Sex is war. It’s a battle for limited resources.

The source of sexual conflict is this: sperm is a relatively cheap resource for males to produce, whereas producing eggs and rearing offspring is a much larger investment on the part of the female. Darwin was the first to realize the implications of this. He reasoned that this imbalance should result in males competing with each other to fight for the limited resource, and females exerting a strong choice on who to mate with. Taken together, male competition and female choice were the two pillars of the theory that he called sexual selection.

The battle of the sexes is not a new idea, but it has changed with the times.

In the 1960s and 70s, the sexual revolution was eroding away conservative ideas about sex. This was the era of promiscuity. And this changing social fabric was being mirrored in science. The ‘free love’ era brought about an equally potent, but more silent, revolution within biology – one that completely shook up our old, prudish notions of reproduction. Research from these decades onwards taught us that in almost all animals, from insects to birds and mammals, females typically copulate with multiple males. We learned that promiscuity is not a freak event, it’s actually the norm. What this implies is that, like any modern war, the battle of the sexes is a messy and involved affair, often leading to surprising and unexpected consequences.

For one thing, it’s being fought on many fronts. In many species, competition between males for the egg doesn’t stop at intercourse. Even after the female is inseminated, the battle rages on inside her reproductive tract. In this alien battlefield, the sperm cells of different males compete with each other to fertilize the eggs. Meanwhile, the reproductive organs of the female can still exert control by choosing between the different sperm.

And just like the Greeks who sneaked into Troy, the soldiers in this battle use every trick at their disposal to gain an upper hand. Some males do the equivalent of taking their ladies out to a fancy restaurant – they present females with a nutritious meal in their sperm, at substantial cost to themselves (delightfully, biologists call this a prenuptial gift). Others resort to date rape  – their sperm includes a harmful cocktail of drugs that alter the females’ behavior in their favor. Even more chilling, there are species in which the males engage in traumatic insemination, where they essentially rape the females. Other males are just outright weird. Some leave their penis behind to plug the vagina from use by other males. Others have smelly sperm that repels other males. And others have spiky penises, that scrape the vagina clean of the sperm of competitors.

In this evolutionary arms race, the females are not passive bystanders. They play an active role, by evolving counter defenses, and by choosing between different sperm in their reproductive tract. A striking example of female reproductive choice arises in the case of ducks. Duck sex is typically forced by the males, and the females have evolved fake vaginas into which they can channel the penis of an unsolicited male. The author Carl Zimmer describes this sexual tension in remarkably eloquent prose:

“My tale is rich with deep scientific significance, resplendent with surprising insights into how evolution works, far beyond the banalities of “survival of the fittest,” off in a realm of life where sexual selection and sexual conflict work like a pair sculptors drunk on absinthe, transforming biology into forms unimaginable.”

And nowhere is this sexual conflict between sperms and eggs more thoroughly understood than in the humble fruit fly. A new experiment published this week by Laura Sirot, Mariana Wolfner and Stuart Wigby at Cornell University introduces a strange new twist to this story.

Here’s the story so far. Fruit flies have long been an experimental workhorse of bench biologists, not least because of their incredibly efficiency at laying eggs. It’s known that male fruit flies include in their semen a cocktail of chemicals that improve their reproductive success. There are chemicals that cause the female to lay more eggs. Others that woo the female into storing more of the sperm. Some chemicals are like a key – they get the female to release the sperm from the storage vault inside her. And some dull her sex drive, making the female temporarily less interested in mating with subsequent males.

The researchers focused on the main chemicals in semen that stimulate egg production in females. One of these chemicals is called sex peptide, and it has the effect of boosting egg production for more than 3 days. It also temporarily makes the females less receptive to the advances of other males.

In the first experiment, they took female flies who had already mated once, waited for a day, and mated them with a new fly. These new mates were of two types – they either had sex peptide in their ejaculate, or they were genetic mutants who could not produce this chemical. By comparing these two groups, the researchers could establish the effect that sex peptide had on females that had already mated. As a control, they also looked at females who only mated once. Their results are summarized below:

The white bars are the females who did not remate, the dark and light grey are the females who mated with males with and without sex peptide, respectively. What the figure shows is that the second mating had no effect on the number of eggs being laid by the female (the white and grey bars are no different). The chemical cocktail of the first male had already pushed her eggs to a maximum number, and additional dosage of the chemical had no effect on the size of her clutch.

Now imagine the plight of the tiny male fruit fly. It faces fierce competition from other flies, and will use any trick that it can to get ahead. The above figure suggests that if a male fly comes across a female that has already mated, then it’s in his interest to ‘switch off’ production of chemicals that boost egg production. After all, she’s already been pumped a full quota of this chemical, so producing any more is a waste.

However, if the fly does away with sex peptide, he faces a disadvantage. You see, this chemical didn’t change the number of eggs laid by the female, but it did have an effect on her behavior. It still makes her less receptive to other males. You can see this in the following figure (SP+ are males with sex peptide, SP0 are males without).

So what’s a scheming fly to do?

There is a way out. If it produces any chemical whose only effect is to boost the number of eggs, than it should make less of it when mating with a female who’s already got some.

The researchers predicted that a chemical called ovulin – the other main ingredient of this drug cocktail – should fit the bill. They argued that since flies can discern whether a female has already mated, it is in their interest to reduce any unnecessary ingredients in their ejaculate. Just like balancing a budget, it’s all about optimizing expenses and minimizing wastage.

They tested their prediction by comparing the volume of these chemicals produced by males in both cases – first encounters, and repeated matings. Here is what they found:

In the figure, V represent matings with virgin females, and M are matings with females who have mated before. The results are in complete agreement with their predictions. When males are not ‘the first one in’, they reduce their production of ovulin, but not of sex peptide. They are effectively tuning the ingredients of their ejaculate to take advantage of their competition.

This is a cool new result, for a couple of reasons. Sperm competition had already pushed the battle of the sexes into the female reproductive tract. But this result shows a new kind of sophistication to this war – ejaculate espionage.

And it also leads to new questions. The mechanism by which flies can alter the contents of their ejaculate is entirely unknown. And no one knows whether males of other species can also repackage their sperm.

Darwin would have been thrilled to see his insight being applied to this virgin territory.

References
Sirot, L., Wolfner, M., & Wigby, S. (2011). Protein-specific manipulation of ejaculate composition in response to female mating status in Drosophila melanogaster Proceedings of the National Academy of Sciences DOI: 10.1073/pnas.1100905108

If you’re interested in the subject of sexual conflict and sperm competition, here are some great reads:

Dr. Tatiana’s Sex Advice to All Creation by Olivia Judson

Promiscuity: An Evolutionary History of Sperm Competition by Tim Birkhead

and you should definitely listen to the Radiolab episode on Sperm

Image Credits

Fruit flies mating by T. Chapman in PLoS Biology; Vol. 6, No. 7, e179; July 29, 2008. Creative Commons Licensed.

The genitalia of the Callosobruchus analis beetle by Johanna Rönn, Department of Animal Ecology, Uppsala University. Licensed by Wikimedia Commons.

Figures were taken from the referenced paper, as always.

Why do we have sex? If this question keeps you up at night, you either have really loud neighbors, or you have the makings of an evolutionary biologist. Some of the most brilliant minds in the field – William Hamilton, John Maynard Smith and George Williams – have spent much of their careers wondering about the value of sex. This is not a reflection on the quality of their sex lives. Rather, it has more to do with their creative insight and ability to look at the world with fresh eyes.

A billion years ago, our ancestors inhabited a world without sex. This was the era of the clones. In this strange world, all organisms reproduced by creating identical genetic copies of themselves, somewhat similar to how modern-day bacteria reproduce [1]. But this clonal strategy has a problem. Populations made up of identical twins are more vulnerable to infection. When a disease comes along, it doesn’t just wipe out a few individuals. It can take out the whole lot.

When sex arrived, it introduced a new pace to life. Organisms were mixing and matching genes in combinations never seen before. Imagine a world where you had to dress well to survive. In such a world, the invention of sex is like going from wearing uniforms to having your own wardrobe. You could pick a gene from here, another from there, and put together a novel offspring. And if a particular outfit were deemed ‘unfit’, it’s not a huge tragedy as there are plenty of alternatives.

In this way, sex helps us by innovating new evolutionary solutions and by protecting us from disease. But sex is not without its discontents. For one thing, sexual reproduction implies that you only pass down half your genes to your offspring. The other half come from the other parent, and they combine to make an offspring with a full set of genes. On the other hand, in asexual reproduction, the mother passes on a full set of genes to her offspring. So by adopting sex, your genes are travelling half as far. In evolutionary terms, this is a huge cost, and sex had better have a lot to offer for it.

Do the benefits outweigh the costs? We would certainly like to think so. But when evolutionary biologists did the math, they worked out that the answer is usually no. Your genes typically have more to gain if you reproduced asexually.

So what gives? Why, then, do so many species adopt a sexual lifestyle? Well, here’s a brilliant solution offered by Hamilton and others: if you are under constant attack by rapidly evolving parasites, then sex is a better strategy than cloning yourself. This idea came to be known as the Red Queen hypothesis and can be summarized in one line: it’s harder to hit a moving target.

According to this theory, the main purpose that sex serves is to rapidly change our genetic makeup in order to keep pace with the threat from parasites. The parasites themselves are also evolving in order to keep attacking us. It’s a race where everyone is running but no-one really gets ahead, quite like the race between the Red Queen and Alice in Through the Looking Glass. While this does have a nice literary ring to it, I prefer a more space-age analogy. I picture the eternal chase between the evil robots and the human race in Battlestar Galactica. Technology keeps evolving on both sides, and so the humans have to work just as hard as ever to stay one step ahead.

The Red Queen idea was a theoretical offshoot of evolutionary theory. And like any good theory, it made a clear, testable prediction. Species that are exposed to a greater load of parasites should be more likely to reproduce sexually. In the last few years this idea has found support in a beautiful series of experiments involving snails, led by Kayla King, a graduate student in the lab of Curtis Lively at Indiana University.

Snails have interesting sex lives. In many species, the snail has a choice – it can either mate with another snail, or it can directly clone itself. Hedging bets by ‘going both ways’ is a remarkably common strategy in the tree of life [2].

In a study published in 2009, the researchers focused on a type of snail called the New Zealand mud snail, that inhabited two different lakes in New Zealand. Crucially, both lakes also had a parasite that infected the snails. The parasite is called microphallus, a bit harsh for a worm that’s only a fifth of a millimeter long as an adult, in my opinion. And these parasites have a strange and alarming life cycle.

Picture this: the eggs of microphallus are eaten by the snails. They hatch into a larva, which begins to grow in the snail’s gut. The larva drills through the intestine, making its way to the reproductive organs. Here the parasite begins to multiply, and consumes much of the snail’s reproductive and digestive tissue, rendering it completely sterile. Eventually the body of the snail contains hundreds of tiny cysts. When a duck comes along and eats the snail, the next stage of the parasite’s life begins. These cysts hatch to form tiny worms, which spend their entire adult lives in the duck’s intestine. Here they meet other worms, mate and produce eggs – which completes the life cycle. If this picture sends a shiver down your spine, you’re not alone.

Now, ducks only live near the lake’s surface. And the parasite can’t survive without ducks, which means that it is basically confined to shallow water. If the Red Queen idea is correct, then a heavy parasitic load should lead to intense evolution of the host, through sexual reproduction. To test this idea, the researchers went to two different lakes and compared the snails that lived in shallow waters to those found in greater depths.

Here is what they found. If you collected both shallow and deep snails and exposed them to their local parasites, the shallow water snails had consistently lower rates of infection. However, if you tried to infect snails from one lake with parasites from the other lake, the shallow water snails would fare just the same as the deep water snails.

This meant that the shallow water snails were indeed co-evolving with their local parasites. The researchers also found that the frequency of snails adopting to reproduce sexually is significantly higher in the shallow water snails as compared to their deep water relatives. These results are just what you would expect if the Red Queen hypothesis were true.

In a follow up paper this January, the authors studied the relationship between parasitic infections and genetic diversity in more detail. They looked at snails collected from 17 independent streams in New Zealand, and screened them for their genetic diversity, whether they were clonal or sexually reproducing, and whether they were infected by parasites of any type.

None of the 17 populations had done away with sex entirely. They found that as the prevalence of infection increased in a population, so did the percentage of sexually reproducing snails. As in the previous experiment, this suggests that parasitic load is driving populations to adopt sex for reproduction. They also found that among the snails that were asexual, as the prevalence of infection increased, so did the diversity between clones. What this suggests is that parasitic load is doing more than just driving sexual reproduction. It is also alleviating one of the main problems of the clonal strategy – lack of genetic diversity.

The Red Queen hypothesis is an out-of-the-box solution to a scientific conundrum. It is creative, theoretically consistent, and makes clear cut predictions – the hallmark of good science. And personally, I find it cool because it teaches us that the little guys matter. The idea that tiny microscopic life forms are driving the evolution of macroscopic beings completely topples our notions of who’s in charge here.

Footnotes

[1] Many caveats here. For one, bacteria can engage in a kind of primitive sex.

[2] All species that have switched to a completely asexual lifestyle did so fairly recently, in evolutionary terms. This must mean that many who have tried to adopt such a strategy went extinct in the long term. There is one remarkable exception, and that is the Bdelloid rotifers, who have gone without sex for 80 million years!

If you’re interested in reading more about this subject, you may be interested in:

The Red Queen: Sex and the Evolution of Human Nature by Matt Riddley

And this Nova documentary called Why Sex?

References

King KC, Delph LF, Jokela J, & Lively CM (2009). The geographic mosaic of sex and the Red Queen. Current biology : CB, 19 (17), 1438-41 PMID: 19631541

King KC, Jokela J, & Lively CM (2011). Parasites, sex, and clonal diversity in natural snail populations. Evolution; international journal of organic evolution, 65 (5), 1474-81 PMID: 21521196

Image References

Mud Snail image and Life Cycle of Microphallus from Lively lab.

Alice and the Red Queen from Through the Looking Glass (Public Domain).

Snail ecosystem figure from King et al (2009).

And death is not just the end of the individual, it’s the end of a lineage. Organisms that die before they can reproduce deny their genes a road to the next generation. In this simple fact lies the engine of change. For example, genes that make a prey more camouflaged will end up increasing their reproductive success, whereas genes that make them more noticeable are not going to get very far. In this way, natural selection is driving prey to become better hiders, and predators to become better seekers.

Nowhere is this evolutionary race more evident than in the case of the peppered moth. This is a species of moth that is found all across England and Ireland. When people first studied them in the early 1800s, almost all the moths looked something like this:

As you can see (if you’re looking closely), the white and black speckles are effective camouflage. For ages, these moths have hidden on light colored trees and lichens. Over time, they have evolved this distinctive pattern to help them evade the notice of the birds that prey on them.

But just fifty years later, things were beginning to change. By the 1850s, moths of the same species had stumbled upon a new color. These new moths were called carbonaria after their carbon-black color, to distinguish them from their salt-and-pepper colored relatives with the dull name typica.

By the end of the nineteenth century, the change was drastic. In 1895, a study in Manchester showed that 95% of the peppered moths were now of the black type. So what was going here? What could cause such an incredible change in appearance in just a hundred years?

They key lies in a major event in the history of humanity that took place during the nineteenth century – the Industrial Revolution. During this time, a large number of factories were being built in England, and they burned a mind boggling amount of coal. From 1800 to 1900, annual coal production went up in the UK from about 10 million tonnes to 250 million tonnes.

This had a drastic effect on the environment. The trees in the woods between Manchester and London were covered in soot. And the increased levels of sulphur dioxide was killing the lichen. All of a sudden, the peppered moth was losing its camouflage. It stood out like a sore thumb against the sooty black barks of the trees, while the rare black form of the moth became an instant success.

In a new study in this week’s issue of the journal Science, researchers in Liverpool and the Czech Republic were able to trace down the genetic signatures of this extreme evolution. They did this by looking at the variation in letters of DNA between the 2 types of moths.

At the heart of the idea is sex. The genetic role of sex is to shuffle together different genomes in a population. This has the effect of creating more types of genomes, and thus increases diversity.

When the Industrial Revolution comes along, it paints the world of the moth black. Most of the genomes in the population get wiped out as they are no longer fit. A few rare ones contain a gene that protects their possessor by coloring them black. These genomes quickly begin to dominate in the population, and so there are now fewer kinds of genomes around – the diversity begins to plummet (think of 1895, when 95% of these moths were now black). This is known as a selective sweep, where a set of genes rapidly sweep through a population.

Over time, as these moths mate with others, the diversity builds back. But just as it takes many shuffles to completely randomize the order of cards in a deck, it takes many generations of sexual reproduction before all trace of the past is lost in the genome. By tracing down regions of the genome with unusually low diversity, we can uncover the signals of natural selection that must have acted on our ancestors. This method of detecting natural selection works best if the selection was strong (so that it wiped out the diversity), and if it happened recently (so that sex hasn’t had enough time to bring the diversity back).

This is just what the authors did. They first compared the genomes of 68 typica and 64 carbonaria moths (the offspring of two pairs of parents) and found that a particular region on one of the chromosomes was responsible for the difference in moth color. But this is a coarse-grained picture, as the region that they identified is over a million letters in length. The next step was to probe the diversity at a finer scale.

To do this, they looked at 6 variant letters of DNA that were spread out in this region, and measured how the carboneria and typica moths vary with respect to these letters. At each of these positions, there are 2 possibile letters that any moth can have. So if the genomes were properly shuffled with the maximum level of diversity, there would be 32 64 possible possible 6 letter words that could be formed here.[1] The spotted moths were found with many different words in this region, a sign of diversity. The black moths, on the other hand, all had small variations from just one sequence: CAGGTA. The scientists inferred that this must be the ancestral sequence of the black moths that thrived in the Industrial Revolution.

By comparing our DNA, we are actually looking back in time. We can use these techniques to infer the pressures that our distant ancestors faced. A cool example of this kind of DNA archeology is the story of lactose tolerance in humans.

Here’s a counter intuitive fact – mammals typically can not digest milk in adulthood. Of course, all mammals love milk as infants (that’s what gives them their name). That’s because they can produce a chemical called lactase, which breaks down the lactose in milk. But once infants reach the age of being weaned, the body switches off production of lactase. We all like to think of cats as cute pets that love a saucer of milk, but in reality this is more likely to give them indigestion and diarrhea. Lactose intolerance is not a disease, it’s actually the norm.

This makes sense from an evolutionary point of view. Milk is a nutrient rich food for infants, but it is costly for a mother to produce. At some point, the growing infant needs to move on, or it will become too great a burden for the mother. This digestive ‘switch’ in mammals ensures that this happens.[2]

So why is it that some us can digest milk? The answer takes us from one cultural revolution to another, to a time  8000 years ago when some of our ancestors had begun to rear cattle. This was happening in the Middle East and in Africa. Through sheer chance, anyone who had a mutation that disabled this lactase switch suddenly had an advantage over their peers. They had access to a reliable and nutrient rich source of food – milk from cattle.

The same process that changed the color of the moths is at work here. As was shown by a team led by Sarah Tishkoff in 2006, cattle herders in Africa and in the Middle East independently evolved different mutations that allowed them to drink milk, an example of what is called convergent evolution [3]. This is why lactose tolerance is very prevalent in Europeans. Many of their ancestors were cattle herders who originated in the Middle East. Similarly, northern Indians are more likely to be able to digest lactose than southern Indians, perhaps due to closer contact with the pastoral Sindhi tribes of north India.

And those of use who can digest milk carry the signs of this cultural revolution in our DNA. To date, the region surrounding the lactase gene has a remarkably low diversity in populations that descended from cattle herders.

We usually think of adaptations as occurring in response to changes from within nature. But I find it fascinating that our culture can also be a driving force of evolution. It has happened time and again, without our explicit knowledge of it. During the dawn of agriculture, we evolved wild grains into harvestable varieties like wheat and rice. In the birth of pastoralism, we modified our cattle to produce more milk, while also evolving ourselves to be able to consume it. And in the Industrial Revolution, our pollutants ended up driving evolution in moths.

As we look further out into space, we learn more about the origins of our universe. But at another extreme, by looking inwards to our DNA, we are also learning more about our place in it. We are unraveling the lives and cultures of our prehistoric ancestors, as well as the effect that we have had and continue to have on our surroundings.

Incidentally, the story of the moth has another surprising twist. Eventually the air quality improved in the UK, and the lichen began to grow back. The trees were restored to their lighter colors. And this meant that the carbonera moths have once again started to get noticed. They are now at a great disadvantage and have become extremely rare. In this way, the ebb and flow of genes are echoing the waves of cultural changes.

Footnotes

The kind of evolutionary genetics discussed in this article is the subject of my research. I have spent the last year and a half working on a project that studies how certain African pastoral tribes have evolved protection to their extreme diets, a case of culture and gene flow being intricately woven together.

[1] There are 2^6 = 32 64 combinations in all. The reason for there being 2 possible letters at these variant locations and not the usual 4 (A, C, T and G) has to do with biology. The variants arise through mutations (for example, an A gets flipped to a T) in somebody. It is incredibly unlikely that two mutations in the recent past (say, A to T and A to C) will occur at exactly the same place.

[2] However, if this lactase disabling switch was only useful to the mother, than it wouldn’t evolve. But such a switch also benefits her genes, as she can now invest the resources that she gains on caring for her offspring or on rearing more children.

[3] Incidentally, the peppered moth also occurs in North America, and there are reports that a similar adaptation towards darker moths arose along with the rise in pollution in the nineteenth century. If true, than this is another neat example of convergent evolution.

References

Van’t Hof AE, Edmonds N, Dalíková M, Marec F, & Saccheri IJ (2011). Industrial Melanism in British Peppered Moths Has a Singular and Recent Mutational Origin. Science (New York, N.Y.) PMID: 21493823

Tishkoff SA, Reed FA, Ranciaro A, Voight BF, Babbitt CC, Silverman JS, Powell K, Mortensen HM, Hirbo JB, Osman M, Ibrahim M, Omar SA, Lema G, Nyambo TB, Ghori J, Bumpstead S, Pritchard JK, Wray GA, & Deloukas P (2007). Convergent adaptation of human lactase persistence in Africa and Europe. Nature genetics, 39 (1), 31-40 PMID: 17159977

Image Credits

Creative Commons Licensed: Peppered moth (typica) by Andy Phillips. Black moth (carbonia) by naturalhistoryman. Cat and milk by Sunfox. Maasai herder Kamaika Kingi by Oxfam International.

Wikimedia Commons Licensed: Light and dark moth (typica and carbonia)

Meet Alice. She is 4 centimeters tall and moves about on wheels. Her goal in life is to look for food. Remarkably,the foraging behavior of this tiny robot has not been programmed by humans. Instead, her creators gave Alice a brain, and let evolution do the job of programming it. And Alice is going to show us why it is that individuals often make sacrifices for each other.

Animals often behave in seemingly selfless ways. The most regimented examples come from the social insects – the ants, termites, wasps and bees. Here selflessness is built in to the fabric of their society, as there are sterile castes of workers who tend to the eggs of the queen. Worker bees will often make the ultimate sacrifice and die protecting the hive from invaders. These are all altruistic acts, as they harm the individual while benefitting someone else.

Take a moment to think about this behavior from the point of view of evolution. If everyone’s competing to get ahead, why take an unnecessary risk or suffer to help someone else? You really couldn’t do much worse than adopt a sterile lifestyle – it’s an evolutionary dead end.

People used to talk about such altruistic behavior as  being ‘for the good of the species’. But this explanation does not work. Natural selection does not operate at the level of species, it is solely concerned with the reproductive success of the individual. Any gene that inclines an individual to be more concerned with the welfare of the species than with their own welfare is not going to get very far.

This type of evolutionary logic paints a picture of a world red in tooth and claw, one where you need to constantly be watching your back. But if everyone is looking out for their own selfish interests, where does selflessness come from? The solution to this puzzle was put forward by J. B. S. Haldane in the 1930s, and made precise by William Hamilton in 1963. Hamilton had the remarkable insight to think of this as an economics problem, and rephrase it in terms of costs and benefits.

In the business of evolution, everyone is looking for the best strategy to invest their genes in the next generation. You are faced with two options. You can either 1. Be selfish and suffer no cost to yourself or 2. Be altruistic and help out a relative, while suffering a cost to yourself.

So what should you do? Well, if the relative is close enough and the benefit to them is sufficiently large, you should pick the latter option, because in helping them out you are helping out your own genes. This is known as kin selection. But if your kin is really a distant relative, and your suffering is not helping them much, then the selfish option is a better bet.

In other words, Hamilton realized that altruism is a more efficient way to propagate your genes than selfishness, provided that the benefit to your genes exceeds the cost that you suffer from the act. He summarized this strategy with the following simple equation:

Here r is the degree to which two individuals are related (1 for identical twins, 1/2 for siblings, 1/4 for nephews or nieces , 1/8  for cousins, and so on). B is the benefit that your kin will receive from your action. And C is the cost that you suffer by performing this act.

This is known as Hamilton’s rule, and when this equation is satisfied, it makes evolutionary sense to be selfless [1]. The biologist J. B. S. Haldane intuitively understood this concept. When asked if he would risk his life to save a drowning brother, he famously replied “No, but I would to save two brothers or eight cousins” [2].

In the nests of ants, bees, and wasps (together known as the Hymenoptera) there is usually a single queen mother, and a sterile caste of daughters who are the workers that tend to her eggs. It turns out that through a quirk of their genetics, these female sisters are more closely related to each (r  = 3/4) other than they would be to their own offspring (r = 1/2). So as a savvy Hymenoptera female, the most effective way to propagate your genes is not to have any children of your own, but instead to get your mother to lay reproductively capable sisters for you. This is the origins of the sterile caste.

Now, of course, no one is saying that these insects are sitting down to calculate degrees of relatedness. Hamilton’s strategy is not being obeyed consciously. Richard Dawkins eloquently popularized the ideas of Hamilton and others in his brilliant book on the subject of altruism, The Selfish Gene. There he suggests the following analogy: you can think of an animal as a kind of unconscious robot following a specific program. The program was not written by any human programmer, instead it has been written and fine-tuned by natural selection. And after many rounds of being optimized by natural selection, you would expect to see selfishness or altruism emerge, in accordance with Hamilton’s rule.

In fact, why stop at an analogy?

In a recently published paper, Swiss researchers in engineering and in evolution collaborated to perform a neat experiment.

They built an arena for 8 Alice micro-robots, who were given the task of collecting food. The food in question was in the form of 8 tokens on the ground. Each robot could see the world with 6 sensors – 3 distance sensors to detect food, a fourth to distinguish food from other robots, and two vision sensors to know where to bring the food. They could get around using two wheels. And they had a software brain, known as a neural network.

Neural networks are an attempt to emulate the ways in which the neurons in our brains are wired together. Think of it as a road map of Alice’s brain. Every neuron is depicted in the figure above as a grey circle, and it can either be on or off. If enough traffic flows into a neuron, it will switch on. On the left, the 6 input neurons respond to Alice’s every sensation. As they fire, they send traffic to the right. The 3 rightmost neurons are the output of her brain.

Alice is programmed by tuning the strengths of each of these neural corrections. You could think of them as speed limits on each of the different roads, which then determine how the traffic will flow. These 33 speed limits (one for each neural connection), taken together, completely determine how Alice will respond to any situation. They are her genome, the programming that makes her tick.

The robots used their brains to make a very important decision. Every time they collected a food item, they had to decide whether to be selfish or be altruistic. If they were selfish, they would rewarded by a certain amount (this is the cost C). If they were altruistic, they would forgo the reward, but instead benefit the other 7 robots (each of whom share the benefit B). So they are either feeding themselves of feeding the others. This decision is clearly a key factor in how much food each robot gets.

The experiment works as follows. Think of the 8 robots as a tribe. They are left in the arena to collect food. After one minute, the researchers count how much food each robot has collected, and tally up the costs and benefits. Those robots with the highest scores are the most successful, and their genes are then the most likely to make it into the next generation. They researchers also modeled two crucial features from biology – mutations and sex. The genomes could be slightly altered by random mutations at every generation, and they could shuffle with other genomes to produce hybrid offsprings (this is sex, with all the fun bits stripped away). In this way, the robot’s programming would change through small increments at every generation.

They repeated this game of artificial evolution for 500 generations [3]. At first, the randomly programmed robots spun about aimlessly, having no specific program or goal in mind. But over time, they started to get much better at collecting food. You can watch this happen in the following video interview with one of the authors (look out for the difference between generation 0 and generation 149):

The researchers repeated this experiment many times, while varying the values of the costs and benefits (C and B), and also varying the relatedness (r) of the robots in a tribe. There results of 500 generations are summarized in the figures below, taken from the paper.

This a plot of the number of food items they collected on average, at every generation. Each curve is a different tribe of robots. Initially, they all started off hopelessly ineffective at finding food. But over many generations, small mutations crept in to their mental program that made them slightly more effective. The individuals with these mutations had the most descendants in the next generation, and the process multiplied. Natural selection was, in effect, programming them to become better foragers. Within a 100 generations, you can see a dramatic improvement in their foraging ability.

But what about their behavior? That’s shown in the figure below.

The blue, yellow and red curves correspond to 3 different robot tribes. The blue tribes are those in which the overall benefit to genes exceeds the cost of being altruistic (rB >C). In the yellow tribe the cost and benefit to genes are matched (rB = C) and  in the red tribe, the cost exceeds the benefit to genes (rBthe robots evolve strategies of cooperation that agree precisely with Hamilton’s rule [4]. (According to the rule, the yellow tribe is exactly at the threshold for altruistic behavior, and indeed they are altruistic about half of the time.)

This work is interesting to me for a few reasons (not just because robots are inherently cool). It shows the incredible power of evolution to optimize strategies with no outside guidance. The robots were never taught how to forage, or when to be nice. But in surprisingly few generations, natural selection managed to wire them with an optimal strategy.

Hamilton’s rule has been notoriously difficult to test in the field, because it’s incredibly hard to quantify the costs and benefits of helping acts. The robot model certainly doesn’t come close to capturing the complexities of navigating the real world. But it does capture the essential features, and allows one to make precise quantitative tests of theoretical predictions of natural selection.

It’s a pleasing irony that by studying the behavior of tiny robots, we can learn more about the strategies of life.

References
Waibel M, Floreano D, & Keller L (2011). A Quantitative Test of Hamilton’s Rule for the Evolution of Altruism. PLoS biology, 9 (5) PMID: 21559320 Link

If you’re interested in learning more about the subject of altruism, these are some great books on the subject:

The Selfish Gene by Richard Dawkins

The Price of Altruism: George Price and the Search for the Origins of Kindness by Oren Harman

You may also enjoy this Radiolab episode on altruism, as well a few excellent documentaries that address the subject such as Nice guys finish last by Richard Dawkins (from where I borrowed the title of this post), or Life in the undergrowth by David Attenborough.

Photo Credit

The worker bees image is courtesy Todd Huffman, licensed under Creative Commons.

Footnotes

[1] This raises the dilemma that you’re not really being selfless, because you stand to gain in the long run. But I’ll leave this one for the philosophers.

[2] Hamilton’s equation is a nice embodiment of another classic Haldane quote – “An ounce of algebra is worth of a ton of verbal argument.”

[3] This would have been prohibitively time consuming to do with the real robots. Instead, much of this work was done using simulations on a computer model that could accurately capture the interactions of the robots.

[4] Even though they are complex enough to violate some of the assumptions of the rule.