Show me the cheaters!

What would you do if your partner cheated on you?
 
Probably you’d break up, end the relationship, and tell all of your close friends and maybe even your Facebook friends about what happened.
 
Your motivation for sharing this info might not be to decrease the chances your ex could cheat on someone else.  But if the story of your breakup went viral, your ex would gain the reputation of being a “cheater”, and maybe others who would normally swipe right would now begin to swipe left.
 
In biological terms, the cheater might miss out on future mating opportunities. Bummer for him or her.  Those not tagged as cheaters more often get to Netflix-and-chill while the cheater just Netflix's.
 
So the tables would be turned, and the “cheating life” would have back-fired on the cheater.
 
Well, this is the case in many of the sitcoms I’ve seen.
 
And it is also the trend in my scientific research in the field of mutualism - the study of how two or more organisms of different species exist in a relationship in which each individual benefits from the activity of the other. In my field, the term “cheating” refers to an individual that does not pay the cost of a mutualistic relationship, and therefore, engages in activity for personal benefit at the expense of its partner.
 
In our personal relationships, we might be moved to call the cheater “a parasite,” “a worm,” or worse. But, biologically, even though cheaters might seem indistinguishable from parasites, there are distinct differences.
 
Cheaters have, or recently had, the capacity to be good, like that seemingly great girlfriend or boyfriend - cooperation is or recently was in their cards.
 
But, in contrast, cooperating and being a good partner, so to speak, was never in the parasite’s deck - that tapeworm never wanted to be your friend. Rather than doing what nature intended, cheaters just fail to cooperate and fail to be loyal. But they are not just duds that fail at everything (we would call those kinds of individuals defective) - no, what makes cheaters some of the most famous, or infamous, players in the mutualism world is that by not paying the cost, cheaters are expected to gain an even greater benefit compared to a legit mutualist, and thus seem, for a while, to be #winning. They seem to be positioned to outcompete their faithful mutualist counterparts, and dominate the system of interactions.
 
But if everyone was a cheater and cheaters replace mutualists in a mutualism world, well, you no longer really have a mutualism. Because of this threat to mutualism evolution, cheaters have been given a lot of attention by people like me who are interested in this discipline.

And here, we – me and people in my field - face a familiar scientific problem.  We have expectations, and then there are facts (not alternate facts, rather the kind that stand up to rigorous study and force us to question our presumptions).
 
Unlike parasites that can be found throughout the natural world and are easy to identify,  cheaters are elusive. One reason that they could be hard to find is because when cheaters evolve, gain strength, and become obvious, the mutualistic relationship disappears and is laid to rest in an unmarked grave. Without nano-sized time machines, we can’t go back and witness these events as they happened.
 
So, we search for contemporary cheaters in action.
 
But where are they?
 
SHOW ME THE CHEATERS!

The fact that it’s hard to find cheaters might simply mean that cheating is not always the best strategy for life.
 
We believe that either the consequences of cheating make it unattractive or there are mechanisms in place that prevent it from even happening in the first place.
 
Using the above sitcom scenario, imagine if every “cheater” had to get a tattoo of the word permanently across their forehead - you could actively avoid them if that were the case. Other mechanisms couple the effort you put in with what you get back - if you put in less, you get less in return - so there isn’t much of an incentive for not giving it all you got. And if the good partners are somehow favoured, the bad ones become harder to find, while the ugly ones went extinct a long time ago.
 
So what are these cheater-identification mechanisms IRL?
The ones I’ve been preoccupied with involve rewarding good over bad partners, which I refer to as preference traits. To use an actual example, leguminous plants are known to form more associations with “good” partners, namely, nitrogen-fixing bacteria also known as rhizobia, while they leave-out or associate less with “bad”, non-nitrogen fixing rhizobia. Similarly, when they do associate, legumes can direct more rewards, or sugar in this case, to more beneficial rhizobia that fix more nitrogen, while those that fix less nitrogen are rewarded less. The net result of both traits is that good rhizobia receive more rewards, while bad rhizobia receive less rewards and thus, do not gain the upperhand in the mutualism.

What we don’t know is how these preference traits evolve. One hypothesis is that because cheaters, or non-nitrogen fixing rhizobia in this case, are expected to be so harmful, legumes are under selection to avoid or punish them; legumes that are better able to do so outcompete those that cannot, and so these preference traits spread in the legume population (hooray for natural selection!).

Another hypothesis is that preference traits originally evolved for another purpose, and it just so happens these traits have the effect of rewarding good over bad rhizobia.

For example, legumes can acquire nitrogen from multiple sources, not just that fixed by rhizobia. If you’ve ever been given flowers for a special occasion, you probably had to add manure or were given a packet of fertilizer to grow your plants, both of which are high in nitrogen. In a natural environment, nitrogen is often present in the soil, but it’s usually quite patchy - there are clumps of it scattered throughout the soil. Because of this patchiness, plants have evolved ways to seek-out and grow their roots directly into patches of nitrogen in the soil, a trait also known as root foraging. So, it could be that a legume’s ability to preferentially allocate rewards to nitrogen-fixing rhizobia is linked to its innate ability to forage for nitrogen in the soil. The difference between this hypothesis and the one above is that cheaters are not the selective agent that gave rise to preference traits - rather it’s that because plants have to cope with patchiness in the soil, they already have a mechanism in place to respond to nitrogen via root growth, and this mechanism just so happens to preferentially reward N-fixing over non-N-fixing rhizobia.

So which hypothesis is correct?
Well, my research to date (Batstone et al. 2016) suggests that neither of the above hypotheses are correct - so this was a trick question.
 
Our current working hypothesis is that rather than to exclude or punish cheating rhizobia, preference traits may have evolved to take advantage of effective N-fixing rhizobia. This conclusion is based on the fact that rhizobia that fix less nitrogen do not really seem to negatively affect their plant host, whereas rhizobia that fix more nitrogen have a highly beneficial effect on their host. In fact, legumes that form more associations with better rhizobia grew larger compared to plants that formed less of these associations.
 
So what??
So, why was it worth it for me to spend three years in a growth chamber trying desperately to get plants to grow their roots into two perfect little sections and at the same time prevent contamination from any other rhizobia that happened to be present in the water, soil, air, fire - yes all of the elements. I have often asked myself this question. First, I did get a publication out of it, ;). Second (and more importantly), we are only beginning to grapple with the problem of why our expectations about mutualism and cheating do not seem to hold up to what is observed in nature. Whether the disproportionate attention on cheaters is warranted or not, theory based on cheating has really inspired a whole new way of thinking about the problem, as we identify the mechanisms that prevent cheaters (if they do exist) from gaining the upperhand in a mutualism.
 
In other words, it seems we have only uncovered the tip of the iceberg that is mutualism evolution, and so there is still so much to explore and understand, making a future career in the field ever more enticing – for me.

If you’re looking for a moral to the story, it would be that rather than cheating, we should all strive to be better partners – give each other more flowers and help them grow.

The end.

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