Honesty is just as important in nature as in a well-functioning human society.
In spring-time, the forest of the Bieszczady mountains is filled with biological codes. It’s like the Enigma machine itself: it pulses and rustles with secret messages, with the chirping of encoded hints, the croak of covert announcements, the hooting of camouflaged calls. If you’re lucky, you might literally trip over such a clandestine signal. In the undergrowth – still cool as the winter withdraws – we can find a fractal-shaped sort-of tree, a branched totem discarded by a stag. We, people, are used to sound communication, messages carried by the vibration of air. The bone candelabra of the antlers is more difficult for us to decipher. In order to understand it correctly – along with the message encoded within – we must travel a few months into the past, to a fog-enveloped mountain: September.
The love game
September has a very distinct smell. It’s probably one of the most geographically-determined months: it smells, very specifically, of a given place. The dryness of maple leaves on warm city mornings. The rain-soaked wind over an empty, ploughed field. The damp viscosity of mud, the earthy smell of thick clay smeared over mountain slopes and squelching against the soles of leather walking boots. I associate that last scent with a beech forest, the bristles on top of the drizzle-wet Bieszczady hills, slippery with autumn. At the beginning of spring, we go back to the very middle of September. As it slowly loses the memory of summer, the forest soaks up the morning; drops sway at the tip of every branch and every leaf that’s still attached to the stalk. It is a black wall with no third dimension, a flat night that I approach cautiously. I feel its chill, my face streaming with sweat and the juicy pre-dawn fog. That doesn’t really bother me, maybe only the water sloshing around in my boots distracts my brain, focused as it is on observation. After a while, the mind returns to the here and now, to pick up the sounds of the Bieszczady jungle, dripping with dawn. In the early autumn forest – like behind a dark curtain – hundreds and thousands of tiny splashes, dying leaves quietly falling onto soft moss, and the bellow of genuine, meticulously-calculated honesty. Stags are playing the love game.
If I had arrived at that forest darkness as a zoologist, I’d probably ponder over every single bellowing stag. Zoologically speaking, a male like this is, after all, almost 200 kilograms of muscle. It is rhythmically distending lungs that breathe out clouds of white fog into the mountain air. It is the powerful heart pulsing at the very centre of the animal. The thyroid, pancreas, liver and spleen – each organ dutifully performing its biochemical tasks. Finally, the ropes of tendons and ligaments which attach all that biology to the skeleton. Today, however, I am not a zoologist, but an evolutionary biologist. And that animalistic, musk-scented construction is, for me, just the packaging, an elaborate shell built around the most precious thing all stags have inside: their own genes. Evolution does not care at all about how something breathes, how it moves, how it hisses at unexpected passers-by and shudders at suspicious rustling. The gene, buried in rolls of flesh, only wants to make as many copies of itself as possible, allow them into the world as soon as possible, multiply itself more and more. The problem is that a gene is nothing more than a string of microscopic molecules oscillating in the darkness of the cell. Powerful, yes – after all, a gene encodes all the information necessary to create its stag. Every bend and curve of that organic, animal shell is described in the language of the letters of the genome – but what good is information this inconspicuous, so difficult to notice that we wouldn’t even pay attention to it if not for the whole panting, stomping, bellowing stag. The ability of this particular loudest stag’s genes to copy themselves and engender new genes, wrapped in their bodies, depends solely on the fitness of that body, on its determination and all its attributes gathered in one place. And the bellowing that carries above the Bieszczady valleys at dawn? Well, it’s nothing but pure, calculated, extreme marketing. Surprisingly honest.
Frauds
Honesty in biology might seem a very unlikely concept. It could be questioned by anyone who has ever encountered a cuckoo. The reserves of dishonesty and perfidy concentrated in that small creature could be enough for at least a few malicious species. As we know, the cuckoo lives on deception. It lays its eggs in other birds’ nests, ‘stealing’ their parental efforts and forcing the foster parents to take care of the cuckoo’s own offspring, usually staggeringly larger than the chicks of the exploited species. To add insult to injury, the cuckoo’s appearance is also deceptive: from afar, its striped body and slim silhouette are similar to those of the predatory sparrowhawk. This effectively instils fear in the potential victims of the cuckoo’s practices, giving it a bit more time and freedom to plant its eggs. It has to be said: this isn’t a species that could symbolize the conscientiousness and honesty of the biological world, which features oodles of similarly perfidious ways of life! Other cheaters include yellow-and-black hover flies: the colouring of these completely harmless, nectar-feeding flies makes them resemble wasps, and so they make use of the wasp’s deadly reputation and avoid unpleasantness from other predators. Then there are the blatant lies of orchids from the genus Ophrys, whose flowers look (and smell!) like the resting females of certain hymenopterans. Excited by this appearance, males of the same species make attempts at passionate copulation with the orchid’s flowers, are obviously sorely disappointed – and also receive the gift of the orchid’s pollinia stuck to their bodies, ready to be transported to another flower.
Is there such a thing as biological honesty, then? If there is, what makes certain species decide to walk that path – even if the cost is horrific – while others blithely continue their deceptive schemes, always looking for ways to ‘game the system’?
It’s not difficult to understand honest signalling in biology, especially if we stop thinking about signals in our human categories for a while. Creating a false signal may seem incredibly easy to us – after all, art history is rife with more or less successful forgeries of the greatest masterpieces, and the crimes of counterfeiting money that come to light from time to time are clear proof that humanity is unrivalled with regard to mass production of fakes. But let us bear in mind that if for us counterfeiting something requires, at most, finding the appropriate tools and devoting a certain amount of time, for animals such a strategy may mean investing everything they have. While a forger of paintings risks, at worst, the client’s dissatisfaction (caused by the forgery’s insufficient similarity to the original) or a few years in prison, an animal that attempts to falsify a biological signal usually pays in the ultimate currency: its own life.
Exceptionally good genes
The morning has stratified the Bieszczady forest into a three-dimensional panorama; after the black cut-out of the contours of the trees, now you can only see the tangle of beeches and spruces, gradually warmed by the sun. Among them there’s autumnal silence; the stags’ echoing bellows have faded away. Now the most I can hope for is an encounter with one of the stags as he steps carefully among the trees, with his absurdly large antlers.
Both the bellowing and the branched lampshade of the antlers are almost perfect signals. First, they’re perfectly detectable. The echoes from the rutting ground are audible from far away; caught by the narrow ravines of mountain valleys they can carry over even 10 kilometres. And the antlers – well, it’s difficult to walk past something that abstract. It is impressive even when found later, on a March morning, separate from the animal, deep in a tangle of brambles coming back to life. To say nothing of when it crowns the head of a stag! While it’s not a structure that can be compared to the antlers of the extinct Irish elk, which could weigh more than 40 kilograms, the weight of a set of red deer antlers can reach 10 kilograms. Manoeuvring something this awkward in a forest full of tangled branches must be quite an achievement – and let’s not forget that deer don’t only sedately walk around their territory. If there’s a need to prove their status, stags take part in duels that often include wrestling with their antlers locked in with each other. In fact, the spectacular quality of the stags’ status symbols is what determines their honesty.
Although not everyone will find the bellow of a red deer or his fractal-like antlers to be the embodiment of biological beauty, biologists refer to these characteristics as ‘ornaments’. They are the individual’s ‘decoration’, a feature that is preferred by females when choosing the best male – and hence the thing that will allow the genes hidden deep in the animal’s body to reproduce effectively in its offspring. The cost of these decorations is obvious. During a stag’s rut (that is, the few weeks of intense wooing of hinds and building his own private harem), he must have a truly iron constitution – in the rutting ground, and then when guarding their females, stags practically stop eating. In the breeding season, they can lose even 20% of their body mass – it’s as if an average human dropped 8-10 kilos, just like that. Only really healthy males, in prime condition and with no illnesses or injuries to slow them down, are able not only to survive the ordeal, but also effectively repel attacks from rivals trying to challenge them to duels. Both producing and carrying the large antlers and the constant all-night bellows echoing in the mountain valleys are a challenge to the stag’s body. A weak or sick individual wouldn’t be able to produce these ornaments in the first place, and furthermore, even an attempt to face down stronger and more experienced males could end tragically for a weakling like this.
The gist of the honesty of biological signals, then, lies in their cost. Obviously, this involves no intentionality, nobody chose these particular characteristics – deliberately expecting their cost, thus ensuring the honesty of the signal broadcast by each specimen brave enough to wear these ornaments. All this was most probably shaped by blind, painfully random evolution, which iterates various characteristics and signalling solutions and unscrupulously eliminates all the unsatisfactory combinations of an animal’s weak constitution and particular ornament. Signals that have no option of cheating emerged from that evolutionary mix in passing, as it were, as a side effect of filtering out all unsuccessful attempts and approaches.
Evolutionists sometimes describe this system of signalling by referring to the so-called good genes hypothesis. Here we return to the beginning of the story, when instead of imagining stags as they wander around the forest, steaming and smelling of wet fur, we thought of inconspicuous genes, wrapped in muscle, bones and glands, and only waiting for the next opportunity to replicate. It is these genes that are probably the most important reason why signalling – and its attendant honesty or dishonesty – has any meaning in nature. For the hind, it doesn’t really matter that a given stag is able to carry the kilograms of his antlers, that he can bellow at the top of his voice all night, oblivious to the outside world for many hours. What she is really looking for are good genes for her offspring, optimal versions of these vital instructions for the ‘reconstruction’ of deer bodies in her children. When trying to secure as good a set of genetic guidelines as possible, the female must be driven by something externally visible, something that the deeply hidden genes reveal to the world.
The problems of excess
Honest signalling, then, came into being as a way to externalize the usually invisible information encoded in genes, allowing for a thorough evaluation of what the male’s genetic material has to offer. But the most interesting thing about all this is not that genes – selfish replicators that direct the biology of their organic shells – have developed such a system. What’s perhaps most fascinating is the variety of ways in which genes can broadcast information about their quality. In the case of deer, it is easy to imagine a mechanism that ensures honesty. An animal will simply not manage to function with excessively huge antlers while also suffering from bad constitution or parasitic diseases. But the animal world signals not only via antlers and loud bellowing. It also includes bright colouring, complicated calls, long feathers or outsized body parts – in each case, the ornament’s honesty is ensured by a specific, often quite surprising mechanism that ties the signal with the body’s physiological capabilities.
As an example, let’s take the yellow and orange feathers seen in many birds – an ornament commonly encountered in species like tits, robins, chaffinches, orioles and greenfinches. Their colouring is caused by pigments called carotenoids – the same chemicals that give the orange carrot or the yellow pepper their tint. Although their usage seems much easier than producing heavy and awkward antlers, carotenoid pigments have a hidden characteristic that lets these signals retain their honesty. All carotenoids are strong anti-oxidants, so they play a vital role in detoxifying the organism and removing the oxidants that appear during normal everyday activity. Carotenoids also protect the delicate body from the effects of aggressive forms of oxygen that appear as the immune system reacts to parasites. An animal that is able to give its feathers or skin an intensely yellow or orange tinge is also sending the signal that it can spare carotenoid pigments for that purpose, instead of mobilizing all of them for their anti-oxidant purposes. Perhaps this individual knows how to get hold of carotenoids so well that it has enough, or maybe it is in such good health that it can let itself siphon off a little from the protective barrier they give. The result is the same. Only the best can survive – the ones that announce themselves with the brightest colours.
The intentional deterioration of certain functions of one’s body – done by moving precious pigments from one kind of tissue to another – is a trace of something more fundamental: a mechanism proposed a few dozen years ago by Amotz Zahavi as a potential way to connect ‘good genes’ with the honesty of biological signalling. Zahavi called his theory the handicap principle; it is easier to understand if we look at the surreal ornaments of a deer encountered in the forest. The ‘handicap’ here means the development of organs and structures that are so difficult to handle, so awkward and gaudy, that they objectively ‘hamper’ the animal’s abilities, making it difficult for it to move, acquire food or escape predators. The handicap can be anything: in the brightly-coloured robin, it is the intensely orange breast, visible to predators from a distance and putting the bird in constant danger; in the peacock it is the gigantic tail whose size practically prevents the bird from agile movement and avoiding predators. Baboons develop red skin ornamentation on their buttocks – it requires sustaining a high level of testosterone in the blood, which, in turn, slows the immune system and increases the risk of infection and parasite attack. In a system like this, every mutation that weakens the innate honesty of the signal is immediately eliminated; natural selection is ruthless towards those who try to hack the system and try to present an equally sophisticated signal at a smaller cost. An animal sending an honest signal is simply telling its audience: “Look! Even though I’ve got this strange thing (antlers, colour, tail, etc.), I’m still alive and well. That must mean something!”
Where does that leave dishonest and selfish signalling, then? If by definition it is supposed to be misleading, doesn’t it undermine the whole clever evolutionary construction, in which only honest signals can defy natural selection? Yes and no. Naturally, deceitful signals cannot be based on the same principles of promoting good genes; their fundamental task is not to advertise any quality, but to mislead. This is partly the reason why we encounter such signals much more often in communication between different species (as opposed to communication within the same species, such as when engaged in sexual selection). Signalling lies also have their evolutionary safety catch – a mechanism that means they remain clear no matter the level of fraud involved. Here, what determines the sophistication of such signals is an arms race, a constant chase between the cheater and the cheated, a game of cat and mouse in which both sides try to commit more effective fraud. Or better: try not to be the victim of fraud. But that’s a story for another mountain trek…
Translated from the Polish by Marta Dziurosz
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