Speech 2009 by Prof. dr Marcel Dicke

This speech was given during the Dies Natalis ceremony in 2009: 'Body odour, behaviour and body building'.

Marcel Dicke

Body odour and body building

Nothing in biology makes sense except in the light of body odour. This paraphrase of the famous statement by Theodosius Dobzhansky is more than just a linguistic pun. Evolution and body odour are tightly linked. However, body odour is something that we, civilized citizens, do not appreciate. Humans spend large sums to mask their own body odour by applying the body odours of animals or plants in the form of perfume.

Darwin’s fantastic work shows that in evolution the basic words are natural varation, competition, natural selection and the maximization of fitness. Fitness is expressed in terms of body building. That is, in the sense of building new bodies that carry your genes. The body building that you see in the bottom of the slide is rather a component of sexual selection where individuals exhibit characteristics that should make them more attractive as a sexual partner. The building of new bodies represents Darwinian fitness. This concept guides modern biologists in their research approach.

Organisms vary in almost all characteristics. Although a large collection of beetles of one species vary in e.g. morphology (Figure 1), all individuals can successfully mate with each other. Figure 1 represents a part of the 600,000 insects in the insect collection of Wageningen University. Gazelles vary in speed. Some can run faster than others and this can make the difference between death and survival.

The world out there is a hard world where individuals need to make the right choices. If they don’t, this will lead to a lower reproduction than accomplished by their competitors, or even worse, to death. If all offspring of an individual would live to reproduce this would quickly lead to huge numbers within only a few generations. However, each offspring has to cope with competition, with finding sufficient food, and with enemies that try to use the individual for lunch. Not the fact that only few offspring are successful and live to form the next generation should surprise us but rather the fact that some offspring máke it at all and form the new generation. After all, there are so many hurdles to take and so many dangers to escape from.

In fact, every individual must not only be a jack of all trades but should master them all. It does not pay to be only good at finding a good food source. If this is combined with being an inferior competitor or with being inefficient at escaping from predators, then finding a good food source is of little use. An individual should be good at finding food, ánd at competing with competitors ánd at finding a mate ánd at producing offspring. That is what life is all about: building new bodies of the best quality: that is, producing viable offspring that can successfully produce grandchildren.

Sacrificing offspring to build bodies

However, sometimes the building of bodies goes at the expense of some of an individual’s offspring. Amazonian poison frogs produce their offspring in water bodies in the leaf axils of plants. A male guards several of these water bodies. He attracts a female to his territory and stimulates her to deposit her eggs in one of his pools. He fertilizes the eggs and takes care of the offspring. When needed, he transports his offspring on his back to a new pool. As the wet season comes to a close, the life time of the pools gets shorter due to evaporation and any tadpole that does not develop into an adult will be lost. So the offspring are faced with a time constraint to develop fast enough to be able to successfully metamorphose into an adult. To make sure that its offspring do not suffer from food shortage and consequently from a reduced developmental rate, their father supplies them with food. The food provided by the father can include younger tadpoles that will not make it to the adult stage anyway. Feeding them to their older brothers and sisters will make sure that they contribute to the reproductive success of their parents: they will be used to build the bodies of their brothers and sisters.

Information and body building

So, organisms face the formidable task of being allround champions that master finding food, escaping from their enemies, finding a mate, producing and raising offspring. But how can organisms master all these trades at the same time? They have to make so many decisions. About where to forage for food, where to go to avoid running into their enemies, where to go to find a mate, about the quality of a potential mate, and about how to make sure that mating results in offspring production as also mating is subject to competition. All these decisions should be well-based and so the organism should be well informed. Indeed, information is a valuable resource. Moreover, it is a special resource: one cannot eat information, information cannot kill you, but still information is essential for building bodies and, thus, for being evolutionarily successful. Information can exist in many forms such as visual cues, auditory cues, and chemical cues. Each kind of cue can be recognized with a separate sensory system. Olfaction and gustation are the most widely used sensory systems that perceive chemical cues. At least in insects, that comprise a large portion of global biodiversity. But certainly not exclusively in insects; chemical information is used by organisms ranging from microbes to mammals. I will come back to this later. Chemical cues allow an individual to be informed under many conditions. For instance, in the dark when visual cues are useless, over longer distances when visual cues have a low value, and also in time chemical cues remain detectable for a longer period. When you have visited a bar where smoking is allowed, your friends will still be able to tell that next morning. And the presence of some women can be traced by the perfume trails they leave behind.

Building bodies is essentially dependent on body odour. For instance, female Asian elephants produce a compound in their urine, (Z)-7-dodecenyl acetate. This compound serves as a sex pheromone that informs an elephant bull that the female is receptive. The elucidation of this compound as the sex pheromone of the Asian elephant was a surprise because the same compound is also used by moths as a sex pheromone component. More than 140 moth species use it. This finding is interesting for several reasons. First, it shows that mammals and moths both use chemicals for communication. Second, it shows that they share the same compound which illustrates a relatively independent evolution of the use of this compound. However, there is no risk that an elephant will mate with a moth. For one thing, the amounts emitted by a moth are so minute that an elephant will not notice them, while the very sensitive chemosensors of male moths do! For another, moths use this compound as one component of a pheromone mixture. Each of the 140 moth species has its own mixture based on the composition and relative quantities of the components. In this way different moth species can share pheromone compounds. Just like a perfume designer can make two different perfumes on the basis of overlapping ingredients.

Natural variation

Within a species not all individuals use exactly the same pheromone mixture. There is some variation in the pheromone blends that are used by different individuals. And if the different blends have different value to the female that produces it, or to the male that responds to it, selection will act on the producers and responders. Those individuals that produce a pheromone that results in building more bodies are more successful in an evolutionary sense. Within a moth species one may recognize different races that use different pheromone blends. For instance, two races of the European corn borer, a moth whose larvae feed in the stem of corn plants, are known. They produce very different sex pheromone blends: the maize race has a blend that is dominated by compound 1 and has a minor amount of compound 2 while the sex pheromone of the mugwort-hop race is dominated by compound 2 with only a minor contribution of compound 1. It is interesting that males of the two races prefer the pheromone of females of their own race.  Thus, the two races are behaviourally isolated and, similar to geographic isolation, this means that the races are genetically isolated groups which is a first step towards speciation. One may say that the two races have their own pheromone dialect and the resulting reproductive isolation will lead to the formation of subspecies and finally to the formation of species that can no longer engage in effective mating.

The world represents sex in many forms, ranging from flowers to dimorphic animals. Why sex is good has been a question that has been often posed but only in rare cases empirical proof has been provided. Yet, the fact that most animals and plants are sexual, means that discrimination between the sexes is a common phenomenon of life. Body odours play a role in many sexual interactions. Chemical communication is, therefore, a common way of communication. Similarly, speciation resulting from the use of chemical information has been recorded in a wide range of organisms, such as orchids that communicate with pollinating bees, snakes, fish, mice and many others.

Selective forces

Just like other characteristics the use of body odour has costs in addition to benefits. These costs and benefits and the strength of selection forces will determine the way that chemical information conveyance evolves.

The emission of body odour makes the emitter stand out. Just as with the tail of a peacock, the emission of odours may make it more difficult for the emitter to escape from enemies. For instance, the use of a sex pheromone by a female moth may have several costs. Apart from attracting potential males, the pheromone can also be exploited by parasitic wasps that parasitize the eggs of the moth (Figure 2). The wasp lays her eggs in the eggs of the moth and, consequently, these will not yield viable caterpillars. The embryo is killed and used as food by the wasp’s offspring. Moreover, there is a risk for responding males as well: some spiders are known to produce a close mimic of a moth’s sex pheromone. Males that are attracted to the pheromone mimic end up as lunch for the spider rather than as father of a new generation of moths. Thus, chemical communication is under selection to maximize the benefits and reduce the costs. It is common to see that sex pheromones are highly specific which makes it more difficult to mimic them and allows for discrimination among moth species. Moreover, the emission is done at low doses, which puts selection on the sensory system of conspecifics and natural enemies alike. Finally, the emission is restricted to certain times of the day and a restricted time window in the organism’s development. Taking a Darwinian perspective has yielded enormous progress in understanding the ecology of chemical communication.

In conclusion, nature is a big food web that represents who eats whom. And superimposed on this food web there is a body odour web that represents who perceives whom. Such food webs and body odour webs occur in the air, underground and in the water.

Putting potential fathers to the test

So far, I may have given you the impression that sexual communication is an activity of females, whether in elephants or in moths. This, however, is certainly not the case. There are ample examples of chemical sexual information that is disseminated by males. For an exciting example I will stick to butterflies, though. Danaid butterfly females do not mate with just any male they attract. The females are choosy and select the best fathers for their offspring. In this case, the father provides his sexual partner not only with sperm but also with a nuptial gift that constists of a plant toxin. This toxin is meant to cover the eggs and protect them from predators. The toxin is collected by the males by specifically feeding on plants that contain these toxins. For a female a male that was successful in collecting the toxin will be a good father for her offspring. To advertize that he was successful in collecting the toxin, the male uses a pheromone that he synthesizes with the toxin as substrate. If he can present the female, before mating, with this pheromone she will accept him as a sexual partner that provides her offspring with protection.

So, organisms are involved in an information struggle. Predators exploit body odour from their prey, such as a dog that can find a pheasant in the dark on the basis of the pheasant’s odour. Alternatively, prey can detect their predators as well. Predators leave all kinds of information behind. Those prey, that successfully exploit this information with an increased survival as a result will build more bodies. Detecting a predator on the basis of chemical cues has been recorded for animals ranging from mites to mice. And in various animals the prey can decipher the previous diet of the predator. For instance, mice can detect whether their coyote predator fed on a vegetarian diet or has consumed animals. The mice show a stronger avoidance to urine of carnivorous predators, for obvious reasons.

From microbes to man

Nothing in biology makes sense except in the light of body odour. You may still be left with the question about body odour and yourself. Insects, mice, cheetah, coyote, even microbes, they may use body odours to be well-informed and to build bodies. But humans? Are we indeed a scented ape? Michael Stoddart states that “When all the trappings and affection of civilisation are stripped away, we are merely scented apes”. In fact, it does not take much to see in our daily life how dependent we are on odours in general. Just think of what it does to you to smell the odour of freshly baked bread in the supermarket on a Saturday morning (is this a marketing trick?), or of the aversion that the stench of a microbe-infected orange induces. But there is much more. Although we think that falling in love is based on emotions, most likely it is governed by our sense of smell. Swiss researchers showed that we select a partner that has a distinct body odour which is a representation of a distinct major histocompatibility complex or a distinct version of the immune system of combating pathogens.

This even extends to the saying that the chemistry between people should be right in order to make social interactions successful and this has invaded national politics in 2003 when the formation of a government was impeded by “the wrong chemistry” between two politicians, as one of them explained.

Applied aspects of body odours

Plants have body odours too and they can modify them to ‘cry for help’. When plants are attacked by caterpillars they emit novel odours that are only produced in response to being attacked by herbivores. These ‘cry-for-help-odours’ attract carnivorous enemies of the herbivores whose feeding activated the plant’s response. Such carnivores include, for instance, parasitic wasps that lay their eggs in the plant-eating insects or predatory arthroprods that kill and consume the herbivores.

Not all plants within a species cry for help in the same way. Some plants produce large amounts (they ‘shout’)  and others produce small amounts (they ‘whisper’). The whisperers are more common among our crop plants, because we have never selected for ‘shouting’ plants. Through studies of the underlying mechanisms we can understand how exactly plants perceive who is feeding on their tissues and how plants respond with the production of specific body odour blends that attract their bodyguards. This involves a systems approach that integrates studies at the levels of genes, cells, individuals, populations and communities. By doing so we can develop sophisticated methods to select the whisperers and, thus, increase the effectiveness of biological control of insect pests. This is a valuable method to exploit natural variation. In nature plants are seldomly overexploited by pests or pathogens. Thus, it will pay to exploit natural variation to understand how plants survive in nature. This is the topic of a new 6.5 million euro national research programme funded by STW, entitled ‘Learning from Nature to protect crops’  that is officially launched today

There are many other economically important phenomena that involve body odour. For instance, the formation of root nodules by nitrogen fixing symbiotic bacteria in the roots of legumes is the result of an extensive communication between plant and bacteria and is of great economic importance for successful food production. The exploitation of insect pheromones is of great value for the prevention and control of pests as executed by the Pherobank at Wageningen UR. Moreover, research in Wageningen on flavours of food and flowers finds its way to the flavour industry. Chemical diversity is superimposed on biodiversity and this provides mankind with ample opportunities to exploit natural body odours.

Biodiversity, as a result of natural selection and speciation, provides the planet with a large variety of life forms that are connected through food webs that compose diverse communities. Within food webs and communities each organism is under selection to maximize the building of bodies and in doing so it pays to be well informed. Body odours appear to mediate many of the essential activities that organisms need to excel at, in order to maximize the building of bodies. I started with the statement “Nothing in biology makes sense except in the light of body odour” and I realize that this statement needs some digestion. Most likely the statement will not have as bright a future as Dobzhansky’s statement. However, even if that is true I hope to have convinced you that body odours play an intriguing role in evolution and biodiversity. After all, also the biology of body odours can only make sense in the light of evolution.

Figure legends

Figure 1: Natural variation in the two-striped blister beetle (Mylabris bifasciata). Picture represents a part of the insect collection of Wageningen University that contains 600,000 individual insects. Picture by Hans M. Smid (www.bugsinthepicture.com).

Figure 2: Parasitic wasp Trichogramma brassicae injects her eggs in the egg of a moth. Picture by Hans M. Smid (www.bugsinthepicture.com).