Ep 129: Beaks and (fitness) peaks (with Trevor Price)
Which factors lead to the evolution of reproductive isolation? What role does hybridization play in speciation? Why are there so many bird species in the tropics?
In this episode, we host Trevor Price, a Professor in the Department of Ecology and Evolution at the University of Chicago and a Fellow of the Royal Society to talk about the evolutionary process driving speciation in birds. Our chat covers the decades he spent studying birds on the Galapagos Islands and in the Himalayas. We also discuss the challenges of doing this research in the wild,why bird distributions are limited along elevational gradients, and a bit about the role of phenotypic plasticity in evolution.
Cover art: Keating Shahmehri.
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Marty Martin 0:05
Hey, Cam, you're an expert on birds, right?
Cameron Ghalambor 0:08
Well, I'm not sure I would say I'm an expert, but I did teach ornithology for many years.
Marty Martin 0:13
So tell me, Mr. Ornithologist, how many bird species are there in the world? Oh,
Cameron Ghalambor 0:18
Oh no, I wasn't prepared for today's pop quiz. I don't know. I think the latest estimates, well, actually, maybe this was like 10 years ago. Uh I think the number was around 9,800 and I know there's been some new species found, so I'd say about 10,000.
Marty Martin 0:36
Well, according to the latest International Ornithological Congress world bird list. There's about 11,000 described species, but it's estimated that the true number will eventually be closer to 20,000 once we find and identify them all.
Cameron Ghalambor 0:51
Whoa. That's pretty surprising. I mean, I do hear about new species being discovered, but I didn't realize the numbers had jumped so much.
Marty Martin 0:59
Well, of course, how you define a species is going to make a big influence on the number. Many of our listeners have probably heard that taxonomists are either lumpers or splitters. Lumpers are more prone to group things together, but splitters are more likely to emphasize subtle differences, and these days, genetic tools are giving a whole different impression. Species that look very different are actually very similar, genetically and vice versa: similar looking species are genetically quite distinct.
Cameron Ghalambor 1:24
Ah, but altogether, things we lumped together historically must have been split apart into different species. There hasn't been any like new speciation since we started formally distinguishing different bird species?
Marty Martin 1:37
Exactly. Most estimates of divergence time among species are on the order of a million years, so any changes to our current number of species derived from our labeling them as such.
Cameron Ghalambor 1:46
A million years for a species to form is somewhat surprising for me. I guess, especially in light of thinking about how common hybridization is and how fast populations can evolve.
Marty Martin 1:59
True, but it's just not that clear yet about how long it takes for a hybrid species to become an altogether different one. We just don't yet know much about the mechanisms that lead to reproductive isolation and reproductive incompatibilities between what'll eventually become different species.
Cameron Ghalambor 2:15
Yeah, I agree. I recently read a very insightful paper from 2023 in American Naturalist, by Sean Anderson, Hernan Lopez Fernandez, and Jason Weir. And they argued that on shorter time scales, reproductive barriers can rapidly evolve when populations become adapted to different environments. But over longer time periods, these barriers can dissolve, particularly when environments change, allowing populations to interbreed. And they refer to these as "ephemeral species"
Marty Martin 2:49
In contrast to non-ephemeral species that are truly reproductively incompatible with each other, and have diverged over much longer time periods.
Cameron Ghalambor 2:49
Exactly. So one conclusion that Anderson and colleagues make is that we need to spend a lot more effort trying to quantify how long geographically isolated taxa have been isolated from each other and experience different ecological and evolutionary processes, while they're in allopatry.
Marty Martin 3:16
The role of allopatry, species interactions, and other processes In driving speciation is a prime interest of today's guest, Trevor Price. Trevor is a professor in the Department of Ecology and Evolution at the University of Chicago.
Cameron Ghalambor 3:28
Today on Big Biology, we talk with Trevor about his research on speciation in birds and the evolution of reproductive isolation and incompatibilities.
Marty Martin 3:36
We also talk with Trevor about some of the other aspects of his research, like his efforts and contributions to studying natural selection in the wild, the processes that limit the distribution of species along elevation gradients in the Himalayas and-
Cameron Ghalambor 3:49
My favorite topic: phenotypic plasticity.
Marty Martin 3:52
Along the way, Trevor shares little tidbits of arguments he's won and lost with his colleagues over the years, stories of his time as a graduate student working with Peter and Rosemary grant on the Darwin's finches and the fun but sometimes dangerous experiences he had while working on birds in India.
Cameron Ghalambor 4:06
But before we get to our chat with Trevor, a quick reminder that we're now a subscription based podcast, so only the first 30 minutes of the show will be free.
Marty Martin 4:15
If you'd like to hear the rest of the conversation, please go to our substack page, www.bigbiology.substack.com, and become a member.
Cameron Ghalambor 4:23
and become a member for just the cost of a cup of coffee per month you can access the full show, as well as extras available only to members such as Marty and my debrief on conversations that we have ask access to discussion boards to talk about the show with other listeners and a variety of other freebies.
Marty Martin 4:44
We've had to resort to this subscription model for most shows as our production costs,
Cameron Ghalambor 4:49
which mostly entail funds for our producers and interns,
Marty Martin 4:53
are just too high to sustain through grants and listener donations.
Cameron Ghalambor 4:56
However, we never want your lack of funds to prevent you from listening. It. If you just can't afford a subscription, write to us and we'll give you one for free.
Marty Martin 5:05
But If you have the means, please consider supporting us, as we can then give access to more students and other listeners that need help to be able to access all the show.
Cameron Ghalambor 5:13
And just one more point before we bring in Trevor, we want to emphasize what we're trying to do with Big Biology. We're trying to share with an international audience some of the most exciting and cutting edge work being done in the biological sciences.
Marty Martin 5:26
Yes, scientific journals and other venues do this, but they're often beholden to publishers or other commercial interests, and we're not. And these days, as the operations are located in the US, producing a Science Podcast seems apt to become more difficult in the near future, we'll
Cameron Ghalambor 5:42
We'll say no more about the future of federal funding for Science in the US. Nevertheless, to keep the episodes coming, we just need your help as subscribers.
Marty Martin 5:51
We want to continue to bring you the ideas of the world's biggest biology thinkers, without any obligations to businesses or other groups that might have agendas. We want to keep Big Biology about the science driven by curiosity, but we need your help to do that.
Cameron Ghalambor 6:05
Again our subscription can help make that possible. So please go to www.bigbiology.substack.com right now and subscribe.
Marty Martin 6:17
I'm Marty Martin
Cameron Ghalambor 6:18
And I'm Cameron Ghalambor
Marty Martin 6:19
And this is Big Biology.
Cameron Ghalambor 6:33
Trevor price. Thanks so much for joining us today on Big Biology.
Trevor Price 6:37
Thanks for having me. It's great to be here.
Cameron Ghalambor 6:39
So yeah, we're really looking forward to talking with you today about your research. And I just wanted to start off by saying I can recall the first time that we met, which is probably over 30 years ago. Maybe I was a graduate student, and you came to give a seminar, and after your seminar, we we went for a hike, and you know, I got to talk science with you, and you know that that hike and talking with you was one of the sort of highlights of my time as a graduate student. And ever since then, your research has been super influential and inspiring for my own sort of interest in evolutionary ecology. We may not always agree on some things, but you know, I just wanted to say, you know, it's real pleasure and honor to have you here with us.
Trevor Price 7:34
It's great to be here. I would like to say you haven't changed a bit, but unfortunately, that is not the case for either of us, but I have followed your work through the years too, and actually referred to it a couple of times. So it's mutual admiration, maybe, if that's the right word.
Cameron Ghalambor 7:54
Thank you.
Marty Martin 7:54
Yeah and Trevor, the paper, the 2003 paper on plasticity, that you wrote, was incredibly influential to the things that a big facet of my research focuses on, too. And I think we share some mentors in common. At some point in the past, bothRosemary and Peter Grant were on my dissertation committee, and you work with him as well. But, but how did you end up tell us about your path to working with Rosemary and Peter and sort of, how did your passion for birding transform into work in the Galapagos?
Trevor Price 8:25
Well, as we were discussing before the podcast started, I was basically in India for a year teaching myself ecology, you know, having been interested in birds forever, and I realized that I needed to have proper supervision. And just before I'd gone to India, I was at Cambridge, and I saw a paper by Peter and Rosemary, which I thought was really cool on the Galapagos. I think one of the very first studies that had actually color banded individuals and looked at them and shown differences between them. So they'd actually looked at variation within species. And they were at McGill, and they were working in the Galapagos. I thought: "This is great. I can spend the summer in Montreal, in the winter in Galapagos and do some fascinating work." And I was also very interested in quantitative genetics, which they were just starting up in the field, so all those things together, you know, the clear obvious that I, although I like working in India, I needed proper supervision, and the great project and the great places to work, just meant that I wrote to them and said, can I come and work for you, or with you? And fortunately, they agreed.
Cameron Ghalambor 9:41
Well and in that time, you know, you were, you were also part of this, this cohort with Dolph Schluter and Peter Boag and Lisle Gibbs and Laurene Ratcliffe. And I know, you know, when I was a graduate student, I was seeing all these just amazing papers coming out from, you know, that work in the Galapagos. And I'm curious, what was the, what was the intellectual sort of atmosphere at that time? It seemed like from the outside, it must have been very exciting and stimulating. But what was it like, you know, being part of that, that that cohort?
Trevor Price 10:19
Teah, you know, I worked on this island called Daphne, which Peter and Rosemary have now written up, because they carried on on that work for 40 years. So it's, you know, the classic example of selection causing morphology to change. And before me it was Peter Boag, and after me it was Lisle Gibbs. So I was actually intensively interacting with Dolph Schluter, who, of course, is one of the, perhaps the, you know, well, one of the foremost ecologists these days. He, just as you may know, won the Crawford prize. But we had very different training. He wanted to do ecology and I wanted to do genetics. So actually, Peter had us down for the opposite projects we took up. But yeah, it was incredibly exciting. Dolph and I shared a room, we cooked dinner together, we worked in the same office, and we debated non-stop about issue. And Peter was always willing to disagree with us. And Rosemary too, she definitely used to say, I don't think that's quite right. So it was a very exciting time, but it was basically the four of us. But I would add that University of Michigan at that time was extremely exciting. Many people on our corridor have gone along to be, you know, very successful like Marlene Zuk and Dave Cruter, they were basically just opposite me. So as a intellectual, you know, it's one of those rare occasions where there's a jiving of many things by chance.
Marty Martin 11:49
Can you tell us? I don't want to dig too much into the details, but I'm intrigued by these conversations the four of you are having. What was the topic? Give us an example of a topic that was sort of contentious, and maybe, who even won the debate, if you go that far.
Trevor Price 12:05
Yeah. Well, as you said that, I was trying to think of examples where I definitely won.
Marty Martin 12:10
Of course.
Trevor Price 12:12
And you know, they seem very, you know, I'm trying to think of an example that would actually sort of make sense today. But, you know, one of the debates was, what happened was we, you know, we had this big, famous drought on Daphne. And that caused the population to crash, and also for the larger birds to survive better than the smaller birds. But what it meant was, when we had the next rain, the chicks grew up to be large. And so there was a debate between us about whether the chicks grew up to be large, because there was basically very few individuals and lots of food, a plastic response, or whether it really was a response to selection. And actually, you know, we debated this, and Peter was poo pooing it. He's saying it had to be a response to selection. I think I was like, Well, Peter Boag did an experiment for his postdoc to show that you could change the beak size of zebra finches by giving them more food. So I was a bit more open about it. And, you know, this is one of the many cases where Peter won because, you know, more recently, the genomics has shown that they can actually see the genes that have changed. So that was one example.
Trevor Price 13:34
Maybe another example is worth talking about, because maybe I have a bit more of a I didn't completely lose this one was, you know, Dolph, and I used to talk a lot about his whole thesis was on competition, and I see that Cameron's been writing about that recently. And he was looking at two species that are along an elevational gradient, and one of his basic observations was that ecologically similar or morphologically similar species on different islands did not, you know, morphologically similar species did not co- occur on the same island. And he was made a very strong case that this was due to competition. But I was intrigued by the role of hybridization. So I was arguing, in fact, what may be happening is these birds fly across, and because they look so similar, mate with each other, and that is what's keeping, keeping them apart. And I think in that case, yeah, maybe, um, maybe there was more to hybridization than Dolph was accepting at the time.
Cameron Ghalambor 14:37
Yeah, well, that time was also a really exciting time in evolutionary ecology as a whole. So in 1983 Russ Lande and Steve Arnold had published their classic paper on measuring selection on correlated traits, and you were one of the first people to use that method in a natural population to look at correlated changes in morphology. Did you have a sense at that time how impactful that paper was going to become? Or was it just sort of, you know, this is the newest kind of method available, and, you know, we should it works well, to apply it in this particular system.
Trevor Price 15:25
No, I think I had a sense that it was a big key breakthrough. Well, you know, Russ Lande is a genius, and I'd been following all these papers before that. And he'd actually found money for me as a graduate student to come to Chicago because he knew we were working on selection. I mean, Peter Boag published his classic paper showing that larger birds survived better than smaller ones, relating it to seed distributions. So Russ was primed for me to come, paid for me to come, and I spent a quarter, you know, really trying to understand the methods. But his earlier methods were important. And, you know, separating the causal features, you know, what are the causal parts of the phenotype and which bits are just evolving as a correlated response to these causal parts was, you know, immediately, a big breakthrough, which I think we could see. Before that time, you know the idea that beaks change, or anything changes, possibly for a reason and possibly because it just happened to be on bigger birds, just wasn't clear. And you know that you know Steve Arnold and Mike, Steve in particular, but Mike Wade as well, were doing a great job at publicizing this across the community. So everyone was well aware that the Chicago School was the exciting place to be.
Marty Martin 16:51
Last year, we had Eric Svennson on the podcast talking about this paper. It was a paper that he wrote about the paper, and, you know, he had a lot to say about the separation of selection from the evolutionary response to selection, the legacy of the paper. I mean, it sounds like you're there's a very strong legacy of this paper in the field.
Trevor Price 17:11
Well what Eric's talking about was definitely earlier than that. I mean, if you want to go into the history of that, that had something to do with John Endler's sort of misidentifying what natural selection should be, where he said it involves genetic change too. Actually, that was an interesting debate, because, you know, Peter and Dolph at the time were ecologists and they took Endler's definition at face value, whereas I'd come from, you know, population genetic school where, clearly selection was on the phenotype and didn't require genetic change. And so at that particular point, I was losing to Dolph and Peter, but I wrote to Russ Lande and got a written letter back saying, yes, you're correct.
Cameron Ghalambor 17:58
Did you show the letter to Peter and Dolph?
Trevor Price 18:00
Oh, yeah, I should have framed it, put it on the wall, because I lost more than I won. But so Eric's talking about something that really did precede this idea of, you know, causality from correlation, which is, it's an interesting history, really, because, you know, Pearson did that a long time ago, but then he got lost when he went to what people call bean bag genetics, where, you know, you were just modeling a single gene that was subject to selection. And so if the history of the field had been different, we might never have gone through that sea change with that paper.
Cameron Ghalambor 18:37
Yeah, it's interesting. I mean, because I think that may be obvious to a lot of people today, but I think at, you know, at the time, that debate was, was, was a was a real one, this kind of more general problem of, you know, why traits that are under directional selection don't exhibit evolutionary change, I mean, that this is something you've thought about a lot throughout your career in the context of life history traits like clutch size and also breeding time and birds. And I think, you know, one of your contributions has been to sort of bring in the condition dependent aspect and the plasticity that's not always captured in the G matrix. And I'm curious, like, you know, there's been an explosion of studies, I'd say, over the last, you know, decade or so, where people have used animal models and field pedigrees to estimate things like heritability and how selection acts on quantitative traits. How do you see these studies? Do you feel like they're a major kind of advancement on our ability to use these kind of quantitative genetic tools in the field? Or are we still stuck kind of with some of the same challenges we've always had?
Trevor Price 19:58
Yeah, large pedigrees are. Obviously very helpful, and we've got some, including Jane Reid, your colleague, but it's very difficult to use. As far as I understand it, I haven't been following the literature that carefully. But you know, there was a flurry of using the animal model, which is basically using large pedigrees to estimate genetic components and then estimating selection on those components, and I think that has been shown to be statistically not really very effective or working, as far as I know. I mean, of course, everyone is now moving to genomics, where they can really look at things like polygenic scores and selection on underlying genes. So it's been superseded in that way. Having said that, it does seem as if this idea that heritable traits can be correlated with fitness but not evolve is still not completely widely appreciated. John Stinchcomb actually told me the other day that he, Lotchka Crook, and me were the only people who were still thinking about it. Now, sure that's not true, but it is certainly true that people measure, for example, selection on breeding day, and then you see papers saying, well, could that selection keep up with climate change? But of course, that's sort of a null question. If that it isn't truly selection on breeding day is that birds in higher condition are breeding earlier and producing more offspring, and it's got nothing to do with the genes underlying the system. In fact, if you think about it, with the genes underlying the system, it would mean that it's going to be even harder for selection to keep up with climate change than people are inferring. So it still seems to me that there's a lot of opportunity to consider further condition dependence. Perhaps I could just mention one other example of this, which is in humans. We see lots of studies now of selection gradients in humans looking at, say, selection on body size and determining that, there's a trade off between the sexes, for example, that maybe large men are favored over smaller men, and there is a cost to being a large woman. But there's clearly going to be condition effects which have not, as far as I know, been sorted out.
Cameron Ghalambor 22:30
Well, you know, for like, human height, I think the last paper showed there's like over 10,000 SNPs. You know, of a very small effect, mostly that affect human height. And we spoke with Nick Barton a couple years ago, and he was sort of lamenting the fact that, you know, we still don't fully understand polygenic selection, still a big problem. I mean, the molecular data seems to, you know, show that there are, you know, genes of large effect that you have a higher probability of detecting, but there's still, you're still only explaining some fraction of the total variation. And that seems a little bit frustrating and not very satisfying like we should be further along.
Trevor Price 23:29
No. And also, of course, there's going to be this sort of a statistical bias there, in which you know a gene that you pick up is one that's by chance become associated, so there's all sorts of statistical issues. But, yeah, you're dead right. We're studying those few genes of large effect and making drawing conclusions when there's all this other stuff going on under the hood that we just don't really understand. And you know, mechanism, how these genes are small effects, you know, might create all sorts of epistasis that we're not aware of, and they have pleiotropic effects that we're not aware of, and and how they're constrained. So yeah, there's a long way to go there, but it is striking that we can pick out some genes of large effect, like in the Darwin's finches. And I don't, you know, I don't know exactly how much of the variants are really accounting for but certainly enough to cause clear evidence for genetic change in beaks and where that variation is coming from.
Marty Martin 23:29
So we want to turn to talk to speciation. We've got a lot of questions about your work in the Himalayas, but having the chance to ask you this question directly, I simply can't pass it up, and you've already alluded to the complex potential roles of plasticity in evolution. So, so where are you putting your money right now? Is it more about shielding genetic variation for selection, or is it facilitating evolutionary change? Or is that sort of simple dichotomy even a sensible way to think about the role of plasticity?
Trevor Price 24:59
Yeah I mean, well, I mean, there's two parts to plasticity. And I don't know why I'm talking about this with Cameron and you two on. But, you know, plasticity as I understand, what people used to call the Baldwin effect. What Baldwin meant was that it enables populations to survive or persist. So that's the, you know, the first part. The second part is, if would it create genetic change on our or lead to genetic change? Well, you know, Baldwin didn't have a mechanism. He just said: "Well, if you survive, eventually there will be genetic change." So, you know, when you say, would it shield things from selection or not? I still think, you know, the peak shift idea is the way to think about this. And will plasticity generally bring you under another peak, or will it bring you some of the way which will then promote further selection? And I think you know so plasticity, A will enable you to survive a bit better, but B, it could well bring you into a situation where you're under a different regime of selection, and I think that's probably more important than just putting you straight under another peak and shielding you from selection.
Cameron Ghalambor 26:12
Yeah, and I think you're the 2003 paper with Anna Qvarnström and Darren Irwin. I mean, I was Marty and I were talking about this, that that paper was so influential in our thinking, because it was the first time where it was clearly articulated that, you know, in the context, like you say, of a peak shift. Well, if you solve the problem of a changing environment through plasticity, you could go from one situation of stabilizing selection to another. And well, then if you're under stabilizing selection, then there shouldn't really be any opportunity for genetic change in the population, and, that was, that was very refreshing to read, and quite profound, although also in some ways, very intuitive. And I don't know why that kind of thinking hadn't been sort of accepted earlier.
Trevor Price 27:13
Well that's really nice of you to say so. I don't really know what how to respond to that. I mean, obviously, you know, I thought other people had said it, but I, I thought, you know, our main contribution was just drawing a picture. I'd actually tried to get Mark Kirkpatrick to do a real model of it with me, and he just said it was too obvious. But that was not a model of, you know, like you said, I'd never actually appreciated that. One of the themes of that paper, the one you picked up on, was, if you go right under the peak, there's no selection. So we were just, I was just asking to do a model of genetic assimilation, which is, you know, moving halfway and then moving but, you know, it's interesting. Another point about this is that, well, first of all, I was asked to write a review paper for proceedings by, you know, the aforementioned Nick Barden, and he wanted me to write it on the philosophers. And I said, Well, I'm on my warbler study. I said, Well, it's not too early for that, but I've been thinking a bit about this, so it's quite he said, Yeah, okay. Quite serendipitous. But the other thing about it was, I would never consider that my best paper has no way I could have anticipated that that one would be the one that's my most cited paper. I've got many other papers that I would think were better, and I think this, you know, it's just, you know, there's two things. One is something gets picked up on, of course, and it gets more widely disseminated. You know, the classic example being Hamilton's kin selection theory, which we could discuss. You know, for years it just laid moribund, and then it was picked up and publicized, particularly in E O Wilson's work, and took off, so that's one thing. The other thing is, the literature is so vast. You know, reading a paper and deeply thinking about it is a lot of work. And I think, you know, my career basically came out of the fact that I just read Russ's papers, Lande's papers, but I couldn't read more than one of his papers a month, and I had to read it every day for that month. So these things just you know that some of my better papers just went under the radar, and you sent me your paper from last year, which is a fantastic paper, but I probably would have only read the abstract if you hadn't warned me that you might want to talk about it today.
Cameron Ghalambor 29:53
Maybe we can shift gears now and talk a little bit about another one of the areas that you've worked in. Is speciation. You literally wrote the book Speciation in Birds. And you know now, I guess the book came out in 2008 so it's, it's getting close to now, almost 20 years. But I guess going back to the time when you started to work on the book, what was, what was your sort of view at the time? Was your motivation to sort of communicate a particular view of speciation, or was it really more just to sort of summarize what the state of knowledge was at that time?
Trevor Price 30:37
Yeah, well, I might just start by saying when I started to write this book. Josh Cohen, who was my colleague in San Diego, discovered that Microsoft Word spell checker corrected the word speciation to speculation every time he wrote. He made a big thing out of that. No, I think I wrote that book for myself. And the idea was that if I learn, you know, I'm not, like, maybe both of you, and certainly like, you know, really good naturalists, that I don't get my ideas so much in the field, as I do from the literature. So I decided that I just wanted to learn what the literature had said, you know, I'm not really an inborn naturalist or anything like that. So, and I was, you know, I was pretty I thought, Well, it'd be kind of fun to try and write a book. But I was, you know, that's an arrogant thing to do, really. So I decided what I would do is just write some review papers, see how they went. So the first chapters I wrote were standalone review papers, sometimes done with colleagues like Dan, and I wrote a paper on learning and things like that. So that basically got me going. And then, you know, I thought, well, this is a good challenge. It has the advantage that you don't submit papers for a couple of years and get nasty reviewers rejecting your papers all the time, which has happened to all of us a lot. So, you know, I just had the opportunity in a sabbatical to finish it up. So it was, it was just basically a way for me to learn everything. But I did have in the back of my mind the one or two books that really got me into this area, Maynard's Smith's theory of evolution. I remember reading it when I was a teenager, and I did think, you know, if, like, just two or three people who are starting out read it and get something out of it, that would be already worth it, worthwhile goal as well.
Marty Martin 32:41
So let's talk about some of the major messages, and maybe start with somewhat obvious geography. So traditional thinking that speciation tends to occur when you have geographic isolation and over evolutionary time, the accumulation of genotypic and phenotypic differences that leads to reproductive incompatibility. That's a traditionalist way of thinking. How does that model hold up today? Is it a sufficient explanatory pattern for speciation in birds?
Trevor Price 33:09
Yeah, I think it's probably a sufficient explanatory pattern for a speciation practically everything. You know, Coin et al's book, I totally agree with. I'm very impressed with the speciation book by them, because they were two geneticists who just sat down and learned all the natural history. And you know, we're still seeing model after model of sympatric speciation as theoretically interesting, but empirically not really relevant. So, yeah. I mean, why do you need a whole book you just outlined how speciation happens? We're done.
Cameron Ghalambor 33:45
But I'm curious, Trevor, because, you know, so you know, you were talking about your debates with, with Dolph Schluter and, and Dolph, I think is really, at least, my impression has been that he's advocated for, you know, the idea of ecological speciation and and a shift away from geography and space more towards like mechanism and and process. And so I don't know if that's a fair way of thinking about, at least that's the way I think about it. You know, we shouldn't maybe think about allopatry and sympatry as much as we should think about like, what's selection doing? How much gene flow is there? Is that a fair characterization.
Trevor Price 34:38
I'm not honestly sure that it is. You're probably well aware of one of those fantastic students, Jason Weir and his recent student, Anderson, who, you know, just wrote a couple of papers on what they call the origin of non-ephemeral species. And although we have these rather remarkable instances of biological species being produced, such as sticklebacks and cichlids, they are very prone to collapse. And so certainly if, if you walk around in a Chicago wood, although it's minus 20 today, you wouldn't see anything. But if you walk around in a Chicago wood in the spring. You know, it's very difficult to find sister pairs of any taxon that are less than a couple of million years old, a very different timescale from cichlids and sticklebacks. And it seems quite clear that, to me, that long periods of allopatry result in a generation of what you just talked about before, incompatibilities. And then, if you have an environmental change, you know, you tell me which which one is likely to produce a diversification event. It's almost certainly something where the two species are already incompatible. It's not going to produce two new species, which can hybridize, and gene flow can across, happen across their border.
Trevor Price 35:08
So I think a very interesting question is species that are primarily produced through ecological speciation, divergent selection that enables sympatry very rapidly, before you got any incompatibilities. So if you would have just let the system run, would those two species ever generate incompatibilities between them? And if you look at species that are incompatible now, isn't a more reasonable scenario was that they had long periods in allopatry where these incompatibilities developed and then they came into sympatry. So does a benthic and a limnetic stickleback ever give rise to a benthic and a limnetic, incompatible pair of sticklebacks in the same lake? Or were there double invasions between long differentiated populations?
Cameron Ghalambor 36:59
But isn't the idea that if the hybrids have really low fitness, then you should have strong selection for reproductive incompatibility?
Trevor Price 37:13
No, I mean low fitness of hybrids will create reinforcement, so that will create selection for pre mating isolation. But you know, when you can't find a mate, you make do with what you've got. So we always get cross species matings. And you know, if I was asked about the paradigm, what's really happened since I wrote my book is that we know hybridization is everywhere, and so you really do need, I think, post mating incompatibilities. Now, of course, in ecological speciation, they're generated by ecological conditions such as no intermediate seed. There's a big seed and a small seed. If you cross the big and a small finch together, you get an intermediate finch. It has no intermediate seed to eat. But that, you know, as the Grant study has shown, is very problematic, because when there are intermediate seeds there, all of a sudden we have a lot of hybrids. We start collapsing to a hybrid swarm. We've seen in the sticklebacks too, all you have to do is introduce a predator into a lake, and that generates sufficient change the conditions they collapse again. So, yeah, no, I think you know people 20 or 30 years ago were criticizing people like Coin because he was studying 3 million year old pairs of species, looking at incompatibilities, and people had said it got nothing to do with speciation. They'd happen long after. But I think actually, they do have a lot to do with speciation. The time scale of coexistence of sympatric species is about the time scale that coexist of creation of at least some incompatibilities that affect hybrid fitness.
Marty Martin 38:59
So I have a question, and we all have our biases from, you know, the systems that we work on, and I work on range expansions, but I work on them in, you know, the decades sort of scale, house sparrows colonizing the world is a big focus of my lab. There's a decent number of passerine species. But we don't tend to think about House Barrow speciation. And yet, in the book and in your writings, you emphasize a lot about range expansion and range fragmentations. And we were just talking about, you know, sort of time scales at which incompatibilities arise, but thinking about these three processes of isolation, expansion and fragmentation. Again, this is my bias, but those seem to be two of those happen on very short ecological timescales, and then the incompatibilities presumably arise over longer periods. Is that fair, or when you say fragmentation and expansion, are you meaning a slightly different thing than, you know, those of us that think about non-native species and pests getting shipped all over the world in the modern context, is that just a different beast?
Trevor Price 39:59
Well, no. That's the Anthropocene for you
Marty Martin 40:01
Yeah, I live in Florida. I'm exposed every day.
Trevor Price 40:06
Yeah. And so I think, you know, there's a lot of allopatric, what we call allo species whose, you know, range is sometimes a but sometimes are separated by a mountain, but they're millions of years old, and that managed to get into each other's range. So I think that's the ultimate limit on speciation.
Marty Martin 40:27
So what are the, what are your favorite examples of, sort of, the role of range expansion in speciation? I mean, sort of, I guess my question is a little bit more. It's a little bit different. Have what have been the arguments about why expansions should sort of start in the first place, and over what time scales were they sort of expected to proceed?
Trevor Price 40:52
Well, you know, it's really, of course, we're talking about something that happened in the past. But you know, my favorite example, which you know, as in everything, is disputed, particularly by people like Robert Moyle. But I believe that the Eocene Oligocene boundary, 34 million years ago, was accompanied by a six degree drop in temperature, which gave an advantage to the song birds, as you know, they're almost half of all birds, to exit from Indonesia and move through the world, displacing non-passerines and sub-ocenes as they went. So this is a classic example where a combination of climate change and a superior competitor in that climate has led to multiple range expansions and adaptive radiations all the way across the world. And it takes time. I mean, they had to get into North America. You know, according to my estimates, maybe about 20 million years ago, you got an invasion that led almost 900 species in North America. So, and I should say, I don't want to, you know, I think the only real difference between myself and Robert Moyle is he thinks it happened more recently. But so that's the sort of thing that I think is really important, and it was triggered by climate change.
Cameron Ghalambor 42:13
Yeah. So this is something also I think about a little bit, and especially in the context of elevation gradients in the tropics and the sort of zonation of species that occupy these narrow bands of elevation. And I haven't worked in Asia, but at least in South America, what you often see is on either side of the mountain, closely related species that kind of occupy similar kind of elevational bands. But what you don't see are closely related species that seem to have speciated on the same side of the mountain. So like, as you go up in elevation and you have species replacement, it's not usually the case that you know, even if they're in the same genus, that they're each other's closest relatives that you know, would suggest maybe that they had speciated in situ. But instead, it seems like they speciated somewhere else, and then they've kind of sorted themselves along, you know, these, these kind of gradients that they occupy. Is that a similar pattern in, in Asia, that the systems that you've worked on?
Trevor Price 43:35
Yeah, I think that really goes back to my, you know, this general philosophy that you have long periods of allopatry, and then you come in and displace and you can see a snapshot of that, you know, Jared Diamond was the first person to point this out in New Guinea, that you can see this snapshot whereby the closest relatives are allopatric. And then you can see places where they're coming into sympatry , with one lying a bit above the other, then you can see other cases where they're in full sympatry. So you're right that closest relatives are generally not along the same elevational gradient. But it is also the case, rather remarkably, that the closest relatives along the elevational gradient do separate by elevation and not by, say, body size or other aspects of the niche. So that has been, you know, a point of investigation about why it is that if you look at not true sisters, but sisters made in a phylogeny of just that gradient, tend to be elevational replacements, in fact, nearly always are.
Trevor Price 44:45
There's one other thing that is worth pointing out, which is, you know, it is fascinating that these species have often very short elevational ranges in the tropics, maybe a few hundred meters, only. But they can go for thousands of kilometers and so in in and this is pointed out by Gary Graves, originally, all the way from Colombia to Peru, the same species can be occupying a thin band in the Andes. What hasn't been appreciated very well is that this is also true in the Himalaya. And it's, in fact, remarkable. It's a 3000 to one rule. So you actually have to go 3000 kilometers geographically to get the same community turnover as one kilometer elevationally. And that means you have to go out of the Himalaya, actually. So you know, if you come, if you go to Canada, you can see, you can see species in Canada that are, or at least, allopatric forms, like the raven and the wren, which are at the high elevations in the Himalaya. If you go to the and they've never been seen in the bottom of the Himalaya, just, you know, 20 kilometers away. And if you go to the bottom of the Himalaya, you can see species that are present in Singapore, you know, several 1000 kilometers away, but they never be seen at the top. This is, to my mind, a remarkable pattern that still needs to be explained.
Cameron Ghalambor 46:12
Yeah, this is where we might have some fun debating. You've argued a lot for the role of competition in species interactions in sort of preventing range expansions, maybe up and down the elevation gradient,
Trevor Price 46:29
Yeah
Cameron Ghalambor 46:30
What role does you know when, when you talk about the lowlands of the Himalayas, which are, you know, quite tropical, versus the higher elevation sites, which are, which are quite temperate. What role does sort of physiology play in terms of the adaptation to these narrow bands of climate?
Trevor Price 46:52
Right. Obviously, I've done no work on this myself, but I was just talking to Jill Jankowski, who's really had a big delve into this in the Andes, she thinks is quite minor in the Andes, in the Himalaya climate it is pretty damn cold. You know that the freezing line, we think it plays a huge part in creating these asymmetrical competition situations that you've highlighted. So species that live above the freezing line have to deal with freezing, and that makes them poor competitors, but good competitors who move above the freezing line simply die because they can't deal with freezing. So that sort of adaptation is clearly operating, at least in plants, and we've got some work on that.
Trevor Price 47:44
But there are multiple adaptations to the different it is striking in the temperate part of the Himalayas, how you have these unique habitats that turn over along the elevation of gradient, and you see strong adaptations of the birds to each habitat. So this will appeal to you, because you've worked quite a bit on nest predation. But there's birch trees in the 3000 to 3400 meter gradient, which are obviously deciduous and open, and there's just one warbler that breeds in them, and it has breeds on the ground. And you can experimentally show that's the best thing to do. Well, that's flanked above and below by Rhododendron above and conifer below, and the closest relatives of this species, which are the same size, build their nest in the trees. And you can show that's probably the most efficient for predation. So clearly, that's a big trade off there, which is enforcing what must be competition induced originally, you know. There's no doubt in my mind that if you remove those other two species, the other this one in the middle, would spread down and up a bit immediately and probably over time, adapt to spread even further. But there's a lot of fitness decrements that come on top of competition at present, if you move into a different habitat.
Cameron Ghalambor 49:11
Yeah, I've just been very curious about, you know, a lot of the focus is typically on the adults and what the adults do. What are they feeding on? What are they, how are they interacting with, with their close relatives? But what, what seems to be really unknown is, is what, what's happening with, as you mentioned, with the nests and and with the chicks. And it may be that some of the challenges of moving up and down a steep elevation gradient has more to do with, you know, how well will your eggs hatch and how well can your chicks survive?
Trevor Price 49:47
I think we still believe in competition, though, and the thought experiment is, if you remove every species from that mountain, they're going to move up and down. So basically, they'll have tons of food. And that will compensate for any fitness segments that they face. And you know, there was a this beautiful paper by Ben Freeman and colleagues in Science that really did show that in species-depapaurate areas, species have bigger ranges. So it's never one thing, but it's clear that if you come to occupy one habitat because of competition, you increasingly get adapted to that habitat, which leads to the trade off.
Marty Martin 50:25
Yeah, a lot of different questions coming in at things from a bunch of different perspectives, but using my bias to the neotropics, I mean, one of the lessons is, you know, as you move towards the equator, communities become more species. So how did it come to be if one of the ideas is that competition is really one of the means by which speciation happens in those communities over time, as they get more species, the niches fill. So it's sort of a little bit confusing about how does it get to be so speciesous, or was it in the past just to pauper it and they were accumulated up to such time as they're now saturated.
Trevor Price 51:05
Well, if you want to talk a big about a big debate that I've gone and lost again, this is one where Dolph and many other people have argued that the limit on species accumulation is reproductive isolation, whereas I've argued that it's range expansions, and maybe we're both in agreement that speciation slows because range expansions become harder, but I think more and more there's evidence for a role of reproductive isolation accumulation as a limit on speciation too. So yes, you know just I think that many communities are saturated, despite what I just said. And over time, the tropics has become pretty close to saturated. I used to think that it was the temperate region could also be considered to be quite saturated. But I'm beginning to think, beginning to believe, that I was completely wrong about that.
Cameron Ghalambor 52:10
What's the evidence that you would say is against that?
Trevor Price 52:12
Well the main reason I've stopped, I started to think about it was, so what's the mechanism. So what you have to do is stop dispersal from the tropics. You know, why don't all the species in the tropics come up to the temperate if it's not saturated? And we were talking about this just now, that if you've got one species that's adapted to freezing, one tree species, it could keep out all these multiple of species that are not adapted to freezing. So that's the way to stop disposal from the tropics. That means, if there's been extinction in the temperate region, the only way to, you know, build up species, is by within the temperate region speciation, and that will take time. And I guess what really shifted my view was that by working in the Himalaya, we see that above the freezing line, we've got bursts of radiation that have happened in the recent past, the last few million years. So that implies to me that there was extinction before that. And so we've got this turnover. And so we've got lots of species at the present time who are sort of allopatric above the freezing line, which has basically waiting to generate enough reproductive isolation to become sympatric. So this is an example where you need enough reproductive isolation to come into sympatry.
Marty Martin 53:41
So one other question that I think we want to talk specifically about richness in India, in the Himalaya, where you've been working, is it, again, my bias that certain species are really broadly distributed and others aren't. I mean, it is the case, you know, the house sparrow is a clear example. We could do the cockroach. We can do the Norwegian rat. A lot of those might not be meaningful examples, because historically, there were no humans to move things all over the world, so there's been a lot of help. They might not be representative, but, I mean, how do we think about, there is the yellow warbler. There are species that are really broadly distributed, right? I mean, how do we think about, are they just not common enough to think about as sort of contributors to community composition? And how can some species be so broadly distributed? I guess is the is the big question.
Trevor Price 54:31
Well, if you could answer that, you'd be very famous.
Marty Martin 54:33
Yeah well, I was hoping you would have the answer, Trevor.
Trevor Price 54:36
I think time is gone. Well, there are cosmopolitan birds, of course, I think there are three more or less cosmopolitan bird species. I mean, they all have the characteristic. What do they have a characteristic? They're all big. I'm thinking of the Osprey, the barn owl and the Peregrine Falcon. So they're all big. They're all able to consume prey. And I think the main thing must be that. They've had enough dispersal, they must move around enough, you know, you get fragmentation into different allopatric species, right? So, why? So the yellow warbler is, you mentioned the yellow warbler, and you know from our discussions, it's all over the northern hemisphere, and in the Galapagos, you know, you can say, well, it's in the Galapagos, because by chance it got there. If you go over North America, it is divided, isn't it, into several subspecies. So there's quite a few species that have clearly recolonized, you know, either since the last glaciation or the one before that. I mean, Chicago was under a mile of ice just 20,000 years ago. So there's been lots of opportunities for range expansions since the Pleistocene, and they're usually driven by extinctions. But that's not true, for example, for getting to the Galapagos, that must be just a chance flop it got over there. Having said that, of course, the Galapagos itself was a completely different habitat 3 million years ago. Climate, like we said, climate change is creating opportunities for range expansions, which are all messed up by us now.
Cameron Ghalambor 56:30
Well, back to Marty's question earlier about you know the this contrast between temperate and tropics and the tropics being more species and is part of the sort of explanation, also that the tropics then are going to have more specialists than the temperate zone, right?
Trevor Price 56:54
So, you know, in your paper 20 years ago, you sort of, you emphasize one aspect of Janssen's famous paper, "Why are mountain passes higher in the tropics?" which I think is what we all took home from that paper, which is that if you can't get over a mountain, you get more barriers to dispersal, And the less gene flow there is, the more like there is to produce new species. So species accumulate. That's very much a non-equilibrium model. Species continue to accumulate forever. But subsequent to that, and I'm not really sure if it is in Janssen, and if it is, it's buried right at the end of that paper, people had this corollary. It started with Christy McCain and and then also John Wiens had a paper similar Kozak and Wiens had a paper where they said: "Well, this means that elevational ranges should be bigger in the temperates than the tropics. That was what I didn't really understand. And but it immediately gives rise to these two classic you know, if you want to dichotomize explanations why there are more species in the tropics than the temperate, the non equilibrium one, aka Janssen through Galen bore and the equilibrium one, which is simply because generalists can expand their niches, you end up being able to pack fewer species in, in a saturated model. And the problem has always been you trying to tell those two apart when they're totally, you know, we don't have an experiment. You can't move mountains up and down latitudes. See what happens. So Emma and I basically set out to work out if these two things were reasonable alternatives, and if there is any way to turn them apart,
Trevor Price 57:20
And so, so where is your thinking now on?
Trevor Price 58:47
Well, like I said, I think I'm sure. Well, I'm not sure. I am sure that if I go to the Himalaya, they look like a pretty saturated system. We do see as all mountain ranges seem to show younger species at higher elevations, by younger species, I mean close relatives share a more recent common ancestor at higher elevations than they do at lower elevations. But even in that case, the millions of years separated much longer than it takes speciation to happen. So the reason that we think we've got younger species at higher elevations is because speciation was indeed more recent, but it was still millions of years ago. We believe it was triggered by a massive climate change about 6 million years ago, and one's lower down we're not as disrupted, that would be the argument. But if you go to the Andes, you see lots of allopatric species that are just not present in the Himalaya. And these, these allopatric forms, are clearly a product of a non-equilibrium situation where they can just wink in and out. And in the Himalaya, we believe that they winked out during the Pleistocene extinctions. So if you go, you know, above the tree line in the Himalaya, and you look at plants, you see evidence for non-equilibrium species accumulation. And, you know, I mentioned that of the one part of the evidence for that is simply, you've got lots of young species that are allopatric. And you know, I'm sure that in if you look at the Black capped chickadee, it's all over North America. So there's going to clearly fragment into allopatric populations if you just let the system run. So there's a non-equilibrium one. So the question has always been, is sympatry in non-equilibrium? If we to produce two black cap chickadees, could they come together in the same forest? And I still think it would take time. But I believe, without really any evidence, that I was probably too adamant in saying no.
Trevor Price 1:01:04
Now there's one more corollary I need to add to this, which is, again, hybridization conundrum. So I used to argue that species couldn't come into sympatry in the Himalaya because allopatric forms are completely reproductively isolated, so that, I think is still a good argument. But the problem is that if, if you're in sort of a situation of geographical isolation, and you fly into another place, even as a little flock, you're going to end up mating with the other species, even if you are having hybrids of zero fitness, that is an extremely powerful way of setting a range limit. So now, although I am sure that ecological competition is the ultimate limit, and I'm sure of that because of what you pointed out with respect to elevational range turnover, where we clearly have no interbreeding. The actual evidence in general, for limitation of communities through competitive exclusion of close relatives is, you know, still out there? Did that make sense?
Cameron Ghalambor 1:02:23
Yeah, although, you know, I guess I want to just add that I saw a recent paper from your group in Ecology Letters on another aspect of the community that I hadn't ever thought about, which are ants. And, you know, a lot of I think our thinking and a lot of our conversation has been in the context of, you know, closely related or morphologically similar birds in competition with each other. But of course, there are other things in the community, and turns out ants may be really important competitors that I had never, ever considered.
Trevor Price 1:03:05
I love to talk about ants. Absolutely amazing. Yeah, a very observant student came with me to the Himalaya once, and he'd been studying ants before, and he just pointed to these ants just eating everything else. I love to say it- insectivorous ant. And, you know, there's a lot I could say about these ants, but it's just we focused on one genus of ants, which actually just contains two allopatric species. There's no sympatry. I could say a lot about that because there used to be a lot of sympatry before the Eocene, Oligocene boundary, when it was much warmer, but most of those ants have gone extinct. Anyway, there's a lot I could say, but this ant is used nowadays in organic mango orchards in Australia to clean all the insects. How?
Cameron Ghalambor 1:04:00
Oh, wow.
Trevor Price 1:04:00
So it's very efficacious. And what my student did was she showed experimentally that if you remove ants from a tree, you get more insects on the tree compared with controls, and they're particularly beetles and caterpillars. And then she used fecal analysis of birds to show that beetles and caterpillars are what they really like to eat. So low elevations in the Himalayas have many less insectivorous bird species than middle elevations, and that's exactly where the ants drop out. Now Larry Heaney deserves the real credit for this, because he showed the same thing in the Philippines with small mammals.
Cameron Ghalambor 1:04:41
Oh, interesting. So small mammals competing also with ants?
Trevor Price 1:04:46
Yeah. And actually, there's a group of beetles too that only become common when ants drop out. Why ants drop out in tropical cloud forests? They're not in the Andes either. And you know, good old Dan Janssen had a big discussion about why we don't see ants in tropical cloud forests, where we see them everywhere else, amazing stuff.
Marty Martin 1:05:06
Well we've just scratched the surface of so many things to talk about. You've left us with a cliffhanger about Janssen's claim of ants. But we do want to give you the chance to raise any other topics. Anything we've not yet mentioned. Something else you'd like to emphasize, what else do you want to say?
Trevor Price 1:05:22
Maybe it sounds trite, but we are in a bit of a crisis in the world. And I think, you know, everything we talked about is relevant to what's happening in the world, particularly what you talked about with house sparrows and cockroaches. I just think maybe we should try and make ourselves a bit more informed about the state of the world. You know, one or two papers are well worth reading. There's been a couple of papers now in PNAS on how much of the world's resources we're using up. You know, I can't remember the exact figures, but I think something like 90% of mammal biomass is cows and people. And I think you know, maybe we should, in our even your young stage of your career, should at least consider, you know, getting informed about what I call COFID, which is climate change over harvesting, pollution, habitat loss, invasive species and disease, because we do not communicate well to our students or public at large about why biodiversity conservation is so important,
Cameron Ghalambor 1:06:33
Very, very good and also sober message to end on, but yeah, there is no bigger problem that we face.
Trevor Price 1:06:41
Well, yeah. I mean, yeah, I like to say that of those six things I mentioned, you know, only one of them is not a huge threat to biodiversity at the moment, and that's climate change. But if we don't do anything about it, then I'm convinced that if we go to three degrees, there's no point worrying about any of the other five threats. So in some sense, you know we should be aware of all of them.
Cameron Ghalambor 1:07:06
Yeah, good. Well, thank you so much. Thanks
Marty Martin 1:07:09
Thanks for your time.
Trevor Price 1:07:10
Well, thank you for having me.
Cameron Ghalambor 1:07:22
Thanks for listening to this episode. If you like what you hear, let us know via Twitter, Blue Sky, Facebook, Instagram, or leave a review wherever you get your podcasts, and if you don't, well, we'd love to know that too. All feedback is good feedback.
Marty Martin 1:07:38
Thank you to Steve Lane, who manages the website and Molly Magid for producing the episode.
Cameron Ghalambor 1:07:42
Thanks also to interns, Dayna de la Cruz, Caroline Merriman and Brady Quinn for helping with the episode. Keating Shahmehri produces our awesome cover art.
Marty Martin 1:07:52
Thanks to the College of Public Health at the University of South Florida, the National Science Foundation, and our Patreon and Substack subscribers for support.
Cameron Ghalambor 1:07:59
Music on the episode is from Podinton Bear and Tieren Costello.