In Our Time - Behavioural Ecology

Episode Date: December 11, 2014

Melvyn Bragg and guests discuss Behavioural Ecology, the scientific study of animal behaviour.What factors influence where and what an animal chooses to eat? Why do some animals mate for life whilst others are promiscuous? Behavioural ecologists approach questions like these using Darwin's theory of natural selection, along with ideas drawn from game theory and the economics of consumer choice.Scientists had always been interested in why animals behave as they do, but before behavioural ecology this area of zoology never got much beyond a collection of interesting anecdotes. Behavioural ecology gave researchers techniques for constructing rigorous mathematical models of how animals act under different circumstances, and for predicting how they will react if circumstances change. Behavioural ecology emerged as a branch of zoology in the second half of the 20th century and proponents say it revolutionized our understanding of animals in their environments.GUESTSSteve Jones, Emeritus Professor of Genetics at University College LondonRebecca Kilner, Professor of Evolutionary Biology at the University of CambridgeJohn Krebs, Principal of Jesus College at the University of OxfordProducer: Luke Mulhall.

This BBC podcast is supported by ads outside the UK. Thank you for downloading this episode of In Our Time. For more details about in our time and for our terms of use, please go to BBC.co.com.uk slash radio four. I hope you enjoy the programme. Hello. What factors influence where and what an animal chooses to eat? Why do some animals make for life while others are promiscuous? Why do some species invest a lot of energy in producing a few offspring

while others produce young regularly throughout their lives. These are the kinds of questions asking behavioural ecology, the part of zoology concerned with the study of animal behavioural ecology developed in the second half of the 20th century, is a combination of Darwin's theory of natural selection, along with ideas drawn from game theory and the economics of consumer choice. Scientists had always been interested in why animals behave as they do, but before behavioural ecology, this area of science never got much beyond a collection of interesting anecdotes. Behavioral ecology gave them techniques for constructing rigorous mathematical models

of how animals act under different circumstances and predicting how they will react if circumstances change. Proponents say it revolutionized our understanding of animals in their environments. With me to discuss behavioral ecology are Steve Jones, Emeritus Professor of Genetics at University College London, Rebecca Kilner, Professor of Evolutionary Biology at the University of Cambridge, and John Krebs, Principal of Jesus College and, Professor of Zoology at the University of Oxford.

Steve Jones, can you give us a summary of what behavioural ecology is and what the key ideas are? Well, you've just more than it's done my job for me, really. That summarises pretty well what it is. It's the scientific study of the interaction between animals and their environment in the widest sense. Their food, their predators, their prey, their mates, their offspring, all of which can be fitted into a fairly homogeneous way of thinking, often based on shared genes, often but not always based on shared genes. And that, as you say, that really did alter the nature of research into animal behavior,

because before that, it had been, to use your phrase again, a series of anecdotes without any explanatory power. It was called ethology. And the classic weakness summarized for me by a famous experiment done with birds, where you give a bird, an egg which is. three times the size of its normal egg. And the bird really likes that egg. Okay. Now, why should that be?

You can think of all reasons possibly. But the answer to an ethologist was, oh, they prefer big eggs. Now, that isn't an answer. I often think... Why isn't it an answer? Well, because they prefer what do you mean? They prefer. Why do they prefer big eggs? I often think that all biologists, I'm sure the three of us around this table,

have a guilty secret, which is they started as bird watchers. And I started as a bird watcher, and I filled up the little ticks in my book. and it never crossed my mind to ask why do ducks have very bright-colored males and the females are rather brown? Whereas swans, the sexes look just the same. Now that's an interesting question which we kind of know the answer to

and that's the kind of question that behavioural ecology asks. So ethology really was just St. John Orbury's diaries, really, was it? Yes, oddly enough, I mean, a slightly distant analogy. Ethology was a bit like modern genetics where you find the gene for something

and then you stopped. You've only just started. So I think, you know, the ship from ethology to behavioural ecology I think has a much wider lesson for biology as a whole. You've got to ask interesting questions, not just make interesting observations. Given the fact that the three of you were fanatical birdwatchers and we've had fanatical birdwatches for centuries,

why did it take so long to get to the idea that there could be a scientific framework of explanation for this? Well, that's a good question. I mean, people did ask why do barnacle geese disappear at certain times a year? And the answer was they turn into barnacles. Now, that wasn't a good answer, but it was a good question. We know that's not true. I'm not sure we yet know exactly why some birds migrate and some don't.

But I'm interested in the wonderful patterns in the sky that we see with starlings and so. Was that always thought, was that again always anecdotal? or they're doing it because of X rather than can we work out why they're doing according to the principles of Y? I remember being told in school that those big flocks of Skarlings were called murmurations.

Why they're called murmurations, but that was the answer. Oh, look, there's a murmuration of Starlings. It has to do, if I remember rightly, to do with foraging, finding patches of food and hunting as a group when food is patchy.

I'm not murmuring to each other, come along, we'll move along the way. That we don't yet know. It's possible, isn't it? Rebecca Kulner, can you tell us about Tinbergen's four questions when they came in and why they were important? So I think Timbergen's four questions were essential in moving the study of animal behaviour

beyond the kind of anecdote that Steve's just been talking about. And that's coupled with the idea that behaviour can be a trait like an organ to which natural selection can be subjected and therefore can evolve and can be an adaptation. these two ideas were generally essential for the development of behavioural ecology. Sorry to interrupt, but could you give us a date? Yes, 1963 was when Timbergen set out his four questions. And Timbergen was just a little bit. He was who, what?

Timbergen was one of the forefathers of the study of animal behaviour. He received the Nobel Prize for inventing the scientific study of animal behaviour in the 70s. And he worked in Holland initially and then he moved to work in Oxford later on in his career. Right, sorry, back to what he told us about. So he set out these four questions, which are four kinds of ways that we can start to begin to investigate animal behavior. So imagine we're looking at some animal expressing a behavior like a parent feeding chicks in the nest, for example. So we can ask four kinds of questions about that. First of all, we can ask a question of causation.

So what's the physiological basis of that behavior? What internally to do with its nervous system, its hormones and so on is guiding that behavior? Secondly, we can ask a question to do with development. So how is that behaviour refined during the course of an individual's lifetime, for example, what's the origin of that behaviour? And then we can also begin to ask a larger scale evolutionary questions of the behaviour. So we can say, to what extent does that behaviour owe its existence to the evolutionary history of the animal? So if we look at close relatives of this bird, do they exhibit similar kinds of behaviour

simply by virtue of sharing a common ancestor evolutionarily? And then the fourth question is really the one that gave rise to behavioural ecology. And this is a question of function. And the question really is, for what purpose has this behaviour evolved? How does it function to promote an animal's fitness? So you've got a grid. Well, you've got the square, anyway, the four points of the square, rectangle, it might be. Never mind.

But you take off with that last one. Why is it that that became the basis or the starting trigger for behavioural ecology? I think because of this insight that happened at the same time, which in fact Timbergen set out in this paper where he elaborated the four questions, which is that behaviour can be a trait that's an adaptation. So just like any other part of an animal's body or its organ systems, it is subject to natural selection and it has evolved for a purpose to promote, in Timbergen's terms, the survival value of that animal.

So does this come into work being done by Richard Dawkins, the selfish gene and so on. Right. So the big question, if you set out the question, what is the fitness value of a behaviour, then you have to define what you mean by fitness. And so at that time there's a considerable debate about precisely what scientists meant when they talked about the fitness of a trait.

And one set of people, led by Wyn Edwards, believe that you measure fitness by looking at groups. So traits exist for the good of the group or for the species. Timbergen didn't believe this at all and neither did David Lack which is another ecologist working in Oxford at the same time and they instead believe that the purpose of traits

was to promote individual fitness but then in 1963 there was quite a revolution because this man called Bill Hamilton changed completely the way in which we think about the fitness of individuals and he said that not only... When you're saying fitness I'm meaning fit to survive Well, this is what I'm going to explain to you. But he said that we can measure the fitness of an individual

by looking at the number of offspring it produces, but we should also look at the number of offspring that that individual helps to produce in its relatives. So we're no longer looking at counting offspring, the accounting system for fitness now focuses on genes, genes that are shared by individuals and genes that are shared by their relatives. So this brings us to the selfish gene idea

of thinking about behaviour because what it suggests is that natural selection favours genes who promote their self-interest by being passed on to the next generation and that can be achieved either by being represented in descendant offspring or by being represented in the offspring of relatives.

And that became, obviously that became very important and because of Richard Dawkins' abilities, a worldwide conversational point of change. That's right. So the unit of selection became moved from the group to the individual to the gene. Can we go on from there, John Krebs? Another important step. And you were there with Dawkins, with them at the whole,

and the beginning of six or three or four of you bringing this on. But the idea of innateness came up. Can you tell us how it came up and why it's so important? Yes. Going back to what Steve said at the beginning about ethology before the birth of behavioural ecology in the, I suppose, early 70s through to the late 70s. Timbergen and Conrad Lawrence,

who shared the Nobel Prize with Timbergen in 1973, had tried to build a theoretical structure for interpreting animal behavior. But it turned out their theoretical structure was wrong. So in a way, a house of cards had been built and then knocked down, and that created a bare landscape in which behavioral ecology was able to rebuild

a theoretical framework. But one of the planks of the Timbergen-Lorent's view was that there are two kinds of behaviour. There are behaviours that are innate or instinctive, and there are behaviours that are learned. And what had struck Timbergen and Lawrence as naturalists is when you go out and watch animals in the wild or look at them in captivity,

some kinds of behaviour just appear spontaneously in young animals without any practice, without any teaching, without any learning. And that's what they called innate behaviour or instinctive behaviour. And in fact, Tim Bergen's 1951 book was called The Study of, of instinct. Now this turned out to be a false dichotomy because when you look at it in detail, no behaviour appears without any environmental experience or influence whatsoever. So the concept of purely innate and purely learned turned out to be a blur. Some things are more dependent on environmental influence, learning, other forms of experience. Some things are less dependent.

When it's less dependent, does that necessarily mean it's innate? Does it not have any value anymore? It doesn't have any value. What Tim Bergen and Lawrence were trying to argue was that things appear, certain behaviors appear spontaneously without any environmental influence whatsoever. There had any form of learning, however broadly defined. And that was really torn apart by, particularly by an American psychologist called Danny Learman in the 1950s. And there was a ding-dong battle throughout the 1950s between the Timberg and Lawrence view and the American psychologist Learman's view and essentially Learman won. So we all now recognize that while genes may create a propensity to behave in a certain way, that propensity doesn't mean to say that the outcome is immutable, is independent of any environmental experience. So we've moved on from this sharp dichotomy between innate behavior on the one hand learned on the other

to say everything depends on a mixture of genes and environment. And the question is what is the mix and what is the balance between genetic influence and environmental influence? So it's the idea of the selfish gene and the critique. give inateness, they come together to make the scientific platform for behavioural ecology? In some degree, yes, and very often what Richard Dawkins said in the selfish gene is misinterpreted. If you read some of the writings and people talk about, let's say, a gene for altruism or a gene for mating, that doesn't mean literally that if you have a particular genetic makeup, you will automatically perform a particular behaviour. that's saying is that the differences between individuals are influenced by differences in their genes.

That's a separate argument from the argument of how does the behavior develop in the life of the individual. So this question of innateness has really become secondary to the discussion about that Rebecca's already talked about how natural selection operates to promote certain kinds of behaviours and not others. Is it still an area determining the effect of particular genes if they can be described as such? Is it still an area that's being explored? There's a lot of work on the development of behaviour which teases apart in

very wonderful and beautiful detail how genetic influences and environmental influencers come together to produce the emerging behaviour in the adult. So if you ask, for example, how does a chaffinch come to sing in the way it does,

that's a very complicated mixture between an inborn genetic template in the brain, which is passed on from father to son and a set of experiences Because only male sing in birds But it could be passed also from mother to son, you're right So that inborn template interacts in a very complicated and sophisticated way

with learning experience during the Chaffinch's first year of life And that sort of research is a very thriving and rich area of research but it's very different from the simple description, either it's innate or it's learned. Steve Jones, game theory came into the equation of behavioural ecology. Can you tell us in what way and why it came in? Well, it's, you know, every biologist has got a certain sense of shame that they can't do maths, okay,

and game theory was a way of getting around that in some ways, in that the game theory, the theory of games, she's been around for almost 100 years now, has to do with... It's basically playing poker against nature. If you're playing poker against somebody, you know that there is a set of cards which are distributed in some way around the table.

And you're all competing in order to get the most advantageous set at the end. And to do that, you need to infer what the other person has likely to have and how the other person is likely to behave. And the better you can infer that, the more likely you are to try and put the expense of the other person. There's a certain amount of random noise in this system, of course.

But game theory applies that kind of logic to, for example, fights between males over females. When should you, as a male fighting for a female over a piece of territory, say, when should you give up? Is it worth going on until death, which sometimes happens, or should you realize early in the game, I'm going to lose this one, I'm going to stop here, and I'm going to run away and fight on another day?

When you're a male, for example, trying to monopolise a group of females, which happens in many creatures, what should you do? Should you spend all your time fighting off your rivals, which allows some of your rivals to use the technical language to sneak in and do some mating, or should you balance the need to fight off rivals with the need to mate with the females? And all this is the province of game theory. And what it's done, knowledge to the work of John Maynard Smith, who was actually at university college, London, not the University of Oxford for many years, was to formalise vague ideas about playing games against nature, which is really what behavioural ecology is.

Can you give us Rebecca, Rebecca Hillen, an example of how behavioural ecology changed the way as well, just analysed animal behaviour? Yes, so I'd like to draw an example which comes from some of the work that I do, which is the field of parent-offspring conflict. So before behavioural ecology, if we looked at interactions between parents and their young, then all seemed harmonious. The parents' interests and the offspring's interests were perfectly aligned,

and the parent and offspring cooperated during provisioning, bounce of provisioning at the nest, for example. But what behavioural ecology has done is to show that actually all is not as harmonious as we might at first suppose, and there is an underlying evolutionary conflict of interest between the parent and the offspring. And that seems at first sight to be ridiculous, because how can a parent possibly be in conflict with its own fitness? But the concept really nicely illustrates how thinking about problems at the level of the gene can yield entirely different insights about how we think about it. So let's imagine, for example, a parent feeding her chicks at the nest. So she's collecting food and she's bringing food to the nest to feed her young.

Now, every time she hands over food, she gains some small fitness benefit by provisioning her. young because they're going to be more successful as a result of receiving high levels of food. But she pays a small price for doing that. And that price comes also in terms of fitness. So she'll lose the ability to breed again in the future, for example, or have a lower chance of survival. So the parent has to opt-in- Why does she lose that by feeding her chicks? Because she's put a lot of energy into collecting food and not consumed it herself, but handed it over to her offspring. So she has to play this balancing game of,

weighing up the costs of collecting food against the benefits of feeding her offspring. And natural selection is a wonderful optimising agent, so it selects the optimal balance between the two so that the parent derives maximum fitness benefits for the costs. Now the thing is that the optimal solution from the parents' point of view is quite different from the optimal solution from the offspring's point of view. And the reason for that is because they're not perfectly, genetically identical. So the offspring are not genetic clones of the parent because there's been

sexual reproduction. So they only have, say, on average, half their genes in common with their mother. So that means that the offspring are much more interested in their own fitness than in the mother's fitness. And so they are under selection to demand food, more food than the mother is under selection to supply. So their optimal level of provisioning exceeds the optimal level of provisioning from the mother's point of view. So there's a tension between them. The offspring would like the mother to bring more food to the nest than the mother is herself under selection to supply. So there's actually a conflict of interest there, evolutionarily speaking, that would not be apparent had we not used the behavioural ecology approach to thinking about this sort of a problem.

Because of what we thought there's a congruence of interest. And yet if a bird has eight chicks and can only really feed two, the other six chicks are neglected or heaved out of the nest. That's right, but it's not in the interest of those six chicks to lay down their lives necessarily on behalf of their siblings. They should try and acquire food for themselves up to some point against the interests of their mother. Yeah, but all I'm just trying to say,

that the idea that the mother is responsible for every chick and that there's this genetic compulsion that every, every person bred by her is equally looked after doesn't obtain? That's true, and it might not obtain because the mother may decide secondarily that she doesn't wish to rear all the chicks that she's produced, and so that's a decision she takes that's in her evolutionary interests, or it might be because of a conflict of interest with her offspring, where offspring are not prepared to be shunted out of the nest in the interests of the mother,

because they want to survive, even if the mother does not want them to. John Krebs, you've done a particular work applying the ideas of behavioural ecology to analyse foraging. Can you tell us about that? Well, I can tell you a rather cruel summary of my work in Private Eye about 15 years ago, which when I was appointed as head of the Food Standards Agency and Private Eye did a little piece about who is this guy. And they said, well, Krebs went to the University of British Columbia in the early 1970s and met a brilliant young student called Rick Charnoff. between them they hatched the idea of optimal foraging theory, which explains that animals go to feed where the food is. So that's the harsh description of optimal foraging theory.

But when I started out as a young postdoc, and this reflects in a way what Steve was saying earlier on, I was struck by the fact that there wasn't really a coherent theoretical framework for trying to interpret the behavior of animals in their natural environment. and I haven't been interested in how animals exploit food in their environment, and really the science of that was very descriptive. So I wanted to ask the question, could we construct a set of mathematical models that we could use to predict precisely how animals move around in their environment, how they choose to go to one place rather than another, which kind of food items they eat? And I was fortunate in meeting this chap Rick Charnoff, who was a graduate student

when I was at the University of British Columbia, and he and I together worked out, when I say he and I together, I mean really he did, and I put my name on the paper, worked out a theory. It was based on microeconomics, the economics of consumer choice. So we basically grabbed ideas from economics

and plugged them into animal behavior. And let me give you a concrete example. So imagine you are an animal that goes to a place where there's maybe a pond, where you feed on fish and there's some fish in the pond. And you start hunting for the fish, and after a while you begin to deplete the fish in the pond, so it gets harder and harder to find the next fish. And there comes a point at which it would, in quotes, be better, close quotes, for your food intake,

to leave that pond and go somewhere else. But, of course, leaving to go somewhere else is not cost-free because you've got to travel to get to the somewhere else, and you don't know quite what the somewhere else is going to be like when you get there. So can you formalize that as a mathematical, relationship and say at what point should the fish hunting animal leave pond A to search out pond B, C or D. And that's what we did. And we stole the ideas, quite frankly, it's a good piece of plagiarism. We stole the ideas from microeconomics. It's called the marginal value theorem. And we were able to apply that economic model, mathematical model, both in field situations and

in laboratory experiments. And miraculously, it did seem to explain. explained what animals did. So we were completely triumphant. I can remember writing to Rick, in those days he didn't have email. This was a sent him an email letter, which I still got a copy of because he sent him back to me eventually, which I said, here are the results from our experiment, read them and weep, because they were so unbelievable. We could actually explain, predict, quantitatively, what animals would do when searching for food. So that was the idea. It turned out later on to be much more complicated, but at least in those heady days, of the late 1970s and early 1980s,

we were martyrs of the universe and we could actually explain and predict what annals would do in their natural environment, which we found quite extraordinary. Steve, Steve Jones. I mean, I think that's, of course, true, but it's a very powerful means of exploration, this way of thought.

For example, let's think of something like a disease organism, let's say HIV, the AIDS virus, okay. Now, that's foraging for prey, where the prey. so it has to alter its behavior insofar as viruses behave to ensure that it has a chance to move on to the next prey once it's depleted the resources of the first prey. Now since the epidemic began, when there was, for a time, confined to homosexuals,

there was a lot of promiscuity, people weren't aware of this, and the virus was extremely lethal. In the last five to ten years, it's got much less lethal because people are aware of the dangers, people are much more careful about their behaviour. So the virus can't afford just to take the maximum out of its first victim,

in the sure and certain knowledge it's going to get another one. It has to be kinder to its victims. So here we see exactly that analogy of hunting behaviour in birds seen in a medical context. So it is actually quite a powerful way of thinking. Can we move to the analysis of mating strategies here? What can you tell us about that, Steve? I can tell you a great deal about that.

I mean, as I say, I'm a geneticist, that my job is to make sex boring, and I'm an expert at it. And in fact, perhaps the least interesting part of sex is the first part. But anyway, we shall talk about that. Well, mating strategies, actually, the logic of mating strategy came from, guess who, Charles Darwin, and he came out with a lovely note in a letter.

Whenever I see a feather in a peacock's tail, I feel sick. Now, I have to say Darwin felt sick much of the time, but that's a separate issue. And it was a very sensible thing to say. But why should a male peacock have this enormous train, which clearly doesn't help it to fly and presumably makes it attractive to predators, whereas the female doesn't? And Darwin thought a bit, and he realized, I don't think he used quite this analogy, but he realized that natural selection,

the survival of the fittest, as it's rather loosely called, is in fact like the driving test. It's a two-stage exam. First of all, you have to stay alive, okay? And I passed that because when I walked into the studio, I was alive, right, and still am. But then the more difficult, the practical test, you have to have children, okay,

and I fail that because I don't have any children. So my genes are extinct, okay? Now, if you look at it that way, the interests of males and females, very different because in principle a male can fertilize in most creatures vast numbers of females as is often famously said. Every time

a man has sex he has produces enough sperm to fertilize every woman in Europe so there's the potential for an enormous variation in male mating success and if you go out and look into the wild you see that's often true even in humans that have been

cases Mullah Ismail the Cruel of Morocco claimed to have had 777 children So males, therefore, really have to persuade females that they are the male who is the best. And that's why we get these very expensive and pricey things like the peacock's tail, or even red colorations, and many of these colors are very expensive to make. And the female, the simple version of the argument, will choose the male who can afford the most expensive decoration because he, the argument goes, probably has the best genes.

And so we have this sexual conflict and this great difference in appearance between. males and females. Sorry, yes. Just to pick up on that, I mean, it's also true that in the animal kingdom as a whole, there's a great variation in mating patterns. Some species are, for example, largely monogamous, some are highly promiscuous, and behavioural ecology has begun to shed light on why you get those differences in the pattern of pair bonding. And I suppose the general principle, the way of looking at is if it takes two parents to successfully raise offspring, if one parent can't do it on its own, because of the kind of food supply they require or the way they have to defend the babies against

predators, then you tend to get pressure for monogamy for a pair bond that lasts during the period of raising offspring. But if that's not a pressure that one parent can raise the offspring on their own, it usually, as Steve has implied, ends up being the female who holds the babies and not the male. But there are some cases where that's reversed and there are some cases in which males rear the offspring and females are the ones with the flashy displays that go around choosing who to mate with. Rebecca Kulner, that takes us to the relationship between parents and their offspring. Could you develop what John Krebs has said? In terms of mating systems.

In terms of the relationship between them, is it always the case that the woman is left with, that the man goes, is there any always? We're looking for theories here and general. rules. No, it's not always the case that the lady's left holding the babies. So, for example, in many fish species, it's the male that undertakes parental care and not the female. So there's huge variation across species

in patterns of care. You can have bi-parental care, male-only care, female-only care, or no care at all. So are there any predominating patterns coming out of this? Well, yes. So one way of looking at how

to analyse this problem is to consider what the costs and benefits of parental care are and also what opportunities exist for parents to mate with other individuals should they abandon the offspring. So if there's no, for example, if we consider a situation where we have two fish jointly raising young together, there's no point in the male abandoning the female

to raise the offspring if he can't then gain mating success with another female if there are no other females available. And some very nice experiments have shown that if you experimentally manipulate the availability of mates, and so increase the number of free females available, you can cause males to abandon their existing family to go off in search of other mating opportunities. And so create a situation where instead of having bi-parental care

and both parents looking after the offspring, the female only is left looking after the offspring. But the same is also true you can increase the number of males available and tip the balance the other way. So these sorts of ecological factors can determine the pattern of parental care that we see naturally. John Crabs, you've done some work on animal communication. Can you tell us how that fits in? Yes. In a way, it links back to what Steve is saying about the peacock's tale.

When I learned about ethology and animal communication as an undergraduate, I was taught by Nico Timbergen. His storyline was that communication is essentially a cooperative enterprise. I am the signaller, and I produce a signal, a sound or a visual signal or a signal, You are the receiver and our interests in the transmission of the information are unified. So I want to get the message across. You want to hear the message or attend to the message. Now, as Steve has already said in relation to mating strategies, that actually is far too simplistic. And Richard Dawkins and I wrote a paper in the late 1970s in which we turned the whole notion on its head.

We said communication in the animal kingdom is not. a cooperative venture where the signal and the receiver have the same interests. In fact, far from it. What communication is is a form of manipulation. Rather like marketing and advertising, you know, why we're all persuaded to buy toothpaste. It's not because the toothpaste seller is trying to convey a genuinely true message to us. They're trying to persuade us to do something. And in the same way, the peacock is trying to persuade the female to mate with him, and the female is resistant to that persuasion. So there's a sort of arms race, if you like, between persuasive signaling and resistant listeners or resistant receivers of the signal.

And Richard and I argued that was a general feature of animal communication. And you could reinterpret all that Timberg and Lawrence and the early naturalists had looked at in relation to how signals develop, how they evolve over time, in terms of manipulation and persuasion and resistance. So it's again, it comes back to taking a selfish gene view of the world, turns things on its head. and the same old things that you've looked at for years and years suddenly appear in a totally new light and you have new questions, new ways of interpreting and understanding.

Did behavioural... You want to say something? Can I ask a question when you can feed it into what you say, which is how did this new behavioural ecology affected views on cooperation? Well, I think in exactly the same, much the same way. These are opposite sides of the same kind. I mean, a classic example which brings that up, actually,

is something which, guess who Darwin wrote about, which was about orchids and plants in a relationship between flowers and insects. And it was thought in those happy days that there was a beautiful, loving relationship between the bee and the flower. From the flower's point of view, as is often said, the bee is a flying penis.

It takes the pollen to another plant. And often they're very closely tied to each other. One species of flower has one species of pollinator. But in fact, the interests of the two are quite different. the pollinator wants to be lazy and promiscuous, whereas the flower wants the pollinator to be active and faithful. And Darwin noticed something very odd, which is in orchids, many of which are very beautiful.

They attract particular moths, let's say, which are perfectly adapted to fertilise that orchid, and they'll put their promosies in and get some nectar out. And Darwin was completely baffled to find that in lots of orchids, they didn't get a reward. They'd go to a flower, and they'd stick their tongue in, and there'd be nothing there, but they still come back. And, of course, the orchid is cheating.

It's saying that this flower has got, it's beautiful, it's lovely, it's going to have some nice reward. There isn't a reward. There's just the minimum number of rewards. So the cooperation, what looks like cooperation, is in fact conflict. So basically, you know, in the end, I mean, the animal world is full of Mrs. Thatcher's. You know, it's an endless war against all. A wall against all. Locke was right.

Rebecca. Well, I'd like to change the perspective slightly and say that there are instances. of cooperation that exist within species. So, for example, there are cases in birds where there are helpers at the nest, and these are adult birds that forego reproduction themselves to assist parent birds in raising their young. So this is seemingly an evolutionary puzzle. Why are they forsaking their fitness to help others gain fitness? And here, behavioural ecology has provided a very nice answer, again through this gene-level thinking,

because frequently the individuals that help raise the young of other. are relatives of the birds that are breeding. And so they're not gaining offspring themselves, but they're doing the next best thing because they have a genetic stake in the offspring that are being reared. And so individuals can help promote their fitness indirectly by helping relatives to raise young. And that explains the puzzle of this apparent altruistic behaviour.

And of course the extreme example of that are the social insects like bees, where you look at a honeybee colony, the vast majority of honeybees that you see in the colony are females that never ever reproduce. So they are giving up their maiden arts that are giving up their whole lifetime to go out and collect nectar

to provision the hive to feed the eggs, the larvae that have been laid by one of their sisters who is the queen. So that's an extreme example of cooperation and altruism. Can we begin to apply some of these notions to human behaviour? John Krebs?

That's something that people have speculated on a lot, and I think we should not try to be too simplistic about this. I think if you take the view that us humans are a tabular raza in which our evolutionary heritage has no influence on our behavioral tendencies whatsoever, that's far too simplistic. I think to say that we've shed our evolutionary heritage is wrong. On the other hand, if you want to argue that we are driven by our genes to behave in certain ways,

and males are driven to be promiscuous and female to be promiscuous, that again is too simplistic because there are huge cultural overlays on our behaviour. So I would take the view that yes, evolutionary biology, behavioural ecology can help us to understand human behaviour but it's not the sole explanation.

There's actually a very nice follow-up to the cooperative breeding story in humans. So I think 45 different cultures were surveyed to look at patterns of reproductive success in these different cultures. and in each of these 45 difference in human societies across the world. And each of these studies revealed that there is a helper at the nest in human families and that helper is the grandmother.

So grandmothers are key to reproductive success in human societies and that their presence ensures greater survival of offspring than in cases where they are absent. and clearly they're related to their offspring. So this is another example of a kin-selected behaviour, which we can see parallels with in the animal world. But the predominating importance of kin, kinship has also been challenged, hasn't it, Steve Jones?

It has very much. I mean, I think the behavioural ecology view is a very useful view. I mean, for example, we heard about grandmothers there. That explains a rather puzzling observation about menopause in human females. What's the point of having a word? woman who can no longer reproduce. She is looking after her grandchildren. But I think

there's been too, I think most people would now agree there's been too much focus on the genes eye view. And ironically enough, what shot that in the foot was the development of techniques for paternity testing in particular. And what we find again and again is what had been assumed to be family groups,

cooperative groups of kin, not that at all. It's a thing called the superb fairy wren, which is an Australian bird, which had been beautiful story, a loving pair of duo looking after their chicks. But in fact if you do the paternity tests

it turns out that many of the young which this male is faithfully feeding are not its offspring at all. And that's true for many of these other cases where, for example, it was often thought that gangs of chimpanzees were kin. Do the DNA test? No, they're not. So I think

the idea that everything is driven by simple kinship is wrong. But like everything in biology, unlike in physics. It's not pure, it's not simple, but you're getting somewhere with it. What are the problems you're working on at the moment, John Crabs, about animal behaviour? Well, I personally am not very active in research now at the moment, but I think if I look at where the field is going, the field of behavioural ecology, I think what we've seen in the last decade or so is the development of a swath of new techniques, ranging from molecular techniques to understand, using DNA to understand the evolutionary history

and relationships between animal groups or plant groups, to satellite tracking of individuals using radio transmitters to other electronic techniques like microscopic cameras that you can fit onto animals. So you can see their eye view of the world as they move around. So these new techniques are opening up a whole new descriptive area of understanding of animal behaviour. And I think the question over the next few years will be, how do these new techniques change, if they do indeed change, the theoretical framework that was developed in the 1970s?

Rebecca Gellner. So I think these techniques are actually allowing us to start to address some of the three other questions that Tim Bergen raised, because there's now considerable interest in understanding, for example, why we see so much variation from individual to individual within a population in the particular behaviour that it's. it shows. And the answer to that kind of question lies in understanding the causation of the behaviour, whether individuals vary in their underlying physiology, for example, and also how

that behaviour develops. So, and we can get at those kinds of issues much more precisely now because of advances in genomic technology and in understanding nervous systems. So these kinds of questions are coming to the fore because that's the way technology is taking us. And equally, we can start to look at comparative questions so we can compare different species more effectively precisely because, as John said, we have the ability to construct accurate phylogenism, evolution-relatedness between species.

Thank you very much, Rebecca Killener, Steve Jones and John Krebs. Next week we'll be talking about truth in 20th century philosophy, and thanks for listening. And the In Our Time podcast gets some extra time now with a few minutes of bonus material from Melvin and his guests. Is there a feeling that you're just, just at the start of this, that it is

going to grow. No, I think the feeling is that we're at the end of it and the things, there are new vistas. I'm not, I'm not taking the Eeyer perspective. I think that the positive thing is that the field is expanding in new directions now. But the questions that behavioural ecology set out to address

originally have largely been answered and now we have to move on. And that's why I think there's just return to the interest in the other three questions that Timbergen has felt out. But also there are other ways of understanding the relationship between behaviour and evolution and whereas we've been interested in understanding

the evolution of behaviour, now we can look at how behaviour might drive evolution. Niche construction, as it's called. Yeah, that's one word. And again, what did Darwin do? Darwin invented it because he noted, his last book, 181, was about earthworms. It was actually the biggest bestseller of his life

was the Earthworm's book. Because Earthworms had been thought to be pests in gardens, bizarrely, but he pointed out that actually earthworms make the soil, they construct their own environment. And there's a beautiful natural experiment in that, because in New Zealand there were no earthworms, one or two very rare earthworms, and a very barren soil. Accidentally, earthworms got into New Zealand with the Europeans, and they began to construct their own habitat by chewing up the soil, and now New Zealand soil is much, much more

fertile than it was, which is good for the worms, and by chance also good for the New Zealanders. I think one thing that when people listen to this, they may form the erroneous impression that we think that animals have intentions and plans, you know, because we say the female aims to do X and the offspring is keen to do Y. But of course, that's simply a shorthand for saying natural selection has produced patterns of behaviour that. So there's no implication of intent here, but often when people talk about it, they give that impression. and those who are listening may not always spot the subtlety. Before you came along, your group, the gang of four in the early 60s, there was the idea that the thing was driven by drives, wasn't it? There was sex drive and hunger drive?

And you said that this was, was it Tinbergen who overthrew that? So a beautiful theory? Well, it's actually Robert Hind in Cambridge, who overthrew the drive notion. I said it was a beautiful theory destroyed by ugly facts. That was said about, no, stand by Spencer. Yes, yeah. But, yeah, that was, it was a wonderful construction,

and Tim Bergen's book, The Study of Instinct, had these kind of flow diagrams with big drives, feeding into little drives, and Lorant's thought of his like a laboratory system, you know, where energy driving behaviour is like the water building up in a system, and then you flush it out. And he was thinking of having had sex, of course, you know, so the energy builds up, and then you have sex,

and then you're exhausted. But he thought that was true for all behaviours, but that just didn't fit the facts. The irony is if you go to the basement of the London School of Economics, there's an enormous hydrodynamic model of the economy, where you pour in demand and a little bit of supply, and you squeeze down the valve, so you've got higher transport costs,

and you crank it all up, and you've got the model of the economy, which, like all models of economy, doesn't mean anything. We are going to be offered a cover of BBC tea or coffee. Thank you, Chris. Yes. This is Luke. There are many more Radio for Arts and Discs

programs to download for free. Find these on the website at BBC.co.uk slash radio four.