Selection in Impatiens: Moving beyond correlation

Last time I reviewed our study of contextual analysis in Impatiens capensis.  We came up with a standard result, and drew a radical conclusion.    The standard result is that Impatiens obeys the constant yield rule that Harper claims is nearly universal, and a result that had been seen in the past (e.g., Schmitt, Eccleston and Ehrhardt 1987 J. Ecol 651-665).  Basically, I argued that the constant yield law is a version of “soft selection”, and that our theoretical analysis showed that this was multilevel selection.  A result that indicates that multilevel selection is nearly universal in plants.

However, as has been amply pointed out in this blog and elsewhere regression is a glorified form of correlation, and as we all know correlation is not causation.  What methods such as contextual analysis do is that they show us that there is an association between phenotype (and contextual phenotype) and fitness.  What they do not show us is that that correlation is causal.  This is exactly the issue that Wade and Kalisz (1989 Evolution 44:1947-1955) addressed.  They raise the important point that if we want to get away from correlation and understand causation we need to do manipulative experiments.

In this view, regression analyses of fitness such as contextual analysis show an association between phenotype and fitness.  From this we posit that the variation in phenotype is causally affecting fitness.  Of course, the phenotype itself does not affect fitness, rather it is the interaction of the phenotype with the environment that causes variation in fitness.  This provides a mechanism for turning the correlational approach into a causal approach.  If we have correctly identified the agent of selection we should be able to modify that agent, and in the process modify the selection gradient.  For example, in Franks, Wheeler and Goodnight (2012, Evolution 66, 1398-1412) we reasoned that the plants varied in secondary compounds and insect damage was a significant selective agent on the plants.  We found that for several secondary compounds selection was significantly weaker in plants sprayed with insecticide than it was in unsprayed plants.  By calculating the selection gradient in two situations, with and without the putative selective agent, we were able to show that insect herbivory was indeed a causal selective agent.

Australian paperbark tree Melaleuca quinquenervia or punktree

Melaleuca quinquenervia, the Paperbark tree is native to Australia, but an invasive pest species in Florida.  It is the species studied by Franks, et al. (2012, Evolution 66, 1398-1412) (picture from

Returning to multilevel selection in Impatiens, it turns out that John Kelly did manipulative study to confirm that multilevel selection (he called it kin selection) was acting in Impatiens (Kelly 1996. 147:899-918).  In his study he used the fact that you can make Impatiens short and bushy by pinching off the apical meristem.  This removes the apical dominance and allows the side branches to grow, but of course it prevents the plant from growing any more vertically (at least until a new dominant takes over).  He set up several plots at, Kellogg Biological Station again, that differed in their light environment.  In each of these plots he set up four treatments:  (1) Unmanipulated plants; (2) the focal individual was pruned, and the neighbors unmanipulated, (3) focal individual unmanipulated, the neighbors pruned, and (4) both focal individuals and neighbors pruned. Full factorial experiments are the best aren’t they!

One of the interesting things he found is that when the neighbors were pruned (and therefore stunted) the focal individuals seed production (fitness) was significantly greater than the seed production of plants surrounded by un-pruned neighbors.

Kelly results

Fitness of a focal plant as a function of whether the neighbors were un-pruned (left) pruned (right).  (from Kelly 1996. 147:899-918)

In short, the pruning of the neighbors was releasing the focal plant from the pressures of group selection, and as a consequence the fitness was entirely determined by the individual traits, rather than the combined effects of group and individual selection.  In other words, Kelly showed that the stature of the neighbors was a causal selective force on the focal individual, confirming that the regression of contextual traits on fitness that we observed was indeed causal, and that there is group selection against large size in Impatiens capensis.

However, Kelly raised an excellent additional point.  He points out that Impatiens, like most plants, are very plastic.  As a result their size is modified by density effects and crowding from other plants.  Kelly represents this as a path diagram:

kelly path diagram

The path diagram proposed by Kelly (1996. 147:899-918).

Using this path diagram Kelly pointed out that with phenotypic plasticity you would have paths f and g.  That is the neighbor’s phenotype changes the focal individuals phenotype and vice versa.  He then goes on to correctly argue that contextual analysis cannot detect these inter-individual modifications of phenotype, thus there is a component of kin selection that contextual analysis will not detect.

This is actually an interesting philosophical point.  The phenotype is the phenotype, and contextual analysis as we did it is purely a phenotypic analysis.  Based on this the path diagram should be:

My version kelly path diagram

Encompassed in the “r2” term are all of the arrows that link the two phenotypes, that is paths a, c, f, and e of Kelly’s path diagram.  The important point is that in the genic view it is important to distinguish between “genotype” and ecological interactions.  In the phenotypic view such distinctions are nice to know but not necessary.  Both are part of the transition equation that gave rise to the focal plant’s phenotype.

It also shows a different and important point.  We can redraw the left half of Kelly’s path diagram as follows:

left half of kelly path diagram

I moved the focal plant phenotype to the right and dropped the g arrow to make my point clearer, but otherwise it is identical to the right part of Kelly’s diagram.  He measured the focal plants phenotype, so it IS that individuals phenotype, further, if selection is acting solely on the individuals phenotype we have to call it “individual selection”.  However, (and this is a big however) just because it is a trait measured on the individual, does not mean it is a trait solely of the individual.  In this case the plants phenotype is determined by a number of factors only some of which are intrinsic to the focal individual, driving home the point that we need to distinguish between selection and inheritance.  From a phenotypic perspective contextual analysis is not a problem.  Rather it is kin selection, with its conceit that our genes are some how qualitatively different than other forces affecting our phenotype, that is the problem.

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