Wednesday, December 3, 2014

Rhododendron walks into a bar...

By Anne Buchanan and Ken Weiss

Plants may be stuck in one place, but they aren't just sitting there twiddling their thumbs.  That they respond to environmental cues has long been known, of course, and the hormonal and molecular mechanisms for responding to light, temperature, moisture and so forth are well-established.  Some responses evoked by one part of a plant, such as attack by predator, can communicate to other parts or even to nearby plants.  But it has only fairly recently been suggested that plants are also able to recognize kin, and respond differentially, and in ways that enhance reproductive fitness, to the presence of plants to which they are closely related.

Among other reported indications of kin recognition, plant roots have been found to grow more in the presence of 'strangers' than 'kin'; kin recognition is said to be via root-derived cues, though that this actually happens is not without controversy, primarily because the molecular mechanism has not been identified (from 'Shedding light on kin recognition response in plants,' New Phytologist, Bias, 26 Nov 2014).  But now a new paper ('Photoreceptor kin-recognition among plants,' New Phytologist, Crepy and Casal, 29 Sept 2014) describes a possible mechanism for kin recognition among Arabidopsis thaliana, or mustard weed, the most frequently studied model plant.

Crepy and Casal did a series of experiments growing Arabidopsis plants in pots, to eliminate the possibility of confounding cross-talk between root systems, in variations on the theme of single genotype or mixed genotype rows, with plants either surrounded by kin or non-kin.  They also included mutant plants with known responses to different light waves, and plants of different ages, all exposed to differently filtered light sources.  They were interested in whether there were effects of proximity to kin, which they measured in terms of how close leaves were to neighboring leaves, or how much light fell on each leaf.  The idea was that kin don't compete over pools of light, but instead allow their relatives equal access.

Bias writes:
Crepy and Casal showed that plants recognized their kin neighbors by horizontally reorienting leaf growth compared with the interactions with the nonkin members. The authors also showed that the mechanism that led to reorientation of the leaf with kin members was regulated by phytochrome B and cryptochrome 1. The work by Crepy and Casal provides the first molecular evidence of the way in which plants respond to kinship.
They also showed that plants that interacted with kin produced more seeds than plants growing among strangers, "a clear indication of mutual benefit and cooperation."

From Bias, 2014;
'Aboveground and belowground interactions in plants experiencing kin and nonkin members.'

Have Crepy and Casal demonstrated beyond doubt that plants recognize kin?  Probably not; it has been controversial, and will surely remain so.  For one thing, there needs to be a convincing mechanism for recognizing what 'kin' means, and this is a serious issue both practically and theoretically.  In animals, with their various pheromones and highly variable immune/identity systems, the latter of which can be highly variable because mutations accumulate rapidly, various receptors and detection systems, also part of the system whose function is in mating or immune defenses, recognition of close molecular similarity in these aspects of the genome would be called 'kin'.   Plants also have high-variability immune-like systems for detecting invaders but whether they monitor this for self or self-like patterns is something we, at least, don't know.

It will take much beyond this rather limited study before any serious evolutionary geneticist will be completely convinced.  This is, in part, because authors must show beyond a reasonable doubt a molecular means specific enough to detect and evaluate the degree of kinship rather than just same-species or locally same-environment, both of which could affect many aspects of plant molecular biology.  Can a plant tell a clone from a cousin, say?  Finding such evidence has proven generally to be a very tall order, but of course that doesn't mean the Crepy and Casal finding is wrong, but it does need to be viewed with circumspection until details are known, because empirical findings like theirs can have multiple explanations.  The reason is not hard to see, and it seems there are some semantics involved, with the meaning of the term 'kin'.

The basic idea and rationale of kin selection
The main underlying idea that makes this of any interest has to do with altruism.  Helping any other organism may be at your own expense, and put you at a reproductive (and hence evolutionary) disadvantage if, say, it costs energy to help the recipient gain resources that lead to its greater reproduction when you could be putting that energy toward your own reproduction.  If that's the case, the genetic variants that lead you to do this won't proliferate as much as the recipient's. The explanation offered mathematically by William Hamilton over a half-century ago was that if your aid to a relative of a given degree -- and this is where 'kin' comes in -- must lead the recipient to reproduce more by a factor at least as great as your direct kinship relationship in order for the behavior to evolve.  In animal terms, you share half your genome with your sibling.  If you lose an offspring because you helped your sib, s/he must produce more than 2 additional offspring as a result of the help -- that is, in the next generation (on average) there will be at least as many copies of the altruism-inducing variant. If the recipient is of a more distant degree of relationship, the advantage must be much greater than just 2 for 1. 

Hamilton's rule was for decades a kind of cult religion among strong evolutionary determinists looking for precise natural selection everywhere.  To be fair, it also was a response to accounting for the evolution of what seemed like self-defeating behavior, to counter a heretical argument that invoked 'group selection', that organisms could evolve behavior that was self-limiting if it was good for the group.  This was heresy in the sense that it went against the rugged individualism of arch-Darwinism -- and mathematical analysis showed that was a more problematic phenomenon to account for.

However, careful quantitative ecological genetic studies have generally not supported the idea as of much practical applicability except in unusual circumstances.  On the other hand, in general if you help another member of your species, relative to other species, or if because you drop your seeds near where you live, your neighbors are  your relatives, then such behavior is easier to understand and doesn't require great precision -- for example, you don't have to have a mechanism for genotyping your neighbor, as you effectively do under Hamilton's rule.  If your neighbors are your relatives, helping is OK, and this can be so even if it's just within species if you are (or your ancestors at the time the helping mechanism evolved were) locally reproducing.

Likewise, if you compete for soil nutrients or sunshine with other plants where you live, it can in principle at least (this needs to be shown quantitatively) mean that you're better off by helping your species members rather than some other species.  Again, in the Hamilton's rule sense they share your genes far more than other species do.  These sorts of things can in principle account for the kin-recognition in plants that this paper refers to: it does not have to be testably close kin.

In this case, we think that the Crepy and Casal idea seems to have rather misleadingly used the term 'kin', not to refer to close family relationship of known degree but to what amounts to more distant group relationship.  Distant groups should not be referred to as 'kin' in this kind of situation because its connotation can be unclear.  After some variation has accumulated, it is clearly reasonable to ask whether similar molecular physiology might induce similar responses, or cross-reactivity, in those from the same group compared to those from a distant group.  No evolutionary kin-rule selection of the precise Hamiltonian kind need be involved.  In the wild, ancestrally, neighbors are kin.  In this case, if the story holds up, one will want to know how these particular genes effect such cross-reactivity.

Is it a perfect good?
But let's say that Crepy and Casal have demonstrated that plants help their kin.  And that kin recognition is an unalloyed good, with demonstrable fitness benefits.  As they point out,
Preferential helping of relatives has been observed for a wide range of taxa. For instance, in vertebrate (bird, mammal) species, helpers preferentially aid closer relatives during breeding (Griffin and West, 2003). In the social amoebae Dictyostelium discoideum, cells cooperate preferentially with relatives and aggregate to form multicellular fruiting bodies (Hirose et al., 2011). In humans, as the cost of helping increases, the share of help given to kin increases, whereas that given to nonkin decreases (Stewart-Williams, 2007).
The assumption is that the more closely related organisms are, the more likely they are to cooperate.  That is, increasing the reproductive fitness of one's kin is good for one's own fitness.  The reason that kin selection has been, and continues to be a hot topic in human evolution is both that it confirms hyper-darwinian fine-tuned selection, which many hold as fervently as a religion, and that it accounts for cooperation without being culturally wishy-washy (as they'd see it), and that there should be a mechanism to account for its evolution; note of course, that mechanism needs to be quite specific to define 'kin', which cannot just be assumed (as we outlined in the previous section).  But we, at least, have plausible molecular-genetic means of detecting close kin.

But people aren't plants, or dictyostelium.  We also have culture, and it can powerfully affect our behavior, so that what makes sense evolutionarily for other organisms doesn't always apply to us.   For one thing, culture allows us to assign relationships symbolically rather than just genetically.  We can imagine what 'success' may mean (e.g., getting to heaven), which goes beyond mere Darwinian proliferation.  We can form clans or other structures based on all sorts of criteria, not just genetic relationships. We don't always optimize our own fitness.  Humans are the only organisms that abort their own fetuses, that blow themselves up in support of an ideal, that have civil wars, killing people in fact most closely related to them. But humans also rescue strangers from drowning, and grow food to be consumed by people across the world.

We can devise all the equations we want about kin and fitness, and we can calculate the heritability of this trait and that, to show that behavior is genetically determined, but our thinking brains, and the power of culture trump those rules.  Members of Homo sapiens simply are not just bags of 'selfish' genes, and meaning isn't just reproduction.  We're not nearly as hard-wired for behavior as many other 'lesser' species of animals and plants are often (correctly or incorrectly) assumed to be.


D G said...

Depending on "thinking" brains to save us from ourselves is living life on the edge. But hey, it's all we've got.

Ken Weiss said...

I'm usually more of a pessimist, but I think that depending on thinking brains, that can assess a situation and choose among options, is far better than being hard-wired. It has made us the hugely adaptable species that we are. Hard-wiring makes a species quite vulnerable to environmental change.

Of course, this is short-term and our abilities may in the longer term do us in because we so clearly trade the present solution for long-term solutions.

D G said...

If we are hard-wired to avoid the middle and choose one side or the other then your pessimism is justified.

Holly Dunsworth said...

This is a comment to the piece, not the above:

I love this today and you know why, Anne.
Yes, fictive kin... essentially friends that we consider family... muddy all this. Plus, how much cooperation during my lifetime actually contributes to my sibling's fitness? Which instances of my cake-baking and CPR do we tally up and credit in our kin selection equations? To me, this makes this whole thing, even in plants, more story-telling than testable-hypothesis generating. Sure the story sounds good but how would we ever know if it's no good? It's gonna be tough. In the meantime, love the ones your with. And beyond...

Holly Dunsworth said...

(oh I hope no anthropologists out there are cringing at my sloppy use of fictive kin! Apologies :))

Anne Buchanan said...

Exactly! (Another love letter to you, Holly!)

Anonymous said...

"But people aren't plants, or dictyostelium. We also have culture, and it can powerfully affect our behavior, so that what makes sense evolutionarily for other organisms doesn't always apply to us."

Human exceptionalism?


Anne Buchanan said...

But Manoj, shouldn't we take culture into account when thinking about human evolution? As far as we know, plants don't kill kin on holidays, or wage civil war, or abort developing buds. Otherwise, you're saying humans are hard-wired. Which would mean, among many other things, that we have genes for doing calculus.

Ken Weiss said...

In this regard humans really are exceptional, essentially unique. Symboling and its various abstractions may exist in other animals but that has never led to anything close to the cumulative, symbol-based phenomenon of human culture. Humans born naked in the woods wouldn't perhaps seem so exceptional, but we are born into the cumulative, heritable cultural environment. In that sense what we are adapted 'for', however it started, is unique.

Anne Buchanan said...

So, a commenter (DG) wrote this:

"In a very short time I have come to see that y'all are excellent, top notch writers. However, this needs a total re-write:

The reason that kin selection has been, and continues to be a hot topic in human evolution is both that it confirms hyper-darwinian fine-tuned selection, which many hold as fervently as a religion, and that it accounts for cooperation without being culturally wishy-washy (as they'd see it), and that there should be a mechanism to account for its evolution; note of course, that mechanism needs to be quite specific to define 'kin', which cannot just be assumed (as we outlined in the previous section). IMHO"

I can't tell you how confusing this was. Finally, I understand that it's the English that's the problem here, not the thought. Here's a stab at clarifying the point:

Kin selection is the idea that we'll behave in ways that enhance the reproductive fitness of our relations, in ways proportional to the degree of kinship, even if it is detrimental to ourselves. It is the subject of heated debate in evolutionary biology, though it has not stood up well in actual direct empirical tests. Nonetheless, the idea persistently appeals to hyper-Darwinians, people who believe that every trait has to have a specific adaptive explanation. Kin selection accounts for behaviors that seem problematic otherwise, in particular cooperative behavior and altruism. Altruism is a problem for strict Darwinians because it doesn't directly differentially optimize the altruist's own reproductive fitness relative to his/her competitors in the population. Kin selection, and to many, Hamilton's rule, is the mechanism that accounts for this.

DG said...


I think this new paragraph is excellent. I had almost worked through the other one.

Yes, if English is one's 2nd language, understanding can be a problem sometimes.

DG said...

"the larger point is to keep in mind that environmental exposures may have unintended, unconsidered, unmeasured or even unmeasurable consequences” This is from the new post and it impelled me to make a comment about blog communication. I put it here because I don’t want to interfere in any way with the solicitation of information on Ken’s premise.

I am of the opinion that the blog where the author responds to commenters (and commenters to each other) will be on par with going from picto-graphs to words. Blogs are a sliver of the history of written communication. Written communication is a sliver of human communication. We are in a sliver of a sliver. For x number of years(K,M?) we could see the other people. All the non-verbal information was there for us. What does our brain do with a blog post without all those non-verbal cues that it has relied upon for x number of years? How does it evaluate motivation, deception, etc? It guesstimates. It fills in the blanks. We know that it does that with visual perceptions. What if it is a general rule? Inputs not available;guesstimate. Fill in the blanks. Does it have a template or formula for retrieving the fill-in information? Our brain tries to squeeze the other inputs out of the one input (words) that it has. This forces the communication error rate up,and that is why it is so easy to fire off an emotionally instigated comment, only slightly restrained and modulated by cognition.

DG said...


Thanks so much for the time spent on the re-write. I am trying to have a light bulb moment and this brings me closer. Would you thought check my paraphrase?

Some evolutionary biologists will not accept the idea of altruism and cooperation unless it is forced through the Hamilton rule. Other scholars do not accept that rigid and inflexible approach and propose that there are other mechanisms that can explain altruism and cooperation.

Assuming that my paraphrase is correct, it explains to me how people who already have a certain strong religious strength political ideology would use the hyper-Darwinian side as a “proof” to support their ideology.

Ken Weiss said...

Reply to DG
All people, even scientists are vulnerable to what we call 'tribalism' and basically to ideology, despite our self-belief that we are objective. We have many different personal, career, and other interests, and they are affected by our culture, etc.

It is also easier to take a strong position than to insist that things are less clear. The biological challenge is to explain, in totally materialistic terms, how complex traits and diverse species got here. When such seemingly self-impeding behavior as altruism is observed, it raises the need to account for it, again in material terms. Simple Hamilton-rule types of explanations are rife (we just heard a seminar this week rather thoughtlessly invoking it as if it were, so to speak, the God's truth.

So the challenge is to try one's best to be dispassionate and discuss, study, think about what the real world is actually like. Doing that, if one does not venture off into theological explanations, one is forced to think about these sorts of traits and to envision they could come about.

Hamilton's rule is an equation that is necessarily true if the conditions are true, but that does not mean that if conditions are not just that way that the same sorts of behavior might not evolve in other, or modified ways.

EO Wilson, a strong purveyor of Hamilton's ideas way back to his Wilson's Sociobiology, as had recent second thoughts, and many others have as well. So there is much to think about and no clear answers except that there must exist such answers, even if they are not unitary.

DG said...

Thanks for your additional exposition, Ken. Your thoughts and comments deserve as wide a distribution as can be obtained.

I share your enthusiasm for reasoned debate. It does seem that such debate is on a downslope. Another problem is that when one or both sides deny the right of the other to exist, reasoned debate is not an option. I will leave you do battle with the other side (and choose your side) on the terms of scientific inquiry. I have faith in the ability of science to right itself.

My thoughts and selfish concerns lie with understanding the interface between scientists and us common folk. Common folk usually choose sides based on the political stances of the involved scientists. I guess the reasoning is that if the scientist is smart enough to get his or her politics right then they will be smart enough to get the bulk of their field of study correct. I am not confident of the validity of that idea.

Everyone might not be as fearful of the consequences of this politicization of science as I am. The gulf between the politics of the educated elite and the common folk is so wide as to be almost unbelievable. One problem is that the left, by its nature, cannot effectively deal with the pervasive anti-intellectualism of the common folk. On the other hand, the right benefits from this anti-intellectualism, and encourages it.

This process of polarization seems to be aided and encouraged by the on-going changes in the ways by which we communicate. The continuing collapse of the journalism ideal of balanced reporting and the shrinkage of the number of outlets for such reporting is not a good sign. I hope that most of my pessimism derives from the fact that I am operating from an n of 1, as Holly put it.

I think I correctly recall that in a comment Anne put forward an idea on how to change minds that I labeled in my mind as the raindrop premise. Keep up the gentle rain.

Ken Weiss said...

Thanks. It has ever been thus. Those in power or of influence, often from a privileged class to begin with, have their viewpoints and they are often not entirely neutral relative to self-interest.

But at least as importantly is the iron cage of history (to paraphrase the sociologist Max Weber about bureaucracy) that affects if not channels how we think, the questions we ask, how we act relative to our intended goals vs our vested interests, and so on.

As Atun Gawande has put it recently (see an upcoming post) there is a role for people in the 'disturbance business', to raise questions, to ask what clothes the Emperor actually has on, but also whether there really is an Emperor in the highly-displayed clothes.

Science needs to be challenged, from within (each scientist by others and by him/herself) as well as by the public. If we can't justify what we do and yet expect the public to support it, then the public shouldn't.

But 'ordinary' people can be given to understand what we are doing and what we can legitimately promise, and given a say in what our priorities should be, etc.

Of course, the reality is largely about power and privilege and leverage and so on, as well as about the facts of Nature, so these issues are never completely simple or clear.

Anne Buchanan said...

Thank you, DG. I would just say that it's not just non-scientists who choose sides based on the politics of the proponent. It has been said that you can tell someone's politics by where they come down on genetic determinism, but it's also true that you can tell someone's view of genetic determinism when you know their politics. This has gotten fuzzier now, as genetic determinism has become more accepted by so many, but I'll still make the point.

But that doesn't speak to your point about a gulf between scientists and non-scientists, and the politicization of science. I agree, and share your concern.