that indeed sort of the genetic basis to traits is context dependent, you know, it varies with with the environment, but that's not the really the problem that can be measured and that we can take into account in our measurements of heritability and that would change the prediction of the evolutionary response and whatnot. What is, I think, more the interesting part here is that that selection may not be acting actually on the genetic component, but actually on the non-genetic component of a trait. And so our understanding of selection here is, yeah, it's just it's it's just not the right way to look at it. And that's been yeah that's been laid out, and that's actually not that's not a problem of theory. That's well understood. It just tells us that we cannot be too simplistic in just measuring a genetic basis and just measuring selection and then multiplying them one with the other, independent of heritability, maybe varying over time depending on the environment and whatnot. That's one part of it.

Pim Edelaar 1:10:18
I think where you're still struggling with is on the one hand seeing plasticity as operating within generations and thereby affecting the strength of natural selection, which I totally agree with. That is, no, definitely happening and and doesn't suddenly I don't deny any of that. But to sort of add the possibility that some of the plasticity that individuals employ, the results of that plasticity, the traits that they develop, can be transmitted to the next generation. That's sort of an additional capacity that plasticity has, and if we take that into account, then suddenly that's a game changer. Then suddenly, the within generation plasticity starts to have a between generation effect. How is that possible? Normally, people have said that's not possible because plasticity doesn't change the genotypes, no, it doesn't change the alleles. So therefore, plasticity is relevant to the variation that's created, but it doesn't actually change the genetic composition of populations. I totally agree with that. But if we expand our concept of evolution as a change in the composition of traits that are heritable, so a more broader interpretation of what what evolution is, then maybe some of the traits that have been developed by plasticity can be transmitted to the next generation, they are heritable, and the composition changes over time. So that's sort of an additional capacity that plasticity has if it teams up with non-genetic inheritance.

Pim Edelaar 1:12:00
So yeah, you have these two players, plasticity, adaptive plasticity in this case, because I'm interested in adaptive evolution, non-genetic inheritance. If those two players team up, they can change the game. That's the mental process that has to happen. And that is hard. I agree. It also took me more than a decade, probably, just to take it on a board. And I still find it sometimes hard because sometimes the logic takes you to areas which make sense but are very uncomfortable. In the book, I address some of them. For example, the evolution of geographic ranges. I apply it to that. How to think about local adaptation, that that location is a trait of the organism. I'm sure that a lot of people are like, "Whoa, what is that? What do you mean? But I think the logic holds up, and it actually helps. And I think it actually helps us to understand how local adaptation works.

Pim Edelaar 1:13:22
But I totally appreciate that it's not an easy process. But fortunately, you don't have to leave behind your perspectives. It's only a matter of expanding them to the extent that is sort of relevant to your own work. Because of course, if you're working on I don't know intergenomic conflict at the allelic level. Then you're good to go, right? You don't need another perspective. But if you're interested in organisms and what happens to organisms, and I think a lot of people are, yeah, then I think there's a lot to be gained with this expanded perspective.

Marty Martin 1:14:01
Slightly different direction. It seems like so much of this is where you want to put the emphasis on allelic change as evolutionary change, and I think that that was one of the differences that I heard between Cam's question and your response. And I guess I guess you know being an organismal biologist, and especially being a sub-organismal biologist, I loved that you represented organisms as Bayesian updaters. So that, but that didn't really come up as a concept towards, I guess, the latter third of the book. So can you say what they are, and more importantly, selfishly for me, like how do you see that as helping us advance this field and sort of add some flesh to your ideas? Specifically because once we came to understand the mechanics whereby genes and epigenetic effects worked, that really helped us figure out how to think about the theory, so, is it going to be valuable to dig into this mechanistic box of plasticity and I mean non-genetic inheritance is already happening, but how much is this Bayesian updating going to be a useful element for the future?

Pim Edelaar 1:15:10
It kind of connects with something that I mentioned before of non-genetic inheritance, sort of settling in between slow adaptation to maybe environments that are relatively constant or changing slowly versus very fast organismal responses through plasticity because the environment is changing all the time. So yeah, I have something about Bayesian updating because I kind of suggest that an organism when it's born, it gets genetic information from its parents that is really useful. That sort of sets the stage for a lot of things that are to be expected about the environment. There is going to be gravity. There is going to be oxygen. There are going to be predators, whatnot. You will have to deal with that. Here's some information that you can use for your development that helps you to deal with that. But then there could be more recent changes in the environment that have occurred, and the organisms would do well taking that into account, no. Maybe the weather is not quite what it typically is. Maybe it's a cold year. Maybe it's a warm year. Maybe there's more predators or less, or the food is a bit different, so organisms have developed capacities to sort of monitor the environment and take that into account in their development. So classical adaptive plasticity.

Pim Edelaar 1:16:31
And then there could be really fast occurring changes, like daily changes, or or even like a raptor flies overhead, and you need to deal with that. So that's behavioral changes, but that plasticity at an even faster rate. So all of this information has to be taken on by the organism, and it has to kind of update in a Bayesian way. How is the environment, and what are the characteristics that I should develop? And why they call that Bayesian? Because you kind of you start with an expectation, what you could call a prior. Then you have new information that's being added, that's being integrated, and you come up with sort of a posterior perspective on the environment and the traits that you need, and that's a recurring process. And by taking on first the genetic information and then maybe information from your parents that you received, and then information you collected yourself as an organism, you kind of come up with the best situation.

Pim Edelaar 1:17:30
How does it link to sort of the framework? Well, we already know that this sort of basic information, the genetic information, is passed on to the next generation. Why? Because it's super useful to have that, no? Organisms use that to sort of base their basic development on, as I said, because there will be gravity, there will be oxygen, you will need to eat and whatnot. But if some of the information that your parents collected for their benefit can be transmitted to you, and that helps you to kind of predict the environment in which you are going to have to develop. If that is useful information, then standard theory, no, Darwinian evolution through natural selection predicts that that capacity should evolve, no? Parents would do well to transmit to their offspring information that is useful for their development if the environment of the next generation is similar to their own, you know, to the parental environment. So, yeah, that's kind of how seeing an organism as a sort of a Bayesian updater, I think, is interesting to understand this different perspective on evolution because it looks at the transmission of different levels of information across generation.

Cameron Ghalambor 1:18:41
Well, okay, you know, I have to say, like intuitively, the idea of the organism as a Bayesian updater is very cool and very satisfying, you know, and it appeals to my inner adaptationist. But when I go out into nature and I see what organisms do and how they interact with their environments, you know, I while I I totally appreciate all of the examples of adaptive plasticity, I also see lots of examples in which the way that organisms interact with their environments often results in in the degradation of the environment, you know, density dependence, resource depletion, crowding. There are many ways in which organisms interact with their environments that don't make things necessarily always better, but often worse. You know, we can make the argument about human behavior, for example. But you know, even in the context of grasshoppers choosing to match the color background, you know, we also know, for example, with like the Fretwell-Lucas model of you know the ideal free distribution. That if so many individuals all go and choose the right habitat, you know, then it ends up reducing the quality of that habitat and forces other individuals into you know poorer quality habitats. So there's other aspects I think that you know need to be also considered. That you know the Bayesian updater idea to me, you know, in a very simplistic form, just is very adaptationist and doesn't accommodate these kinds of complexities of the sort of negative effects of the way organisms. You know, I think this is the idea of negative niche construction, or there's a term when when organisms actually make things worse for themselves rather than making things better. I don't know. I mean, I assume those are things that could be accommodated into the sort of more general model. But you know, I guess I'm just very cautious about like updating and select the sorting process is always resulting in an adaptive outcome.

Pim Edelaar 1:21:04
No, that I totally agree, and I don't. Let me say what I mean. So, if you say, for example, individuals if they would all go to the same habitat and then it becomes crowded and therefore is bad, then that they can take into account, and some individuals may decide, look, this really, you know, it's a great color, but there's no food, so I'm going to go somewhere else because there's lots of food, even though the color isn't really working out for me, but you know, it's still the better choice. So you could say that the negative effects on the environment that organisms have, of course, organisms will or can respond to that too, no. And then still do something that is maybe a positive update. Just basically dealing with bad stuff too, no, not only with good things. That's the part where I say maybe I kind of don't agree with the way at least how you describe it, but I do agree that I focus a lot on adaptive plasticity and kind of brush over the neutral and even maladaptive plasticity. But why do I do that? Because I'm interested in adaptive evolution. So my argument is: sure, this happens, can be super important, but I'm just not interested in it, no. Because it doesn't contribute to what I want to explain, which is adaptation.

Cameron Ghalambor 1:22:20
No but I think it does. I think it does because if you think about it in sort of akin to maybe the way people think about evolutionary rescue, where does the adaptive plasticity come from? I mean, if you initially make bad decisions, or, you know, the plasticity is maladaptive, that if that actually creates selection, then the outcome of that is an adaptive response. So, so the if if maladaptive plasticity is increasing the strength of selection, then it has to be part of the part of the equation for how adaptive evolution occurs.

Pim Edelaar 1:23:01
Yeah, yeah, yeah. Not totally. Yeah, yeah, yeah, yeah. So what I also argue in the book that yes, adaptive plasticity once it is there and once it teams up with non-genetic inheritance, no, can be an independent driver. But where does this driver come from? Obviously, it must have evolved through natural selection. Now, both the capacity for plasticity to be adaptive has been selected on and have been fine-tuned. But again, sort of in that sense, is predicted now to exist at least to to certain extent. Some of the plasticity is expected to be adaptive, exactly because of what you're saying, because natural selection would favor that, but also non-genetic inheritance is exposed to natural selection, no, that doesn't just happen, or in many cases not just coincidentally. But as this experiment that I mentioned before with the C. elegans that lose the ability to transmit traits to the offspring when it actually is maladaptive, suggests that non-genetic inheritance can also evolve, no, and so natural selection ultimately explains everything. So natural selection is still, you know yeah my ultimate explanation, and I totally agree with that. But that doesn't mean that once the second driver evolves, that it can't have additional and, to some extent, independent contributions, no. And I think those are the interesting ones because if you really want to explain things at a deeper level, at more complete level, and probably come up with better predictions and explanations, then this added level of explanation is just useful.

Pim Edelaar 1:24:51
I don't know if I say it in the book, but I sometimes say to people: natural selection, you could say, explains it all. But natural selection is only possible if there is actually variation, right? So if you're interested in genetic evolution, then ultimately it's mutation that explains it all. And natural selection is just something that appears once mutation is there. Would you therefore say, okay, natural selection just isn't interesting? It isn't no because it ultimately all depends on mutation. I would argue that yes, you could do that. That would be logically defensible, but you lose a whole lot of you know interesting biology and explanatory power. I think natural selection is super cool, very important. I think this sort of second driver is also super cool, maybe less important, because it explains less. I totally agree with that, but maybe we also don't yet know how much it explains because we haven't actually looked at it a whole lot. That's an open question, no, it's an empirical question. Like, how important is this?

Marty Martin 1:26:09
Well, speaking of empirical, of a sort, one that I can't resist asking because Cam and I've talked about it with so many people that have been on the podcast. There's about nine chapters where you're building towards organisms as agents, and then at the very end of the book, you seem to step back from the concept. So, can you sort of just tell us what you think about? You could have named the book the agential organism instead of the selective. So, what's your feeling about the concept of agency, and why does it feel like at the end it's not your favorite thing?

Pim Edelaar 1:26:44
Because I think it's both bleeding obvious that there's agency, no, in organisms. They do stuff, as Cam, for example, has said, you know, they eat resources and thereby there's less food around. That is an effect that organisms have, no, in the world, so we can't deny that that organisms have effects. At the same time, I don't think at the moment that it's a very useful concept, just because it is so bleeding obvious. I kind of have a breakdown at the end of the book where I say, okay, there's, you know, different levels of where organisms actually don't use the term agency. I think or hardly. What I mostly use is "do organisms affect their own evolution?" I think the more interesting question. And then if they do, how? And I kind of have a breakdown in how the many many ways that organisms can affect their own evolution, both in affecting the environment and and and through things like evolving the mutation rate or being sexual or asexual, etc. There's different levels or components to individuals affecting their own evolution. And then this second driver, no, adaptive plasticity combined with non-genetic inheritance, is yet another way that they can affect their own evolution. Is that an important one? As I said, that's maybe an empirical question too. But I do think it's one that has been neglected, that's maybe qualitatively quite different. If people want to jump on that and say, "Look, here's really an important aspect of agency in organisms. That is where the agency concept helps us to understand some real biology. I am totally okay with that, but it's not my main argument because I think the agency of organisms and the effect of organisms on their own evolution is already well established and is also part of the standard theory.

Cameron Ghalambor 1:28:55
Yeah. So Pim, as you know, we're kind of wrapping up, I think I pushed back on you on some of these ideas, but at the same time, I also want to say that you know I also really appreciate your perspective. And, you know, you have been advocating and pushing for the importance of like habitat selection as an important driver of you know population differentiation and things like that, and this actually you know affects me in a personal way because of my own research experience. So I think you may have been a reviewer on one of our papers, but for years we've been studying this island scrub jay, this island endemic bird species, and the whole species is found on one island. And years ago, a graduate student, Katie Langin, found that there's three pine forests on the island, and all the birds in the pine stands have long, thin bills, and they all spend their time feeding on pine cones. And in the surrounding area they are in oak forests and they have short bills. And our interpretation of this pattern was that this must be due to disruptive selection and we did..

Pim Edelaar 1:30:14
The classical explanation, right?

Cameron Ghalambor 1:30:15
The classic explanation.

Pim Edelaar 1:30:17
It's not plasticity. It must be divergent natural selection.

Cameron Ghalambor 1:30:20
Well, and we know that the traits quite heritable. We used an animal model approach, and in fact, yes, bill size is heritable. And then a more recent graduate student, Rebecca Cheek, did GWAS and found the same genes that you find in Darwin's finches and other bird species are differentiated in the exact way that you would expect across the different habitats, further confirming our sort of idea. But you know these were very small populations, and we collaborated with Paul Hohenlohe, and he had a student who did a very complicated quantitative genetic model, and the conclusion of that model was basically there is no way natural selection can maintain these differences. And that it that the only way this would work, and even even with assorted mating, it didn't work. The only way it would work is if the birds were choosing their habitats. And so we've we have started looking at using telemetry and looking at habitat matching, and, you know, exactly like your grasshoppers and the your tree sparrows. It does seem that the birds are at least, I mean, it's very difficult to quantify choice in this context, but there's certainly for a bird that could fly anywhere it wants to, birds with long bills seem to restrict themselves to the pine forests, and the birds with the shorter bills tend to restrict themselves to the to the oak habitat. So when I talk about that research, I say you know I I build up selection as the explanation for the pattern, and then I say, okay, but there's something going on here that we can't explain, and it it does seem the the alternative is, but I guess the I think where we diverge maybe in terminology is like whether it's a pattern of local adaptation, but because the pattern is not generated by selection, I feel like in my terminology, I would say this is an example of adaptive differentiation as opposed to local adaptation, which I strongly associate with being a product of selection. I know, I know that that's the old standard theory baggage that I'm carrying around with me. But I think you know that's going to be the barrier that you have to overcome. That people are going to be holding on to that kind of thinking.

Pim Edelaar 1:32:55
I would argue it still caused by selection, but my habitat selection, no? In a way, that's a nice way to think. Okay, but you know, selection isn't only natural selection. We have we have mate selection, you know, and we have that habitat selection. So we already use selective terminology in different contexts. So that's one thing. The other thing, yeah, as you mentioned, sometimes we realize that, you know, we have a pattern of well, let's call it differentiation and population differentiation. Natural selection just doesn't cut it. We had the same with the grasshoppers, as you said. We marked grasshoppers individually and then tracked them over time, and we realized, no, if they move as much as they do in random directions, then the divergence that we see would break down within a week, whereas they would stay constant, no, the divergence that we saw with with grasshoppers matching in color the substrate that they use was constant throughout time. If we said that must be due to divergent natural selection, the mortality had to be so high that the population would go extinct in a matter of days, so it just couldn't be that there had to be something else. And I'mso very happy that you're finding the same in your birds. And of course, I can neither confirm nor deny that I was a reviewer on one of those papers.

Pim Edelaar 1:34:18
But I think that is sort of the interesting thing here is that if we never knew that individuals might choose or select their habitats, if for one reason or another no one had ever thought of that, then, you know, your data just wouldn't match with what you see. The theory that you would use that well, if it's not plasticity, it must be divergent natural selection-it just doesn't cut it. And then what do you do? Well, I don't know. You don't publish it, and you forget about it, or whatnot. But by having this sort of expanded perspective, these other hypotheses present themselves, and I think that's the the value, yeah, of this this this perspective that I that I offer this supposed higher adaptive peak, it gives you, you know, a different view of the landscape, a different view of the world around you. It may suggest some alternative hypotheses that actually could explain particular systems, particular questions. Not always, not not all the time. You know, there's many things where you don't need it, but I think there's maybe more than we think, in many cases, that it is actually useful. So that's yeah, that's what I hope to to motivate people to at least entertain that, or to know that if I make an assumption or if there's something that I'm not studying, that is what I'm doing, no. I'm aware of the restrictions that I'm imposing in my research. Maybe you have to, just be to be practical, you can't do it all, but at least you know that you're maybe doing something or you're assuming something. Yeah, and not not because you didn't know, but actually you are aware of it. And then if something goes wrong, then maybe it's like okay, let's go back to my assumption, or maybe let's go back to this process because otherwise I just don't. I don't understand what's going on.

Marty Martin 1:36:02
So that sets up my last question very well. It's a practical one, and you partly answered it. But what does a biology built around your ideas look like? What are the things practically that individuals should do, that funding agencies might support the kinds of things that we do in our teaching to help our students? What is different than the status quo?

Pim Edelaar 1:36:24
So, so in the last chapter of the book, I have a number of suggestions for research, different questions, different approaches that people can use, different methodologies. So, yeah, that is a good resource to go to. If you say, yeah, what should be different in teaching? What should be different in funding? I guess not teaching and not supporting, not funding this sort of restricted view, unless it's really necessary, no? If you are only teaching population genetics, then you're good to go. If you're teaching evolutionary biology, if you're interested, as a funder, that people understand the evolution of organisms, and not only of genetic variants, then I would say, okay, this expanded view has things that are worth adding. What is my What is my advice? Read a book, and because I think it is so important that people read, and I hope that a lot of people read my book, I think we haven't mentioned that, but it's available for free. I've managed to convince Ministry of Science in Spain to fund for the publication of the book under open access, because I hope that that really helps people, yeah, to have access to the book.

Pim Edelaar 1:37:36
So perspectives really matter, no, in the end, a research perspective really drives the questions that come to mind. It really sets the research questions that's well known. That's like a feature of how research works. We know that the perspectives that people have are conditioning, really to a large extent, what they're doing, what they're finding interesting. As I said before, the only thing you have is a hammer, and then you only see nails, or you will only address the nails. And it's really up to the almost the creativity or the insight of of every individual reader to say, "Hey, with this altered perspective, this comes to mind, or now I understand this, or maybe I want to readdress what I did before, or I'm going to change all my research, I'm going to propose something else", no. In the end, science is a collaborative enterprise, and we're all hopefully pulling and pushing in the same direction. But everybody with their own individual contribution. So in that sense, I'm really looking forward to what people are going to do with this.

Cameron Ghalambor 1:38:38
Yeah, and I would add that the early chapters, although you kind of say that, well, I think there was some. If I remember, you said something like, well, maybe for the you know typical biologist, you can skip to like chapter six or something. But I also thought that the treatment of the variation, inheritance, selection, the kind of historical perspective was also, you know, very nice and very scholarly, and you know, I learned some new things reading both. So, you know, that was that was really nice.

Marty Martin 1:39:10
Good. Well, Pim, thank you so much for doing this. We wish you the best with the book.

Cameron Ghalambor 1:39:14
Yeah, thanks, Pim.

Pim Edelaar 1:39:15
You're very welcome. You're very welcome.

Marty Martin 1:39:29
Thanks for listening to this episode. If you like what you hear, let us know via Bluesky, Twitter, Facebook, Instagram, LinkedIn, or leave a review wherever you get your podcasts. And if you don't like something, we would love to know that too. All feedback is good feedback.

Cameron Ghalambor 1:39:41
Thanks to Steve Lane, who manages the website, and Molly Magid for producing the episode.

Marty Martin 1:39:46
And thanks also to Caroline Merriman and Cass Biles for help with social media, Brianna Longo who produces our awesome cover images, and Clayton Glasgow who blogs about topics covered in the main show. Check out his work on our Substack page.

Cameron Ghalambor 1:39:57
Thanks also to our Substack and Patreon. Subscribers and the National Science Foundation for support.

Marty Martin 1:40:03
Music on the episode is from Podington Bear and Tieren Costello.

Big BiologyOctober 22, 2026

Ep 155: The Selecting Organism (with Pim Edelaar)

Episode Transcript