Ep 111: Evolution of the Invaders (with Ruth Hufbauer)
How do small, founding populations establish and thrive in new places? What is biocontrol, and how is it carried out responsibly?
In this episode, we talk with Ruth Hufbauer, a Professor of Applied Evolutionary Ecology at Colorado State University about the ways that organisms successfully establish new populations in new places. Ruth uses lab experiments on Tribolium flour beetles to understand how evolution facilitates or impedes the founding of populations. In our conversation with Ruth, we discuss range expansions, species invasions, and biocontrol among other topics. Biocontrol is of particular interest to Ruth, as it can be an effective way to control pests, but also comes with some risks that the control agents themselves get out of control. We also explore the genetic paradox of invasion and talk about many potential mechanisms that could help populations to quickly spread to a new place.
Cover photo: Keating Shahmehri
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Cameron Ghalambor 0:08
Marty, what's the weather like in Florida these days?
Marty Martin 0:11
Oh, of course, as you know, pretty much perfect, partly cloudy, nice and toasty outside. How about you up in Norway?
Cameron Ghalambor 0:19
It's brutally cold. But you know what the house sparrows in my yard don't seem to mind. Every time I look out, they seem to be happy. And I think about you a lot. When I stare at those house sparrows. I think about all the different habitats and climates how sparrows have colonized and how lucky you are that you get to study them all around the world.
Marty Martin 0:41
Yes, we are incredibly lucky to be able to study this species all over the world- Kenya, Vietnam, Senegal, Israel, it's really been a fantastic project, we're really lucky to be doing it. It's such an interesting species for trying to understand the processes that have allowed for colonization of new environments.
Cameron Ghalambor 0:57
Super cool, but I have to confess there is another sparrow I think is a lot more interesting.
Marty Martin 1:03
What?! How can another sparrow be more interesting than a house sparrow?
Cameron Ghalambor 1:07
Alright, well, I'm fascinated by the Eurasian tree sparrow. It was also introduced to North America, but unlike its close relative to house sparrow, it's been unable to spread beyond the area surrounding the city of St. Louis. The two species looks so alike why was one species able to expand its distribution around the world while the other species has remained local?
Marty Martin 1:28
I have lots of thoughts on this topic, and we could do a whole episode on it. But the tale of these two sparrows highlights really big research questions about the ecological and evolutionary processes that constrain or facilitate how populations expanded geographic distributions.
Cameron Ghalambor 1:43
This question is not only an academic one, understanding what controls the spread of invasive species has vastly important consequences for human health, think mosquitoes, food security, think, agricultural pests, and biodiversity.
Marty Martin 1:58
Not only that, these ideas are also important when humans decide to purposefully introduce species into new environments. A classic, but kind of macabre example, is the introduction of the myxoma virus to Australia.
Cameron Ghalambor 2:09
Myxoma was a very effective pathogen of rabbits in South America. So when rabbits got out of control in Australia, this virus massively reduced populations. Now the pathogen has evolved to be more benign, so rabbits are far more numerous than most Australians would prefer.
Marty Martin 2:26
Well, in this episode of Big Biology, we talked to Ruth Hufbauer, a professor of applied evolutionary ecology at Colorado State University. We talked to Ruth about the evolution of new populations as they colonize new areas.
Cameron Ghalambor 2:37
Ruth's current research addresses the complex interactions that determine how some populations come to establish, and sometimes thrive, in new areas.
Marty Martin 2:46
Ruth is interested in this invader evolution for two reasons. First, colonization is generally interesting to understand. It's how all new populations get going and ever got going in the past.
Cameron Ghalambor 2:58
Take the genetic paradox of invasions, how do new populations ever get established and takeoff from a small number of founders? Clearly, some populations establish that how they overcome genetic bottlenecks, founder effects and all sorts of other challenges of being the first to arrive has perplexed biologists for decades.
Marty Martin 3:17
And don't forget our favorite concept: plasticity.
Cameron Ghalambor 3:21
Yes, how do invading populations ever adapt to new conditions if the plastic responses that helped them colonize also shield those individuals from the selective forces in the new areas? Another paradox.
Marty Martin 3:32
Ruth's other major interests in invaders has a practical bent.
Cameron Ghalambor 3:36
The applied dimension of her job title, right?
Marty Martin 3:38
Right. So many successful invaders are successful at the expense of resident species, including humans. A major focus of Ruth's research has been to use her experimental evolutionary work on beetles to reveal the conditions that facilitate spread of these pests.
Cameron Ghalambor 3:53
On today's show, we talk with Ruth about beetle adaptation, plant and animal invasions, and climate-related plasticity. We also discuss how this work is giving resource managers valuable insights into how to mitigate the effects of all sorts of different pest species.
Marty Martin 4:08
But before we get started, please remember that we're a nonprofit. And to be brutally honest, the Big Biology coffers are getting dangerously low. We really want to keep making your podcast but we can't do it much longer without your financial help.
Cameron Ghalambor 4:19
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Marty Martin 4:38
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Marty Martin 4:47
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Marty Martin 4:55
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Cameron Ghalambor 5:05
We're really grateful for your help.
Marty Martin 5:08
I'm Marty Martin.
Cameron Ghalambor 5:08
And I'm Cameron Ghalambor.
Marty Martin 5:09
And you're listening to Big Biology.
Cameron Ghalambor 5:25
Ruth Hufbauer, welcome to Big Biology. We're so excited, you could join us today to talk about your work on invasive species biocontrol and range expansions. Let's jump right in. Why should we care about climate driven range shifts of species insecticide or antibiotic resistance as examples of rapid contemporary evolution? What are your thoughts on how this kind of rapid evolution, how it's differentiated from sort of long term examples of evolution? Does it change the way we think about the evolutionary process when it occurs on such a rapid timescale?
Ruth Hufbauer 6:07
Yeah. Well, first of all, thanks so much for having me. It's really a pleasure to be here. And yes, I do think, I mean, we've known for around 20, 30 years that evolution is much more rapid than historically we thought it was. And that understanding that kind of dawning of understanding that started happening was just like: "Oh, wow, this can happen in a few generations. Oh, wow, this can happen within a generation." So realizing how rapid evolution is means we can't think about species ecology in the same way as we used to, you know, we used to think about competition as kind of a fixed trait of a species, for example, or what plant an insect fed on as a fixed trait or ability to avoid predation, or what means of capturing prey all as fixed traits. And these are, they're ecologically important traits that can evolve. And they evolve rapidly, some of them. So yeah, I think it really matters. And it really matters to those examples you gave of insecticide resistance, for example, that that matters to food production, and it matters to farmers and growers, livelihoods and the cost of food in the grocery store. So it matters.
Marty Martin 7:29
So it seems like a part of a lot of these topics. It's about adaptation. You know, you talked about insecticide resistance, so not killing the pest as effectively as before, they obviously have no interest in being controlled, we want to control them. We're going to talk about non-adaptive evolution in a few minutes. I mean, it becomes really important for many, many different reasons. But what can you tell us about the evidence for adaptation in these rapid context? What's the sort of gold standard, or what's a really good example that we might focus on?
Ruth Hufbauer 8:01
Yeah, sticking with adaptive evolution. So now we're just thinking of a gold standard for rapid adaptation as opposed to range expansion, for example, there can be comparisons through time and natural populations. Sticking with insecticide resistance, or herbicide resistance, a population is controlled, and then the next year, the population isn't controlled, for example. But what I often do is work with the model system, and then you can create environments where populations can evolve or not, and not let some of them evolve. And so that's a really, really direct way to look at the action of evolution and have an actual control. Because in nature, we typically don't have kind of a control scenario where something isn't evolving. Everything is evolving all the time.
Marty Martin 9:02
Right, I mean, that's even hard for me to get my head around. So tell us more about these systems where you "stop evolution." So you can get a better handle on well, yeah, that's adaptation. What kind of systems are you talking about? What do your experiments look like?
Ruth Hufbauer 9:16
So I work with an insect as a model system, a Tribolium beetle. So this is it's a flour beetle, so we're talking about flour that you make your cookies with, not flowers that you give your sweetheart. And so it feeds on flour, all sorts of grains actually. And so we can use that in the lab to create experimental environments. In nature these days, it's a pest in grain silos. And then in the lab, we can have very controlled environments where we can get different kinds of media, media are mixtures of different kinds of flour with different amounts of brewer's yeast.
And I like this as an experimental system, because they're deployed and obligately, sexually reproducing. There have been tons of really elegant, really cool experiments, looking into the role of rapid evolution, rapid adaptation to novel environments in lots of microbes. And those have revealed a ton of important things. And the way that they can have controls is they can like freeze them, stick them in the freezer, and then let a subset evolve, then resurrect the ones that are frozen and compare them. And so that is great. It's super rigorous. But a problem is if we're, as humans, often the things that we're concerned about, have obligate sexual reproduction, and are diploid or have more complex genomes. And so inbreeding happens and inbreeding depression happens. And all of these, they're things that are going on within those genomes that are different from a lot of the microbial systems. And so with Tribolium, I feel like I can kind of model better things that we're concerned about managing in nature, and also things we're concerned about conserving in nature. And then I completely neglected to say, how do you control evolution?
Marty Martin 11:15
Well, that's fine. I mean, we needed to know the background of the system to get our heads around the rest of it. So that was good.
Ruth Hufbauer 11:20
So how do you control evolution with something that's obligately sexual is really laborious- you have amazing students in the lab. So what we can do is have populations that are kind of running side by side with experimental ones that are evolving, where we replace individuals, one for one each generation.
So for example, if we release some individuals into a novel environment in our experimental system, so we might put it on a different kind of flour, for example, a different carbohydrate source. And we're interested in adaptation to that carbohydrate source, the control populations would be released onto that carbohydrate source as well. And each generation, when we census them, so that's something else that we can talk about, if we want to I can get a complete census data. So we know how the populations are growing or declining. We replace them with individuals that aren't in that environment. So each generation they're replaced one for one. So the population demography is essentially unchanged. But there's no longer a continuous line of descent and evolution.
Cameron Ghalambor 12:37
And so Ruth in these kinds of experiments, like so in your experimental populations, do you generate like unique family lines, where you're controlling the kind of genetic variation that goes into the experiment? Or are you trying to sort of maximize the genetic variation by just like putting in a whole bunch of outbred individuals?
Ruth Hufbauer 13:01
It really depends on the experiment. We've done both of those things. So with some experiments, saying, kind of, if you start with a genetically diverse population, how does for example, the number of founders influence the ability of a population to adapt? And then we can simultaneously either factorially, or in a different experiment, say what if you start with a population that's passed through a bottleneck, either a mild bottleneck or a really extreme bottleneck, we know that that should influence their ability to adapt, right. And so it's nice to be able to control, have the evolutionary control, to know how much of that adaptation is or inability to adapt is due to the initial founder effect and how much of it is the genetic background of the individuals that are founding that population?
Cameron Ghalambor 14:04
So I think that's a good transition to talking a little bit more specifically about range expansions. And that's something that Marty and I talk about a lot either in house sparrows or guppies. And one concept in this range expansion literature is the idea of a "pushed" versus a "pulled" expansion. Can you talk a little bit about those and which one you think is more common in nature?
Ruth Hufbauer 14:33
Yeah. So as a range expansion happens, individuals that disperse out to the front of the range expansion are individuals that were good at that dispersal. And so then they get out to the edge of that range expansion. And they mate with each other and their offspring then continue that range expansion. So you can have a pulled range expansion by individuals colonizing, good dispersers colonizing out at the front of those patches, bringing the population, pulling the population along behind them. And then "push" range expansions are the population growth is really, behind the front is kind of driving what's happening. And some similar processes are happening. But there can be, for example, positive density dependent dispersal, that then as the population grows, individuals are kind of pushed out of that high density patch and out into further space.
Marty Martin 15:44
In those cases, I mean, I think the expectation would be that that sort of a more random, some fraction of the population gets moved, they're not necessarily obvious pioneers in the sense that you know, longer legs or wings are the things that we've seen in many different systems. Is that fair?
Ruth Hufbauer 16:03
Yeah, I think, probably less so. We like to think about, you know, the extremes to understand, we as in we humans, or we scientists, like "there's this and there's that." So we like to think about the contrast and what's at the ends of the continuum, but really, those individuals that are pushed out might be the ones that have some particular tendency or ability to disperse.
Cameron Ghalambor 16:27
Do you sort of have a sense of what's more common in range expansions? Is it really maybe not a dichotomy? Or is it this kind of continuum? Or even in the same system, it could be both processes happening at different times?
Ruth Hufbauer 16:42
Yeah, I think there can be both processes happening at once. But it depends. I think, which dominates can depend upon the environment. So cane toads, they have expanded, largely, though not entirely, across a fairly continuous environment. And lots of the experimental work I've done with Tribolium, and other folks have done, have had constant environments. And in that case, there's nothing that is going to slow the range expansion down necessarily. If as the populations, if they're adapted to that environment, then this pulling by the dispersers, out in the front can be particularly powerful.
Marty Martin 17:26
Alright, so let's put these things together and get into the genetic details of Tribolium. You know, these various different systems to the extent we know them. I want to do that, from the perspective of what we all know, is the 'invasion paradox." So bear with me, I mean, I know you know, this story. But to get all of the listeners on board, I mean, how do we think about the roles of mutation and various sources of genetic variation and invasions? Cause introduced populations are small. And so because they're small, stronger effects of genetic drift, in general, mutation rates are not super high. So how do these new populations really ever get going, especially on the path to adaptation? How do we resolve this paradox? Maybe from the perspective of standing variation versus mutation?
Ruth Hufbauer 18:12
Yeah, I think there are a lot of things going on. So one thing is that new populations come in, and that might become the you know, the next big invader say, or might dwindle to extinction. First of all, the ones that dwindle to extinction, we generally don't see. So there might be lots of introductions that are happening of tiny little, you know, little propagules here, little groups of propagules there, and they just, they dwindle to extinction, they don't have the genetic variation to adapt to their new environment.
The ones that we see that are able to establish multiple things can happen. One, there can be introductions from one part of a range and productions from another part of a range. And so the standing genetic variation in each of those small groups of propagules might be low. And by propagules, like it could be seeds, it could be eggs, it could be the actual individuals. But then when they meet up in the introduced range and outcross with each other, then there could be actually much higher genetic variation than found in most native populations. So that's one thing that can happen.
Another thing that's important to remember is that if bottlenecks are short, most heterozygosity remains. So rare alleles, rare mutations are lost, but most of the heterozygosity is still there in a short bottleneck, and that's just kind of a fundamental of population genetics, that I think people forget how much variation is actually retained.
Another thing is that if the population is able to, so maybe it's not poised to adapt, and become the next big invader. But maybe the match of the environment is good enough that that doesn't matter so much. If the population is able to grow reasonably, mutation, even though mutation rates are low, mutation does… it adds variation that does add genetic variation there. There's now good data and I think a beginning of a shift to kind of discounting mutation as a source of genetic variation in contemporary evolution to realizing that no, in fact, mutation is contributing, at least somewhen populations get large. And if generation times are rapid, then from the human perspective, you know, there's many individual mutations can happen over the course of relatively few years. Because so many generations, so many individuals in some population of insects, for example.
Marty Martin 20:55
Can you say more about the kinds of mutations that happen? Because I mean, this is not something that I'm really so much into, but my lab has started to focus a lot on particular forms of gene regulation. Are there any kind of traits of mutations, special forms of mutations that play into the success of colonizing populations?
Ruth Hufbauer 21:14
I wouldn't say we're there yet, or if we are, then I don't have that knowledge. It's true that a lot of what we do see are deleterious mutations. So that's not necessarily playing into the success. But we know the mutations are happening, and, so you know, if you have a kind of a typical distribution of fitness effects of those mutations, some of them will be beneficial.
Cameron Ghalambor 21:38
This is something Marty and I've been talking about lately. And we've started to think about this a lot more in our own research. And I've been talking to other people about this in the context of the ability of guppies, for example, to adapt to new environments, seemingly from very low, small populations and low genetic variation. And I think I just finished reading, rereading, I guess now for the second time, Barbara McClintock's biography, A Feeling for The Organism, and more with an eye towards her thoughts on transposable elements' role in adaptive evolution. And I think, in the context of sort of what we know now, you know, with modern molecular tools that the idea of the genome as far more dynamic, I think, then you would think of in our traditional population, genetic models, and there's all kinds of crazy stuff in there. And sometimes it's, you know, predictable. And a lot of times it's not, but yeah, it just, you know, in the context of like, this invasion paradox, and these cases of repeated adaptive evolution from small effective population sizes, it does make me wonder what role these kinds of structural, big genetic changes might be playing.
Ruth Hufbauer 22:55
Yeah, absolutely. I think, huge roles, like you said, it's so much more complicated than traditional population genetics paradigm would have. And there are also things like, have you seen any of this stuff from my department on the evolution of herbicide resistance, where there are, there's extra chromosomal DNA that has increased in copy number. There are these little bits of DNA floating around the cells. And if plants have a lot of copies of them, then they're able to basically just, they're able to resist the herbicides in the- I would say they tolerate it from kind of my academic background- but the terminology used within weed sciences "resistance," so that the plants are able to grow just fine. And it's just this copy number of these little things that are outside of the chromosomes, and repeat and repeat and repeat and somehow get duplicated. And they're having huge effects on rapid, huge and rapid effects on phenotypes. And there's nothing Mendelian about it.
Marty Martin 24:17
Well, this is a good point, I think, to bring up another of our favorite topics, plasticity, because this copy number variation is often driving, you know, quantitative variation in the expression. I mean, that's not the only mechanism that can be involved here, but how are you thinking about plasticity these days? Because it's another one of these brings in another one of these paradoxes, right? Where the plastic organisms are presumably, really good colonizers. And yet plasticity itself is a well known mechanism to buffer selection, so the whole adaptation thing becomes kind of complicated if plasticity is initially favorable. So how are you thinking about that now?
Ruth Hufbauer 24:55
Yeah, plasticity I find to be kind of a mindbender. Is it a trait? Is it an outcome? One of the ways I'm thinking about it now is, with a specific study system, is that it's kind of. In this study system, I'm thinking about it. I don't know. Is it a trait or is it an outcome? And is it buffering selection? Or is it a response to selection? It's a response to selection in this system I'm thinking about.
So one of the natural systems natural as an a not an experimental in the lab system that I'm working on is a biological control agent that was released against a invasive shrub called tamarisk, that is in river systems across western North America. And so the cool thing about that, in terms of doing research on it, is that with range expansion, sometimes it's hard to find true replicates. But with this, because it's in different river systems, we can have different range expansions that are going down, we can't, with the Tribolium system, I'll replicate things, you know, 20 to 40 times. It's not like that, but at least we can say, okay, these three river systems are distinct replicates of this range expansion. And there, the beetle is expanding its range from the north to the south, which is also a little bit unusual in this era of climate change. At least for the northern hemisphere, we're often thinking of things moving further north, with climate change. But here, they were released into areas in Colorado, for example, and Wyoming, and then are spreading southward where there's more habitat, more of this tamarisk weed for them to spread onto.
So these beetles, they have to go into diapause to survive the winter. So diapause is like hibernation, but for an arthropod. And the cue that winter is coming is that the light changes. So in Colorado, we have nice long days in the summer. And then as fall comes, the days get shorter and shorter and shorter, and the short days precede the hard frosts. And so those short days cue beetles to go into diapause hide in the literature- in the literature that is so funny- hide in the litter. I clearly need to have another sip of coffee or two. And their physiology changes, they resorb their fat, their eggs and bulk up their fat bodies.
So in the south, however, the day lengths are more constant. So down in southern Arizona, for example, days in summer are a little bit longer than days in winter, but not that much longer. And days in winter, are all much closer to 12 hours, they're all relatively short. Whereas in summer in Colorado, like you start with a, you know, a 16 hour day and you go down. Now I feel like I am getting us off on too much of a tangent, but they need to cue into a different day length to be able to survive the winter, because even though it's further south, and it's warmer, there's still a winter. So they risk freezing to death, and also the leaves fall off this tree. And so there's not enough for them to eat.
But the light cue sends them into diapause basically too early. Because the winter temperatures, they could in fact have many more generations. There's both evolution of what light/daylength regime they cue into. And there's evolution of plasticity in that. So in the north, no matter what the temperature, it can be a warm, sunny day, but if the light is at a certain length, they will physiologically start to enter diapause. And what my graduate student, a graduate student in my lab, Eliza Clark has found is that in the south, it's temperature dependent, whether a daylength sends them into diapause depends on the temperature. If it's warm, they'll keep going and have another generation. And if it's cold, they'll start the path into diapause. So there's this amazing evolution of plastic response to day lengths that doesn't exist in the north. So there, the plasticity is absolutely part of their adaptation to the environment and their ability to continue further spread. Which is not published yet, so you haven't read that one!
Cameron Ghalambor 29:42
Okay, and also, I that think, really resonates with kind of my thinking about sometimes plasticity. So you have this ancestral plasticity that's based on the length of day as a cue?
Ruth Hufbauer 29:56
Right, and so there's already plasticity there just in In what what phenotype do you get based on the length of day? Yes.
Cameron Ghalambor 30:04
Right, but then when you move into this new environment, that is not adaptive, that type of plasticity is not beneficial in this new environment. And so it's initially maladaptive. So there must be really strong selection to evolve, either in this case, switching to a different cue or relying more on a different cue. And that initial mismatch, I think, between the phenotype that's produced based on the ancestral plasticity versus what ends up actually evolving, is probably what generates very strong selection. So where does the adaptive evolution come from? Where does the strong selection come from? It's because it's not always adaptive to be plastic, or at least, you know, the plasticity doesn't always necessarily help you in these new environments, because there hasn't been an opportunity for selection to act on the variation.
Ruth Hufbauer 30:56
Absolutely. So another really cool part of this story is that Eliza actually did an old school half sib mating design, and measured heritability in a trait related to going into diapause. In terms of how quickly beetles enter diapause, given a daylength. And given a daylength, close to their natal environment, so that they're probably not maladapted. It's not if they're, if they're not perfectly adapted to it, if they're not going to be far off. There was a ton of heritability among her half sib families. So lots of genetic variation and how long it took them to go into diapause.
Ruth Hufbauer 31:42
You give them a day length. So these are relatively northern beetles, you give them a day length representing a southern fall, and there was zero heritability.
Cameron Ghalambor 31:54
Wow.
Ruth Hufbauer 31:54
So it's like if they move too far, yes, there's underlying genetic variation, there's stuff going on in their genomes, it's there. But if you move too far, that is not even expressed. But if you move a little ways, there's a ton of variation selection can act on.
Cameron Ghalambor 32:12
Just to kind of clarify like how heritability is calculated. So we think of heritability as sort of the the additive genetic component that gets passed on from one generation to the next, divided by the total phenotypic sort of variation in the population. So I'm guessing then what's happening is when you simulate this very southern environment, the amount of total variation must get really huge. And it just swamps out everything else.
Ruth Hufbauer 32:41
That is exactly what I thought would happen. And when Eliza told me the basic pattern, what I thought was happening, but it's not. It's so strange, the total phenotypic variation is very small, and the additive genetic variation is even smaller, there's no variation expressed. So additive genetic variation goes down and total phenotypic variation goes down. Because like you said, like the genomes are complicated, like additive genetic variation, even though we think of it as a thing, it depends upon the environment, just the additive genetic variation, and then the phenotypic variation depends on the environment as well. And both, I expected the additive genetic variations to stay the same and total phenotypic variation to vary by environment, but both of them changed radically.
Cameron Ghalambor 33:38
But you know, I wonder, in this case, if traits related to diapause fall under this kind of like threshold model, where you have to cross some environmental cue, some threshold before the phenotype can be expressed. And so maybe it's one of these cases where you don't reach the threshold. And so then the trait doesn't get even expressed.
Ruth Hufbauer 34:04
Yeah, I think it is very much like that. And in this case, it's almost, it's a threshold, but everybody has completely crossed that threshold. Because day lengths in the south are shorter. So a northern beetle thinks, to speak very anthropomorphically, that: "Oh my gosh, I'm so late, I haven't gotten into diapause. And yet winter is already here, go fast." Everything goes into diapause absolutely rapidly, and there's no variation in that. Whereas in an environment close to their home environment, they're going into diapause at all different sorts of timings, different rates.
Marty Martin 34:48
Interesting. So okay, I was going to come up with a brand new word, but I like you guys’ explanation, "regulatory overload," but in fact, it's more that they're getting a signal. Everybody's got getting the signal and responding to the signal really quickly and diapause just happens for everybody. So that's why the heritability declines in everything. Can we track back to the first part of the story, though, because you said that the new thing that happens in the southern populations is that they're now switching to temperature as the more adaptive cue for a presumably adapted cue for entering diapause. Do you think that that kind of transition is a common thing? In general? I mean, it seems to be a, it would be a difficult thing and a lot of systems for just paying attention to some wholly new cue, but temperature and day length, you know, they correspond reasonably well across the landscape and in a lot of places. So how are you guys thinking about that now? Was that transition easy? I mean, how do you think it happened?
Ruth Hufbauer 35:45
So first, a point of clarification, they're not transitioning wholly to temperature, it's a combination of temperature and day length. So if temperatures are cold, and the day lengths are long, they will not go into diapause. It's that temperature is modulating their response to day length, such that they can have a little bit more time to feed and reproduce, if it's warm. And if it's cold, and the days are short, they'll go into diapause.
Marty Martin 36:17
Okay, so do you think it's an issue of sort of weighting these cues then? That in the north, they wait day length, most, and maybe temperature little to none. And then as they move south, they come to balance these things out a bit more?
Ruth Hufbauer 36:30
Yeah, I think in the north, if again, speaking anthropomorphically, if-
Marty Martin 36:35
We love to do that, that's fine.
Ruth Hufbauer 36:39
Yeah, if the beetles, if they get it wrong, and they aren't in diapause, when that first hard freeze comes, like, in two days, we're gonna have temperatures of 10 Celsius. It's gonna be really cold overnight. And it's been balmy and lovely. And just so. But if a beetle isn't in diapause, already, it's dead. The consequences of not going into diapause in accordance to daylength are dire. Whereas in the south, the consequence of not going into diapause, according to just daylength, are much milder. The freezes are much milder, some might be able to make it through. And they come much later. And the benefits of not going into diapause are much greater, because they can keep reproducing, and they can keep feeding and that family line that keeps reproducing and feeding is growing relative to the other family lines that have gone into diapause, and wake up next spring with fewer offspring.
Cameron Ghalambor 37:37
Yeah, interesting. So I wanted to circle back though, you said something that really kind of caught my ear, which was that plasticity's role as a sort of a consequence, versus what was the
Ruth Hufbauer 37:53
Yeah, Is it a trait itself or is it an outcome?
Cameron Ghalambor 37:58
Well, so I'm curious, and maybe I don't know if you have data on this, but like, within the Colorado populations, how much genetic variation do you see for the plasticity? So do you see evidence for genotype by environment interactions across the different family lines? Because presumably, that is the variation that then selection acts among these different lines? And I could imagine maybe, in this case, that they either might all have similar slopes, similar plasticity, or there might be, you know, variation in their sensitivity to the cues?
Ruth Hufbauer 38:40
Yeah, that's a good question. What we have is, as you pointed out before, that just going into diapause, that's plasticity. And now I'm talking about this other layer of plasticity, you know, like temperature modulating that, so just the going into diapause by day length, there's genetic variation for that plasticity, but we don't have data on the role of temperature in that.
Marty Martin 38:59
Along these lines, you wrote about this word, "evolutionary potential," is it straightforward to measure that? I mean, if you think that evolutionary potential is a meaningful concept, you've got your next graduate student says: "Hey, I agree." And so what are you going to decide to go out to a controlled or unintended to be controlled population and measure.
Ruth Hufbauer 39:23
This is one of those places where it can be fascinating intellectually to quantify something like heritability or evolvability as a form of evolutionary potential. And that on the practical side, we don't actually have to do that, you just have to start with enough individuals of a population, you have reason to think has some genetic variation has enough genetic variation and the evolutionary potential will be there. It won't necessarily, so like the beetles on tamarisk that have spread from Colorado, down south through, all the way to Mexico, they were initially released in Arizona and didn't survive. So they did not have the evolutionary potential to adapt to that environment at that time, but doing it more slowly from north to south, they were able to. So that's not to say that, you know, genetics immediately solves it all, having a large propagule of diverse individuals immediately solves it, but it's a start.
Cameron Ghalambor 40:31
So Ruth, we've been talking a lot about genetic variation, and the potential for populations to evolve, and there's this concept of genetic load, especially when we start to think about like the ability of a population to adapt to a new environment. And I know you've thought about that a fair amount. Can you talk about what genetic load is and why it's an important characteristic of populations to sort of quantify?
Ruth Hufbauer 41:03
Yeah, I would say if you're thinking about phenotypes, genetic load is the difference in kind of fitness or performance otherwise, of an actual individual relative to some ideal individual genotype that doesn't have all of the deleterious mutations that that actual individual does. So we all have lots of deleterious mutations in us, right? For humans, it's something like we have somewhere between two and six lethal deleterious mutations per individual. And these are recessive, thankfully. But if they were then, as diploids, they were in a homozygous state, instead of being recessive and heterozygous, then we'd be dead. So genetic load is taking into account the fitness effects of all of those various deleterious mutations that are in an organism's genome and looking at what is that fitness effect? That reduction in fitness relative to if you didn't have those deleterious alleles?
Cameron Ghalambor 42:06
And so then how do you estimate that optimum that you compare to?
Ruth Hufbauer 42:11
Yeah, I know, yeah. So we, I don't have any way of creating that magical optimum, if I did, you know, humans would stop aging, all sorts of things would happen if we could do that. So what what I've done experimentally is, is if you take, for example, two populations that have been evolving independently and out, cross them to each other, then all of the deleterious mutations that have evolved through drift, through inbreeding, to become homozygous and therefore expressed and therefore reducing fitness. When you're out crossing them, most of those are going to be masked, you know, it's basically kind of hybrid vigor. You know, they're going to be paired up with an alternative allele, and so you're not going to have that recessive mutation expressed. And so you can use that fitness, the fitness of those individuals to say, the difference in fitness between the outcrossed individuals and the other population to say: "Wow this population is suffering from a lot of genetic load."
Marty Martin 43:22
I want to talk about the sort of practical ramifications of this kind of work, because what I find really neat about your research is that, you know, it's valuable in the basic biological sense, but it also has application to biocontrol. First, though, can you say something about one of the things that we don't think as much about as maybe we should, and especially with regard to biocontrol, we need to think a lot about. What's the combination of factors at these vanguards, in these range expansions? I mean, sometimes it seems to be the case that you can get this mix of phenomena that leads populations to really just run like wildfire. I mean, you get, you know, these pioneers maybe out on the edge, and then you're getting some kind of metapopulation structure or, you know, the feeding into this genetic variation allowing for admixture And eventually you get this just sort of big rapid, like even more rapid than the original colonization, that things just really speed up. So what are the kinds of conditions that most concerns you in the sense of biocontrol?
Ruth Hufbauer 44:22
So biocontrol, lots of things come under that umbrella of controlling a pest whether it's a weed or an insect pest or something else, an arthropod, with another living organism. So I'm mostly working on insects that are controlled by insects or weeds that are controlled by insects. But there can also be plant pathogens that control weeds, for example. So a major subset of biological control is having invasive organisms, that then people bring natural enemies, so these predators are herbivores, or parasitoids, parasites, from the native range of that invasive organism and release them. And so that's the context that you're talking about I think. So then that biological control agent itself is invading a new environment.
And so yeah, it's fascinating. They're amazing systems to study because otherwise, it's like, you don't get to introduce something into an entirely new continent, right? That's pretty unethical. I'd like to say that with modern biological control today, these things are studied really carefully. And they have, especially for weeds, they have very narrow host ranges that, surprisingly to me, seem not to evolve. The worry would be that you would release something into a new environment to control one thing, and then it explodes and starts feeding on other things or doing damage in other areas. So that would be the worry. And it really doesn't happen, which kind of blows my mind as an evolutionary biologist, because I feel like everything can evolve, and evolution can be rapid. Yet even when, so some of the things that I've studied to know if that kind of thing is happening is when two different biological closely-related herbivores are introduced to control a weed, and they hybridize, there's going to be an explosion of genetic variation in that population. So my thought is, oh my gosh, this is a perfect situation for them to start eating other plants, non-target plants. And in two cases, I've studied this in detail and two completely different biological control systems. And their host range just doesn't change. It just doesn't change. Some call these highly specialized herbivorous insects, just kind of evolutionary dead ends, in terms of what the cues they use to find a host, their ability to detoxify the compounds that the host has for defenses, it's such a complex system that it just seems to not shift easily. I mean, clearly it does over millions of years, but it's not something that is rapidly evolving in these specialized insects. You can see rapid evolution of host use in generalist insects, in more generalist insects. There's great examples of rapid evolution of host use generalist insects, but these specialized insects just seem like they just can't change.
The other thing, I personally have never released a biological control agent, as an ecologist and evolutionary biologist that seems like "wow, that's a big responsibility." I very much respect my colleagues who are doing the research on host range. And the folks in the USDA and Fish and Wildlife Service and Tribal Nations, who evaluate all those data and say: "Yes, we think that this is safe enough to release. The benefits that could have far outweigh the costs of not doing something or trying to use only chemical controls or whatever." So biological control, nonetheless, it has a bad reputation. People say things like: "But what about the cane toad?" And it's like at the time that cane toads were released, supposedly to feed on insects that were pests in sugarcane. There were also people, Europeans coming to North America and doing things like let's introduce all of the birds that Shakespeare ever mentioned.
Marty Martin 48:36
I've heard something about that. Yeah.
Ruth Hufbauer 48:39
Yeah, people were doing some wacky stuff. And some people said that oh, this is like this ferret is going to control some rat or something. But people were moving vertebrates around in crazy ways, and that is not biological control. So I just want to say what was happening that is not biocontrol.
Cameron Ghalambor 49:01
Yeah. You know, I can recall, there was a it's, I guess, kind of dated now, but there was a time paper by Dan Simberloff, several years ago, where he took a very dim view of biological control. And my take on that paper was that most cases of biological control resulted in lots of collateral damage that, you know, it was not intended. Do you feel like, if you when you look back on that paper that did a fair job of characterizing like, what currently is going on in terms of the more careful study and standards that maybe have changed relative to like, you know, if you go back and you review the whole literature, maybe if you're including original cases that, you know, had a much lower threshold or standard for what they would be willing to release as a biocontrol?
Ruth Hufbauer 49:54
Yeah, it's been a while since I've read that paper. I would say that two things one, biological control of insect pests has been much less rigorously controlled, and overseen, and regulated than biological control of weeds. And that is, it's a cultural thing. In the US, and in many other places, where basically insects are seen as pests. Like who wants insects around? I do. But 50 years ago, people like, you know, you had something in your house, you crushed it, you didn't put it out, gently put it outside. So there's that, and so things were released that okay, yeah, this generalist predator is gonna feed on other aphids as well, and not just these pests, aphids, but who cares, they're all aphids, we want to get rid of all of them. There was a kind of cultural agreement, that those things were pests, whether they were in our, you know, cropping systems or not. And then also, because insects are little arthropods are little packets of protein. Whereas plants are packets of complex chemicals defending themselves. The packets of protein, all sorts of things can attack them, there are some very specific predators and parasites, called parasitoids, of insects, but it's hard to find them. It's harder to find them than it is to find it more generalist one.
And so I think a lot of what Simberloff was talking about is biological control of insects. And I think some of those critiques especially from like you were saying, Cameron, that longer term perspective where people felt like, you know, insects are bad, let's get rid of them. That there's valid critique there, I do think that there's a tendency to not consider the other alternatives. There are pros and cons everywhere, you know, if we don't control a pest, what happens? That's a valid approach to decide that this thing is not going to be controlled, and so we're not going to have this tree or this crop grown in this area, and that's a choice. Because this pest is going to demolish those trees are make that crop untenable to produce. Or we use insecticides to control these things. And there are pros and cons there as well. Insecticides can be incredibly powerful tools and can cause cancer in humans, and they're very difficult to keep in the place we want them to be, and they get into the water systems. And you know, there's all sorts of problems there. But it's also a valid choice, or there's biological control. And if that can be done safely with something that's host specific, then it's often a good choice. But it's like it's one of those kind of three main classes. And I think that completely discounting it, the way Simberloff does, is short sighted.
Cameron Ghalambor 52:49
Yeah, that's an interesting point, it sort of makes me also kind of wonder about the ecology of a lot of these invasive species and their introduced range relative to their ancestral ranges that they were originally native to, and just how challenging of a question it becomes to sort of also figure out like, well, what does regulate the populations in the native range? Even for, for a lot of things, you know, we struggle to figure that out. And so, but, you know, I totally agree with your point that, you know, these are really big options that we have to weigh the pros and cons of and big decisions, and they're not, it's not black and white. There's a lot of gray area there too. So it's good to think about those things.
Marty Martin 53:41
Yeah, yeah, that's an interesting take on the Simberloff paper. I never heard it framed that way that, you know, the decisions that were made historically, and therefore, the way that he would write that paper, you know, might not resonate with what we've learned in the time since and the way that we approach biological control now.
Okay, so you know, when we not we because I don't do it, but when you come up with a plan for biological control, presumably one of the stages is going to be you know, you're collecting the organisms from wherever they are in the world, then you're breeding them to make enough of them to do the introduction. That has to mean some period of time when they're in completely foreign conditions, right? Before they go from native to new, right? There's a lag, there's a breeding effect. How do you account for that? And like, couldn't genetic load accumulate in those kinds of contexts? I mean, what's the current standard and what would be the best practice if we could afford it?
Ruth Hufbauer 54:35
Yeah, that is an outstanding question. Yes, there's definitely a reduction in genetic variation and potentially build up in genetic load as natural enemies pass through quarantine. So what happens is, so let's go to weed biocontrol, because that's what I know best. Organisms will be found, herbivores will be found in the native range. They'll be brought to a common garden, also typically in the native range, sometimes in a quarantine facility, where they're tested against a whole range of different plants to see what is their host range. Say everything looks great, and they are petitioned to be released. And that group that I mentioned before, like USDA, Wildlife, Tribal Nations approves it, then you go back to the native range, and you collect individuals, pass them through one generation in quarantine to try to remove any possible parasites or pathogens they might have. And then release them. So you try to have that part be very short. But sometimes that ends up being several generations to do what you were just saying, Marty, of building up the population size. Yeah, gotta grow enough of them.
Marty Martin 55:52
You gotta grow enough of them, right. So after you've done the validation, that they're only going to focus on the weeds that you want to control, or something close to that, then you bring them in to clean them with parasites, do you bring in individuals from different parts of the native range? I think in one of your papers, you emphasize that that would be pretty cool, if that could be done. And it makes sense for the reasons we've been talking about. But is it common practice?
Ruth Hufbauer 56:15
It is not common practice, at this point. All of the host range testing has to happen for each population. And because that can be like 10 years of work of a scientist's time and their whole team, it often doesn't happen. It used to happen. But we are justifiably concerned with, you know, what if these populations differ in their host range? And that is, that's why I did those experiments to say, oh, you know, once upon a time people introduced these different things. And now they're outcrossing with each other, is that changing their host range? And so far, I found like, no, it's not. Their host range is not changing.
Cameron Ghalambor 56:53
So one kind of related question that I was going to ask Ruth is, is sort of the interaction between the underlying genetic variation in the population, population size, and then the kind of demography. So like, from the evolutionary side, the capacity for populations to grow, seems to be associated with also the opportunity to adapt and evolve. And so a lot of these cases of rapid evolution often occur when populations are released from like, any kind of density dependent effect. And so they can, they can take off very quickly. But then on from the sort of more ecology side, the small populations also can potentially be limited by what we call like Allee effects, where the capacity for growth is limited, because you just have like a small number of individuals, you know, maybe hard for them to find each other to mate with. And so in like, either the the natural systems that you work on, or in the experimental systems, do you ever see that sort of ecological Allee effect, for example, and the genetic variation side with the small populations kind of in conflict with each other? Or where like one constrains the other? Or does it even play out in any of these studies in any meaningful way?
Ruth Hufbauer 58:19
I think it can, for sure. So one thing with the Tribolium system, since they're obligately, sexual reproducers. With small populations with very small numbers of individuals, you can easily have, all males or all females, and no reproduction whatsoever. So even with an experimental population, when they're in little experimental cages, and finding each other is not a problem, which is often, Allee effects in nature, is often they don't find each other like you mentioned. Just the sex ratio variation can lead to some propagule, some groups of founders not being able to establish a population. Interestingly, I did in one experiment, see an interaction between that and the genetic diversity of the population. So with founder size, and genetic diversity interacting such that low genetic diversity and low founder size was extremely bad. You know, so maybe the sex ratio wasn't quite all females or all males. It was, you know, one female and then some males and diverse populations were able to establish in those situations and ones experiencing high genetic load, the low diversity populations, were not.
Marty Martin 59:45
What do you know about assortative mating in the beetles? Are they choosy, or as long as the male or female is there, they'll take the chance?
Ruth Hufbauer 59:53
They mate multiply, so they're not super choosy. And they can meet multiply very rapidly as well. But they are choosy. So I haven't done this research, but others have and given related individuals and unrelated individuals, they will mate with unrelated individuals. So there's something some kind of relative avoidance and inbreeding avoidance. And I don't know that literature super well,
Marty Martin 1:00:19
Gotcha. Okay. It's another one of those challenging dimensions. It's not just finding a mate. It's how picky you are once you've found one. Yeah.
Cameron Ghalambor 1:00:25
So Ruth, I have one last question that I'm curious to get your opinion on. Obviously, when we look around the globe at one of the main threats to biodiversity is the movement either naturally or by humans of invasive species. And this has consequences, obviously, for both native populations and biodiversity, but also like for agriculture, and things like that, given sort of what you've learned about these experimental systems, and the kind of combinations of the right cocktail that you need, in order for something to really take off, do you get the impression that like, there's lots of organisms that are being spread all the time, but most of the time, they just don't take off because of things like, by chance, it just happens to be all males, or some demographic stochastic event happens, and just, you know, the population gets knocked out? Is that really common, but we only see this nonrandom subset of cases where the populations do end up taking off and they're detected, and then, you know, we recognize that as a problem? But below that, you know, there's all these like natural experiments potentially, that are happening all the time. Is that a fair assessment of what might be going on? Or is it really just, you know, most cases, the invaders are successful?
Ruth Hufbauer 1:01:50
There's the idea that one in every ten introductions establishes, and one in every ten of those is able to start to spread and one of it in every ten of those is able to start to invade. And at the very beginning of that, you know, maybe one in every ten of those survives transport. So there's not a lot of data behind that idea, but I think it's pretty well accepted that it's unlikely that everything is able to make it. And there are so many introductions happening all the time that there must be lots of failed ones. What that proportion is, though, I don't know if it's one in ten at each of those stages.
Marty Martin 1:02:35
Well, Ruth, this has been fantastic. We always give guests a chance to mention anything that you want to say?Some topics, some research, recent discovery or something. What did we not give you the opportunity to talk about?
Ruth Hufbauer 1:02:50
Oh, this has been so much fun. It's a little bit like an oral exam.
Marty Martin 1:02:19
Sorry about that
Ruth Hufbauer 1:02:59
No, no, no, but mostly like a conversation among colleagues that is just a hoot. Yeah, so I've really appreciated it. And it amazes me that you all have read any of anything that I've written at all, and that think any of these issues are important. One thing that we didn't talk about a lot is the flip side of range expansion: range limits. And more about kind of the expansion dynamics and genetic load at the expansion front. But I think there are lots of other folks working on that you can interview some of them.
Cameron Ghalambor 1:03:36
Okay. Good. Well, thank you so much for taking time out of your schedule to talk to us. We really appreciate it.
Marty Martin 1:03:42
Yeah, thanks.
Ruth Hufbauer 1:03:44
I really appreciate it too. Thank you so much. This has been such a pleasure.
Marty Martin 1:03:59
Thanks for listening. If you like what you hear, let us know via X, Facebook, Instagram, or just leave a review wherever you get your podcasts. And if you don't, we'd love to know that too. Write to us at info at bigbiology.org
Cameron Ghalambor 1:04:09
Thanks to Steve Lane who manages the website, and Molly Magid for producing the episode.
Marty Martin 1:04:14
Thanks also to Dayna De La Cruz for her amazing social media work. And Keating Shahmehri who produces the fantastic cover art.
Cameron Ghalambor 1:04:20
Thanks to the College of Public Health at the University of South Florida and the National Science Foundation for support.
Marty Martin 1:04:26
Music on the episode is from Paddington Bear and Tieren Costello.