Pheromones

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Hello. In 1959, scientists discovered pheromones, the chemical signals that make so many animals act without thinking or needing to think. Ants marching in a line follow pheromones. Queen bees keep their status in the hive with them. They're the instant code word for bees to swarm, to attack or flee, and are the great unconscious signal of sexual attraction across so many species.

Insects, fish and mammals use them to advance the cause of their own species. As for humans, that's debatable, as we'll hear. With me to discuss pheromones are Tristram Wyatt, Senior Research Fellow at the Department of Zoology at the University of Oxford. Jane Hurst, William Prescott Professor of Animal Science at the University of Liverpool, and Frances Rutniak, Professor of Apiculture and Head of the Laboratory of Apiculture and Social Insects at the University of Sussex.

What were the first inklings that there was something that could be called pheromones? Well, we've probably known about signals between animals right from the beginning of hunting. And they are accounts of the ancient Greeks knowing about the way that dogs attracted each other by smell, not by the bark. Charles Darwin, in his book, Descent of Man and Sexual Selection, writes...

During the season of love, a musky odour is emitted by the glands of the crocodile and pervades their haunt. And he described smelly ducks, smelly elephants, smelly goats. But the problem was... Quantities were so small they couldn't be identified with the chemistry of the time. And so how did it develop? That was an observation, but that didn't start research. When did research into it begin?

Well, the serious research started in the 1940s and 50s, and it was a German chemist who'd already been awarded the Nobel Prize for his work on the structure of hormones. And he spent about 20 years trying to identify the sex pheromone of the silk moth. And he made the breakthrough, which was...

Since you couldn't see the molecule, he used the response of the males. They would flutter their wings when they detected the pheromone, and that way he could track the pheromone as he made lots of extractions. He then isolated the molecule from half a million silk moths, identified it, synthesised it, and then the next crucial thing was, using that bioassay, he went back to the male moths and said, have I got this female sex pheromone right?

And they said yes. It took 20 years and half a million. This is a staggering figure for someone to concentrate on something that seemed obviously so very elusive and difficult. What instruments did he have? What did he use? How did he set about it? Well, basically he was using the behavioural response of the moths as his bioassay, as his indicator. Incidentally, somebody in the next-door lab, Peter Carlson, a biochemist...

was living in an apartment next to an early electrophysiologist, Dietrich Schneider. And in 1953, he suggested to Schneider, well, why don't you try recording with your new electrodes from the... moth antenna. So long before the molecule was actually identified in 59, Schneider started making electroantennograms and that basically means using the antenna as the instrument and...

All these sensory hairs get really excited. They fire off when they detect the pheromone. And so he was using the antenna as a detector. But that was too late for the...

real chemical identification. That was done just using the fluttering bioassay. Could you give our listeners a succinct and unforgettable definition of a pheromone? It's invisible chemical signals between members of the same species. Well, that does it. Thank you very much. Frances, Frances, why are the pyramids so important to insect colonists? Well, the animals, the insects live in colonies like honeybees and ants. Probably of all the animals, they use pheromones the most.

They use them not just in the case of, say, the silk moth, so that the female can attract a male. Indeed, the honeybee does have such a pheromone so that the queen bee can attract the drone bees on a mating flight.

They do, but they do a whole lot of other stuff with their pheromones. For example, honeybees use pheromones to help in the regulation of foraging the regulation of reproduction to organize their defense when their colony is attacked to help bees who got lost find their way back to the hive entrance there's just so many things

that they use pheromones for, honeybees have about 20 different communication signals to coordinate the thousands of workers in the colony. And more than half of those communication signals are... pheromones and actually new ones are kind of being discovered I wouldn't say all the time but on a fairly regular basis we're discovering new communication signals in honeybees and the same kind of applies to

Ants as well, they use a wide range of pheromones. I think the social insects, they are the sort of prime beneficiaries, if you like, of pheromones. So this is just a particular smell that comes out of a chemical action.

The pheromones. Well, the pheromones say that the honeybees produce, yes, they're all chemicals, all the pheromones we talk about. So this is just released into the air and they're picked up by those they're intended to be picked up by mates or the rest of the... colony or whatever it is some of the pheromones indeed are released into the air but certainly not all of them the queen pheromone for example in the context of mating yes the male bees do detect it in the air

but the primary way it's detected is by touching or licking the queen and also passing it around the colony but some of the pheromones are passed in the air so the alarm pheromone of the honey-bee if you were to be so foolish as to go to a bee colony and disturb the hive. And one of the bees at the entrance, one of the guard bees, if you molested it, it might well sting you. And that would be one sting, and many people wouldn't like that. But the stinger itself will release a pheromone.

and that pheromone smells of bananas and it wafts through the air very quickly because it's very volatile and then other bees will come out of the hive and continue the attack so what started as one sting might be many So the advice is pull out the sting as fast as possible? Well, it's probably too late by then. You should pull it out, but I think you'll be slower than the bee's response.

So that's a sort of defence mechanism that they're using it for. Yes, in this case, the pheromone is used in the organisation of the defence of the colony. And if you think about it, a social insect colony like a honeybee hive... does have something to defend. Whereas if it was a solitary insect, it would maybe fight for its own life or flee for its own life, but it wouldn't really have anything that it would need to do to call up support.

Whereas the insect colony, say a honeybee colony, has got a treasure of food inside of it. You know, tens of kilograms of young bees, honey. Many predators would love to get in and plunder that. And equally, they've got thousands of bees to mount a defence. So you can be stung by a thousand honeybees, especially the so-called killer bees from Africa. And so they can mount a pretty decent defence. Just to flip back a few centuries...

The interest in bees has been constant in classical literature right through it in Shakespeare. Were people noticing these things in their own ways of expressing them rather than the ways you could express them as chemicals and so on? Pliny the Elder, he knew a lot about honeybees. Aristotle, not everything Aristotle said was correct.

But because honeybees produce honey and beeswax, which is so important to people, there was a huge amount of interest in bees. But if we come only to roughly 16, 20 or 30, a British person, Charles Butler... wrote a book called The Feminine Monarchy. He was actually, the first 30 years of his life was the time of Queen Elizabeth, so maybe he had female monarchs on his mind. But he made some observations.

If a bee stings you, what he referred is to the rank odour. In fact, I don't think it's a rank odour. It's of bananas. The alarm pheromone of the honeybee smells of bananas. I wouldn't call that a rank odour. And then he said it would... cause an attack which would be like hail and so I think he had a particularly nasty beehive so that was well

1620s, so that's nearly 400 years ago people were talking about things which we now know to be pheromones. And you've told us how quickly they can react together. Jane Hurst, what is it about mammals that make them less likely?

Do you use pheromones? Well, mammals actually find scent cues really important, and scent cues are used in... most aspects of their biology and behaviour. But the sort of pheromone cues that Francis has just been talking about, the sort of classical pheromone, is not just a signal between...

between two animals of the same species. It's a signal that will normally produce a sort of stereotyped response, a very reliable response. And those sorts of responses that Francis has just been talking about, you can reiterate those responses. is just by producing this pheromone Q. Now, mammals are a little bit more complicated than that. They've evolved large brains and they are able to process and store an awful lot of information and learn.

from their previous experiences. And that's so that they can adjust their behaviour according to the information they've learnt before and any information that they've gained about other individuals in their environment and the relationships they've...

built up. So when we start to think about pheromonal responses, which are just sort of fairly simple responses, reliable responses to a particular cue, doesn't really fit in with that idea of adjustable behaviour, where animals can respond very differently according to what they've learned about. And indeed, there's been quite a lot of...

about whether really mammals use pheromones much at all to regulate their behaviour. And some scientists have said they don't believe mammals use pheromones that actually have these very reliable... effects on behaviour. However, we have now identified some sort of classic pheromones that are used by mammals, and we're starting to understand how those pheromones can be used in the much more flexible behavioural system of mammals. Including us.

Possibly. I think perhaps we'll get to that later. It's probably easier to start by thinking about some rather simpler situations in mammals, and in particular situations perhaps where mammals haven't had an opportunity to learn, such as newborn animals. to be able to find milk. if they're going to survive. And one of the first really clear examples of a mammalian pheromone is the rabbit mammary pheromone, which was identified by Benoit Charles and Gerard Coureau and their group in France.

and it's a small aldehyde which female rabbits produce in their milk. And they were able to show that by synthesising this one little aldehyde, and they presented it to newborn rabbit kits. And they actually did this by putting the aldehyde on the end of a glass rod and held it in front of the nose.

the pups. What happens then is you see this very stereotype response, which is the pups start rapidly searching around with their noses and start grasping and try to grasp hold of what essentially should be a nipple. And it's a response that is just stimulated by this very, very simple...

and is essential for these pups to be able to feed very efficiently off their mother. Particularly important in rabbits, because rabbit mothers actually only visit the nest for a few minutes each day, and the pups have to... grab hold of the nipple and get as much milk as they can from the female before she disappears again. So you need a very, very efficient response. And, of course, they haven't had very much time to learn how to do that.

So that's the beginning. Would you say that's a simple example and there are more complex ones that you could produce? It's a simple example, but actually it gets a little bit more complicated because the other interesting thing they discovered about that pheromone is that the pheromone actually induces the pups to learn.

and they learn other cues that are associated with the pheromone. So when they're exposed to the pheromone, if they're also exposed to another odour, they learn to respond to that odour in the same way.

So initially they wouldn't respond, say, to just the general odour of their mother. But once they've associated the odour of their mother with this milk pheromone, then now when they encounter that... odour they'll start to show the same kind of searching behaviour and in fact if you watch a female rabbit going into her nest you see the whole nest erupting with these baby rabbits starting to search really rapidly and try and get hold of the nipples as quickly as they can.

Thank you. Tristram White, what role have these pheromones played in evolution or evolution in pheromones? Could you give us a dissertation on that? So... One of the surprising things is that almost any kind of molecule can become a pheromone. So we've heard about some small molecules, these volatile alarm pheromones and that volatile rabbit mammary pheromone. Underwater...

the pheromone molecules can be huge. They can be proteins, so long as they're soluble. So in different habitats, in different places, different kinds of molecules evolve to be pheromones. in some cases we can have a feeling, an understanding of how molecules that are just around, as it were, just leaking out, can evolve into pheromones. So...

Goldfish pheromones were discovered by accident. Scientists in Canada were studying hormones in goldfish and the water was flowing from one tank into the next. When the upstream tank had female goldfish that were getting hormone treatments, the male goldfish downstream got very excited and started producing lots of sperm.

And it turned out that the goldfish pheromones were based, were like the hormones that were coursing in the blood of the female goldfish. So the female sex pheromones were based on the hormones. And what Peter Sorensen and Norm Stacey hypothesise is that way back in evolutionary time, males that responded quickly... was sensitive to these molecules, which were basically just cues in the environment, would reach the female first. There'd be selection of the generations for greater...

and greater sensitivity but also specificity so they didn't have false alarms. So that starts as eavesdropping but it's to the female's advantage to attract a male to be there to deliver sperm when she spawns. So it turns into a signal when females evolve to produce these molecules as a signal, as a pheromone. So that's one of the ways that pheromones can evolve.

Is there an evolutionary history there? Is what you said at the end of some development or halfway through some port of development, is it still developing? I'm using the word develop, mutating, whatever you'll find a better word. Pheromones can certainly evolve. They're used in pest control, and we'll hear about that later. Well, not necessarily, so you can tell us now. OK, so one of the strange things is that the first New York State entomologist in the 1880s...

anticipated that pheromones would be powerful. So he watched male moths flying into his window and people were gathering on the sidewalk. And he hypothesized in the 1880s that if only we could synthesize these molecules, we could perhaps use their power to control insect pests, which were a big thing in North America. Fast forward to the first pheromones being identified in Germany.

Rapidly, people started identifying the molecules and trying them out in the field. And if you release enough of these synthetic pheromones, the males can't find the females. They don't fertilise the females. Without fertile eggs, no caterpillars, crops protected. And most of the apples we buy today have had some pheromone protection. And so that's one example of evolution. And that's evolution, but that's manipulated evolution. Now...

That's manipulated evolution and what we might expect if pheromones work like pesticides that we get resistance. And so far we haven't had any resistance. So is this a good thing? A very good thing. and particularly because the pheromones are used in relatively small quantities because the moths don't need very much to be confused, and because...

They don't affect predators. We leave intact all the spiders and the predatory beetles. So you can have organic farming that works really well. Thank you. Francis, what's the queen substance and why is that important?

Well, the queen substance is... And we're back to bees. Yes, we're talking about honeybees. The queen substance is perhaps the only pheromone which has a common name that, you know, man in the street or woman in the street might have heard of. So before it was, if you like, chemically discovered, people knew that there was something going on. So a British scientist, another butler actually, but this time Colin Butler.

he hypothesized that the queens were making a certain material which he called queen substance and without knowing what it was he set out to learn about it and it's known to beekeepers that if you take the queen out of a colony very quickly within a few hours and certainly within half a day or a day the worker bees know that the queen is absent and they set about

maybe trying to find the queen, but what they do and what Butler used to study the queen's substance was that they'll start making a new queen. And this can be observed because what they do is they take a larva

a female larva in a worker cell. These are these famous hexagonal cells everybody knows about. And then they would try to... if you like promote a few larvae into queens and to do that they have to feed the larvae with royal jelly and they also modify the cell making it looking like an acorn cup.

Just a second, they're acting like you lot, aren't they? They're acting like scientists. They're doing an experiment on this bee to change the bee. They're doing Frankenstein. I mean, for somebody like me who knows nothing about it, it's amazing. So they haven't got a queen bee. They want another. They pick up something. You're going to be the next queen bee. And then they take things from other bees and inject.

Project? Penetrate? How do they get them in this other bee so it turns into a queen bee? Well, fairly simply, Melvin, they feed the larvae. Oh, they force feed them? No, they don't force feed them. Honeybee larvae actually... float in their food so it's a bit like being in a bath of food and the honeybee larva is floating in its bath of food secreted by the worker bees so they're kind of lying in bee milk

And if you want to become a queen, you have to be lying in the special bee milk we call royal jelly. Anyway, this construction of these queen cells or queen cups was the bioassay that Colin Butler used. So he could... basically study the queen's substance. He didn't know what it was and one of the experiments he did for example was to put a queen in a cage so the worker bees couldn't touch her.

but the air could pass over. And if he did that, the worker bees felt as though they didn't have a queen. So he knew, therefore, that the queen's substance was not volatile. Tristan. Well, I wanted to pick up on the royal jelly, which was mentioned by the two scientists who coined the word pheromone in 1959. So one of them was a termite biologist, the other was a biochemist, Peter Carlson.

But they consulted widely, including writing to Colin Butler about the Queen's substance. But they anticipated that there might be some different kinds of pheromones that would actually act by mouth. So most of the pheromones we've been talking about so far are detected by the nose, whether in the mouse or the antennae of a bee or a moth. There are other pheromones which are ingested and act directly on tissues in the developing bee larvae in this case, and those are called allo-hormone.

There's a bit of debate about whether we should include them, but in the sense that they're released by one animal, the nurse bee, and given to another and have an effect.

they actually count as a pheromone. So it's a particular kind of pheromone that acts not on the normal sense organs, but actually acts directly on the tissues. Jane Hurst, can we switch to mice? Okay. How do they deal with, how do they use pheromones?

Well, it's kind of quite interesting, really, because you might think that, you know, having had the example of the rabbits, it's an obvious example. The pups need to find mother's milk and they haven't had any experience. They use a pheromone. But actually, when people looked at mice, it turns out not.

to be the case. And in the case of mice actually the pups imprint on the maternal odour, the individual odour of their own mother and they find the nipples by following the odour of their own mother. So when they're actually born, the mother cleans them off and that stimulation of the pups stimulates the pups to learn the mother's odour. And they'll learn the odour of the mother's saliva and they're also...

learn the odour of the amniotic sac that they've been sitting in. And then the mother distributes that odour on her nipples, and that's what the pups will respond to. But if you give them the odour of another mother, they don't respond to that.

Here we have a social animal, and I think the big difference here is that in the case of rabbits, individual females have different nests. The pups only need to recognise their own mother. They can use a simple pheromone. In the case of the mice, mice are social and there are other...

mice using the nest. So it's very likely that this imprinting on their own mother allows them to get to their own mother's milk and of course we see that sort of response in many other mammals where it's very much an individual specific response. There have been most of the pheromones that have been actually identified in mice, these things which don't depend on which individual produces it, but it's a generalised response. They're mostly involved in what we call reproductive priming pheromones.

So these are odours that will change the hormonal status of an animal, usually to make it more or less likely to mate. And we do know of quite a few of those pheromones. But actually recently we have... We have discovered another pheromone in mice that really does have an effect on their behaviour. And it's a pheromone that we've called Darsin.

You're plundering Jane Austen there. Yes. You'd better explain this to the listeners. I think I'm being too clever by half. I read it in your thing and that's where I got it. Right. So, well, the thing with mice is that

They might use sort of fairly simple pheromones in the sort of context of reproduction. But when it comes down to mate choice, that's very much more an individual specific response. And females are really choosy in who they choose to mate with. And what males will do is that they will... will scent mark their territories with a lot of scent marks that they...

stuffed full with little proteins which actually advertise their own individual identity. So each male produces his own little pattern of proteins. These proteins are called MUPS or major urinary proteins. and they're trying to advertise to females who they are. And they will compete with other males. If other males come and try and also deposit scent marks, they will...

countermark that male scent marks and try and drive them out of their territory. So they're really kind of communicating to females, not just I'm male, but I'm this male. This is the male that you should mate with. Well, females are quite interested in these ODQs, but they don't really find them very attractive. So they will investigate them, but they don't actually find them more attractive than, say, an individual signature from a female.

That is until they actually contact the male scent. And when they contact the male scent, they detect another little protein pheromone. It's another... But it has a slightly different sequence from the others. And unlike the individual specificity of the signatures that the males are producing, this is a protein which all males produce. And this protein females find really attractive.

And we've sequenced the protein. If we just give the female that protein, they're really, really attracted to it. But the really interesting thing with this protein is that it doesn't just attract them on its own. It's another one of these proteins that is...

super potent in stimulating learning in the females. And the moment they have a sniff of that protein, they learn the individual odour cue of the male that's associated with it, and now they find that individual male's odour really attractive.

And that's called the Darsin protein? That's called the Darsin protein, yes. And you sat around a table and decided that this protein would be named after Darsin. We've got to come to a conclusion on this. So, actually, well, not so much a table. I have to say we sat with a glass of... We sat with a bottle of... wine and my husband and collaborator on this he's a protein biochemist also at liverpool and he said that you could name a protein anything you liked but usually it has the suffix in

on the NIN. And there'd been a couple of other examples. There's a protein pheromone that newts use, which they emit when they're... courting females to attract them. And that's been called Sodeferin, which is actually after the Japanese... Do you mind me saying, could you tell us about Darcy and then we can move on? I probably have a bit of a red pheromone in there.

So Darcy and Wee named after Jane Austen's romantic hero, Mr Darcy, in Pride and Prejudice. And it was really inspired by the first line of the book, which I'm sure you know. It's a truth universally acknowledged that a single man in possession of a good fortune must be in want of a wife. Well, of course, a good fortune isn't particularly important to a female mouse, but it does appear that a single male mouse in possession of Darsin must be in want of a mate. Great.

Can we talk about the context in which they usually talk about the chemistry? We've talked about the literature. What about the context? It matters a lot. One of the interesting things about insect pheromones... is that it was often assumed that this was a completely stereotypical response and males would always respond in the same way, or for that matter, females in those situations.

But it's actually much more subtle. And in the same way as in mammals, context is everything in certain cases. So, for example, turnip moth males... get very excited by the female sex pheromone, but once they've mated, they turn off for 24 hours. Now, if you record from the antenna, that electroantennogram again... The antenna are receiving the signal, but in the brain...

the response is switched off. It's context-dependent. And the reason for that is when he mates with a female, he's going to give a whole lot of proteins along with the sperm, and it takes him 24 hours to produce them. And so he shouldn't respond. until he's got them ready. Also in moths, the male moth, when he's flying to the female at night, is in danger of being eaten by bats.

So they try and leave it as long as possible, but then they do have to fly to find the female if they're going to mate. But their willingness to fly depends on whether or not they've heard bats calling, and so they'll fly faster if they have. and they'll sometimes even shut it down. So lots of things are, even in insects, context-dependent. Francis, can we talk about ants? How do they deploy them when they're out and about and moving as they seem to be doing incessantly?

Well, one of the commonest things you can see is ants following a trail. And what ants do, say an ant finds some food. On the way back to the nest, it may lay a pheromone trail by either dragging its sting or dotting its abdomen to lay a chemical trail. And back in the ant colony, it will then sort of stimulate other ants to go foraging and they will be able to follow this pheromone trail to the food. So that's actually something that honeybees don't do. And ants have...

a huge repertoire of trail pheromones. And in our own work, for example, we discovered in one pestant, which lives in Britain, that they really have three trail pheromones. One is very short lived, only lasts for minutes. another one which is much longer lived and to detect that one the ants actually have to not smell if you like but taste they have to touch the substrate with their antennae because it's less volatile presumably.

And the third one, maybe the most interesting of all, one of my former students now at York University, Elva Robinson, she discovered a no-entry pheromone. So this is not saying... come this way but don't come this way because ant trails frequently have branches in them so it's not just a matter of going to the right branch.

it can also be important to be told, don't enter this particular branch. So there's a great deal of sophistication going on in ant colonies and their pheromone trails. And of course, as everybody knows,

you have a picnic or you spill some food, and the next thing, there's ants all over the place. Jane Hurst. How have animals adapted to detect pheromones using something more than a sense of smell? Ah, OK. So as humans, of course, we do think of the sense of smell as being scents that you can detect, the airborne scents that you detect when you breathe them into your nose.

what we call the main olfactory epithelium, which is at the back of the nose. But actually most other mammals, reptiles and amphibia, have evolved another... olfactory system. It's called the vomeronasal organ. And this is a separate system. Unfortunately, humans

don't have it. So we really don't know quite what it's like to sniff something through the vomeronasal organ. Humans don't have it, great apes don't, and old-world monkeys don't have this, at least not a functioning... system as far as we can tell.

But this is a rather different system. So the way that our main olfactory system works is that the receptors are quite broadly tuned. It allows us to detect a whole range of different sorts of odours, not just scents, but all the odours in your environment. Whereas the vomera nasal... organ, the receptors there are tuned very finely to detect only a single chemical. So each receptor detects one particular chemical and those will be chemicals which have particular biological significance to that.

So those could be pheromones, which are important for communication within species, but they could also be molecules from other species. So, for example, predators evolve receptors for key molecules from their prey and vice versa. So this is a very specialised system, and it was at one time thought that all pheromones would be detected through this vomeronasal system. But we do know now that some volatile airborne...

can be detected through the main olfactory system. Thank you, Tristram. How do some animals use this to deceive? So... If you rely on chemicals, then you can have illegal signalers. And there's a fabulous story about bolus spiders in North America. The female web spider... in this case, puts her web into a sticky ball at the end of a long thread. So it looks like a bolus, just like the gauchos in South America.

She synthesises, as it were illegally, she counterfeits the female sex pheromone of moths. Male moths fly upwind at night. and she detects when they come close by the vibrations as they fly, and she then throws her ball, the bolas, catches the male moth and draws it in. It gets... Weirder. At different times of night, she releases different counterfeit blends, so that way she can pretend to be the female moth and lure them in like a siren. It's extraordinary, isn't it?

And you have pictures. Can you photograph this? Patiently, yes. So there's a biologist called Ken Haynes at the University of Kentucky who's got some wonderful photographs of this. There are other examples where families of beetle larvae group together, pretend to be a bee, and they produce the smell of a female solitary bee. The male tries to mate with this apparently a female bee. They jump on and then they jump off when he actually does find a real female. You're trying to come in.

you can go to YouTube and see a video of the Bolas spider, and I think none other than David Attenborough introducing it. And indeed, I show that to my students in one of my animal behaviour lectures. But we also have the reverse.

case where in going back to honeybees there's a honeybee species living in asia very similar to our western honeybee and it has a really important predator the giant hornet and the giant hornet has a pheromone so if one giant hornet finds a honey bee nest to plunder it releases a pheromone which attracts more giant hornets its nest mates to the attack of the victim colony now what the honey bees do is they also detect this pheromone

and they then mount a very specialised anti-hornet defence, and they try and capture the hornet, surround it with a ball of bees, and cook it to death. And we call that a chyromone. Just a second, just a second. I'd like to know more about that place.

I mean, Captain, I'm going to cook it at us, right. You've seen that again and again, it's news to me, so it'd be lovely to know more about it. You haven't been watching enough television, you've probably been too much on the radio, but again, you can see good videos on this. Well, the giant hornet is... Very, very armoured animal, and the honeybee stings just can't penetrate it. But the honeybees form a dense ball of maybe 500 worker bees around the hornet.

they raise their temperature and they literally cook the hornet to death because the honeybees can sustain and stand a higher temperature than the hornet. But the point is the honeybees get warning of the hornet. by eavesdropping on the horn its own communication to its nest mates. And there are a few other cases where that happens where a pheromone of a predator is detected by the prey who then can mount a special defence.

Jane Hurst, which ways do males and females respond to the same phenomenon, the same pheromones in mammals? So typically, of course, males and females are going to respond differently to any kind of sex pheromone. They have very different meanings and they need to show different types of responses. So I guess traditionally we sort of thought, oh, a pheromone has a specific response. It's evolved to have that response and then all other animals...

are going to respond to it will respond in that way. But actually that's not the case when you start looking at different types of individuals. So if we look, for example, at Darsin, Darsin has evolved as a signal to females, to attract females to the male. And of course, males are not passive in this. When males detect Darsin...

from other males, it makes them highly competitive. So Darsin will stimulate a competitive counter-marking response and it actually stimulates aggression against the sender. Now, of course, it wouldn't be appropriate to really think of that as an aggression phenomenon.

because it's not likely that a male will have evolved a pheromone that causes other males to attack it. However, it has evolved as a pheromone to attract females and so the appropriate response from males, if you like, they're eavesdropping in the... same way that we've just been talking about species eavesdropping on the sense of other species, in this case males are eavesdropping on the signals that other males are producing to attract females and responding to that in a very competitive way.

And it's a race to the... It's a race... It's competitive... Competition sets in. It is very much a big stimulus for competition. But actually, even within the same sex, we can see different responses to the same pheromone according to the state of the animal. So, for example, while Darcyn attracts...

females that don't have offspring, if they're lactating and a male comes in expressing Darsin, females will attack it if they're not familiar with it. Can we come back to humans, Tristram? We said we had...

Now, let's say humans have pheromones, but we're too complicated, busy or occupied to make any use of them. Is that all we have to say about it? No, it's an ever interesting story. Our sense of smell is very good. We're very good smellers. The problem is there's a lot of bad science concerning human pheromones. I'm persuaded that we probably do have them.

But if you search for pheromones on the internet, you'll get lots of sites offering you pheromones for sale. They tend to be some steroid molecules. They're basically made up. The same group, though, that has been working on... Rabbit pheromones in France is also working on a possible human pheromone. So the sex pheromones, we probably might have them, but none properly identified.

But this group in France is looking at something different, and this is a potential mammary pheromone. And it looks as though baby humans, human babies, respond to secretions from the nipple. around the nipple of lactating mothers, these Montgomery or areola glands, the little bumps around the nipple. And it looks as though secretion from any mother will cause any baby to respond.

And that, I think, may be the first human pheromone to be identified. The things on the internet, they could have a placebo effect, but they're not real. Can you just say a little bit more about the things on the internet? These are advertisements... Empower your sex life by using pheromones. They promise to make you irresistible. I see. And I guess if you... Darsin again. Indeed, if only we had a Darsin. Although, well, humans can do things in other ways. Jane.

Yes, there is quite a big difference actually in the way that mammals like mice are using these pheromones. Because I guess if we take the... idea of a classic pheromone this is a signal that will produce a very reliable stereotype response and that's generally not what mammals want to do and the way that mice are using this pheromone is to actually have choice

whether they're exposed to the pheromone or not. I think that's a very important thing about the vomeronasal system because in order to detect something in the vomeronasal system, animals have to actively deliver the scent.

to the system whereas if you detect something in your main olfactory system you're exposed to it simply if you just breathe air into your nose and I think that's potentially a reason why it would actually be quite hard to think of a sexual attraction pheromone working in humans because actually most people don't want to be just attracted to every person of the opposite sex that they meet they need to have some kind of a choice they're using a lot more information to to make those choices

Do you think that you're at the beginning of research in this area, Francis? In the case of pheromones, the honeybee situation... Maybe 50 years ago, they thought they understood it. I'd say today, you know, we are learning so much and there's so much new stuff coming in. There are so many pheromones. How do they work together?

We still, in many ways, are still at the beginning. Well, thank you very much for that. That was terrific. Thank you. Thank you, Francis. Right next, Tristan Wyatt and Jane Hurst. And next week, it's... Antara ibn Shaddad and the poetry of the Arabian Peninsula before Islam. Thank you 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.

This program is called In Our Time, and Colin Butler, the discoverer, one of the main people in the discovery of Honeybee Queen's substance, well... He only died three years ago. And I think that shows you that it's all pretty recent. And another element of the recency is that in the time of Butenant and the discovery of the silk moth, he used half a ton of moths.

Now, chemistry has evolved to such a degree that one moth would be more than sufficient. Maybe just a glass full of air around the female moth might be enough. So the chemistry has really helped. the study of pheromones a great deal, the much more sophisticated analytical chemistry we now have. Because Budden didn't have the gas chromatography and the mass spectrometry that modern chemists have, and that has revolutionised the whole field. It's funny, chemistry held things back.

It's another example of how science moves by new techniques being developed and suddenly you can do new things. We actually got very close with observations back in the 1870s. there was a French entomologist, naturalist really, Jean-Henri Fabre, and he was another of these people describing male moths flying in through the window. And...

He went through this logical series of experiments. So he tried covering up the female under a gauze. The males still found her. He took the cotton wool that she'd been resting on. The males flew to the cotton wool. And he's moving towards the idea that it's probably smell. So he tries covering her under a glass. The males are not interested. So he concludes that it must be smell. And then he makes the fatal error. He assumes that...

Any smell that is important for sex is something that we can smell. So he sniffs the female moths. And he can't smell anything, so he rules it out. And what he forgets, of course, is the male moths are exquisitely sensitive to those molecules. Now, if he'd only... made the right conclusion, it would have brought things forward, but we still would have had to wait for half a million salt moths.

And I think actually that's also been the case in terms of mammalian pheromones, because we've always assumed that there are these volatile molecules that we can smell. And it's turned out that an awful lot of these pheromones are... proteins. Of course, humans can't smell proteins at all. And you can only detect these when they're actually delivered to this special vomeronasal system. And I think actually while we...

also need the chemical techniques. The other really important thing in these areas is having a really good bioassay and having a bioassay that actually measures realistic behaviour. And I think that's probably the best way. that we're going forward now in understanding the much more sophisticated effects that these pheromones are having.

And that's actually, of course, the thing that's holding back the study of human pheromones. The nice thing about the work on babies and the potential mammary pheromone is they have a nice bioassay, which is the baby turning its head... puckering its lips, even sticking out its tongue in response to the potential molecules. When we come to sex pheromones in humans, it's really hard. There are so many cultural things.

And trying to get those kind of experiments through an ethics committee don't even start. So it's going to be very hard to get good bioassays, and that's another thing which has held back all the work on human sex experiments, if indeed they exist. Do you have anything to offer on that? I was going to say to Jane, maybe you could tell us what the ideal experiment would be for a human sex attraction.

I was only joking, really. But it might be a fun thing to think about. I'm assuming we can get permission. Well, I think one of the things that I really noticed the difference in the human literature, I think there are two things. First, that many...

people working with human pheromones have a very different definition of pheromones to those of us who work with animals. And I think this idea of a pheromone that stimulates a very specific response is a really good one because actually we can see this. time and time again in animals, whereas a lot of people working with human pheromones would accept any kind of response, even if it's a learned response, if it's just something that arises through cultural... responses.

And I think the thing we particularly have to look for in humans are those situations where it's a really reliable response. Because when you see responses to the purported pheromones that have been tested, you know, some people respond to it, some people don't. well actually if we test any of these pheromones on my mice I can guarantee you

they will respond. And I think that's the whole point about pheromones. It's a reliable response. It's a signal that's evolved to really produce this type of response to the advantage of both signal and receiver. And so if we're going to try and look for human pheromones...

I think we have to be very clear about what kind of response we would expect to see so we know what we're trying to measure and we should expect, if it's a pheromonal response, to see that response really reliable, shown by people. We're also rather fixated, a bit like the advertisements for deodorants for young men, on long-distance attraction.

If humans did have sex pheromones, they might occur at a much later stage in courtship, perhaps in really quite intimate situations. And so it's going to be very interesting indeed. So they wouldn't work in a crowded pub at 11 o'clock at night on a Friday then?

No, I think we're safe. Not really, Melvin. I suppose if everybody had the pheromone, it would all cancel out, wouldn't it? You know, we'd all be back to square one. Well, the alcohol would interfere with the pheromone, perhaps. Oh, would it? Probably not. Well, thank you all very much. That was really enjoyable. Thank you. How would you respond to an offer of tea or coffee? Tea, please. Coffee, please. Black tea, wheat, please. In Our Time with Melvyn Bragg is produced by Simon Tillotson.

Hi there. I'm sort of sorry to interrupt, but not that sorry. It's Jane Garvey here. And I just wanted to make absolutely certain that you'd heard about Woman's Hour. It's a programme about women, but it's for everyone. We've got loads of fantastic guests like Malala. My university friends would not call me a role model. Okay, well, I'm actually rather encouraged to hear that. Thought-provoking conversations.

The term clean eating gives off the narrative that if you don't eat that way, then you're dirty and you're eating dirty food. And we mark big moments for women around the world. A hundred years to the very day, women in this country could vote for the very first time. A round of applause from all of you, please. A ripple of excitement. Please join in. Subscribe to Woman's Hour on BBC Sounds.

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