Reconciling continuous and discrete models of C4 and CAM evolution.

Abstract

A current argument in the CAM biology literature has focused on the nature of the CAM evolutionary trajectory: whether there is a smooth continuum of phenotypes between plants with C3 and CAM photosynthesis or whether there are discrete steps of phenotypic evolutionary change such as has been modelled for the evolution of C4 photosynthesis. A further implication is that a smooth continuum would increase the evolvability of CAM, whereas discrete changes would make the evolutionary transition from C3 to CAM more difficult. In this essay, I attempt to reconcile these two viewpoints, because I think in many ways this is a false dichotomy that is constraining progress in understanding how both CAM and C4 evolved. In reality, the phenotypic space connecting C3 species and strong CAM/C4 species is both a continuum of variably expressed quantitative traits and yet also contains certain combinations of traits that we are able to identify as discrete, recognizable phenotypes. In this sense, the evolutionary mechanics of CAM origination are no different from those of C4 photosynthesis, nor from the evolution of any other complex trait assemblage. To make progress, we must embrace the concept of discrete phenotypic phases of CAM evolution, because their delineation will force us to articulate what aspects of phenotypic variation we think are significant. There are some current phenotypic gaps that are limiting our ability to build a complete CAM evolutionary model: the first is how a rudimentary CAM biochemical cycle becomes established, and the second is how the 'accessory' CAM cycle in C3+CAM plants is recruited into a primary metabolism. The connections to the C3 phenotype we are looking for are potentially found in the behaviour of C3 plants when undergoing physiological stress - behaviour that, strangely enough, remains essentially unexplored in this context.