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.