Family roots

Experiments in which related and unrelated plants were grown together reveal the ability of roots to recognize their kin. The ecological and evolutionary implications are tantalizing topics for future studies.

Knowing who are your relatives and who are not creates behavioural, ecological and evolutionary opportunities. Organisms capable of recognizing kin can adjust territories, avoid incestuous mating, decide to fight or not and, importantly, benefit evolutionarily from promoting the success of brothers, sisters and cousins — individuals that share their genes. Kin recognition is widespread in animals that recognize relatives by sight, hearing, smell and even taste. Dudley and File¹, writing in Biology Letters, now demonstrate that plants can also recognize their family members — through their roots.

Plants do not see, hear, smell or taste. But they communicate with each other in other ways, including chemical signalling among roots²; unknown mechanisms for pollen–stigma recognition; chemical signals between parasitic plants and their hosts³; volatile molecules emitted as warning signals by leaves damaged by attack⁴; gases in smoke from burning plants⁵; and neighbour-altered light-wavelength ratios⁶. Some of these communication techniques function to discriminate between self and non-self⁷, and between members of the same population and those of a distant population⁸. However, unequivocally documenting self versus non-self recognition has proved difficult⁹, and clear demonstrations of recognition of relatedness among plants are still rarer. If plants, like animals, can distinguish related non-self from unrelated non-self “and adjust their behaviour on the basis of kinship”¹⁰, thereby enhancing the prosperity of close relatives, their genes might preferentially be passed on to future generations in a process known as kin selection.

But to do this, kin must first be distinguished from strangers. A plant called the Great Lakes sea rocket (Cakile edentula; Fig. 1) seems to possess this ability. Dudley and File¹ found that, when individuals from the same mother were planted together in a pot, the total root mass produced was less than when individuals from different mothers were planted together. It is not clear whether kin-recognizing siblings reduced their own root growth, or whether unrelated individuals aggressively increased root growth to seize resources in a 'tragedy of the commons' scenario¹¹. Either way, roots of the sea rocket responded differently to kin than to strangers. A possible result of lower root mass in the presence of kin is less root overlap, which could mean less competition for resources among kin than among strangers.

Figure 1: The Great Lakes (or American) sea rocket, Cakile edentula

D.DITCHBURN

Dudley and File's experiments¹ on root growth show that kin recognition occurs in this species. Whether kin recognition translates into kin selection in sea rocket remains an open question.

Root behaviour⁸, overlap and competition were not directly measured by Dudley and File, however, leaving the ecological and evolutionary consequences in question. As Hans De Kroon remarked to one of us, for kin recognition to be interpreted as kin selection, one must demonstrate that recognizing kin results in increased progeny among the group of relatives — that is, in increased fitness. The plants in Dudley and File's experiment showed no such reproductive increase, but this may have been because they were grown in pots. Pots can be good for detecting root recognition but they are lousy for assessing a plant's full growth potential. Avoidance of root overlap, as a consequence of recognition, requires space, and space is severely restricted in pots.

In a natural field setting, however, a plant detecting neighbouring kin at low densities could decrease root growth in the vicinity of neighbours and increase root growth away from them, thereby decreasing root overlap and competition for resources and increasing its performance. In support of this possibility, other research on sea rocket has shown that, in the field, groups of siblings have higher reproduction rates than groups of strangers¹². By demonstrating kin recognition, Dudley and File have taken the critical first step; measuring the fitness consequences should be comparatively routine.

Kin recognition is sometimes linked to altruism, but reduction in root growth and overlap among sibling neighbours may not be purely altruistic. By detecting family members and sharing space with them, sea rockets may simply be ensuring that direct competition for resources does not suppress all members of the group. Competition among densely spaced individuals could result in a limiting resource being spread so evenly among relatives that no individual acquires enough to reproduce. This would be a disaster for an annual species such as sea rocket. On the other hand, kin recognition accompanied by inhibition⁸ of neighbouring roots may constitute a formidable interference mechanism that would allow plants to form large enough territories¹³ for the successful growth and reproduction of some family members at the expense of others. Kin recognition, therefore, may not directly benefit all members in a family. But it may increase the odds that at least a few members will successfully pass on the family genes to the next generation.

Without brains, how do plants recognize their relatives? No one knows. Possibilities include communication through chemical exudates, released volatile molecules, electrical signals, and enzymes functioning at cell surfaces¹⁴. Research on a desert shrub, Ambrosia dumosa, suggests that root interactions may involve at least two levels of recognition and interplay among physiological and genetic components. At the self versus non-self level, roots on the same individual shrub did not inhibit each other upon contact, whereas roots from genetically identical but physically separated individuals did¹³. At the population level, roots on different plants from the same population inhibited each other, whereas those from different populations did not⁸. In addition, recognition and response probably constitute two different mechanisms, because studies on other species have found, in contrast, that self-recognition can lead to inhibition¹⁵.

Clearly, research on root behaviour is just beginning. But if neighbour identity commonly dictates root interactions, major overhauls of theories that assume that direct resource competition determines plant community organization will be necessary. And if kin recognition among roots can be unequivocally linked to evolutionary consequences, we will have to expand the pool of mechanisms known to drive plant evolution.