Darwin built his theory of Evolution on two pillars, “heritable variations” and “survival of the fittest” by which occurs evolution by the means of natural selection. How did the heritable variations move from one generation to the next? The genes (we know that alleles) carry the variation in the parents to their offspring. Survival of the fittest, said that the organism with the most advantageous trait or character survived, at intra- and inter- population or species level. So what generates the variation and the chance of survival or adaptability?
At the molecular level we know about mutations, which are stabilized in the population or species ( then called substitutions), can be a reason for variation. We are aware about the neutral theory of evolution pertaining to the genome level or molecular level. Wherein we learned that most (deleterious) mutations are “purified”, and the variation at the genetic level is as a result of random fixation of mutations or random genetic drift. The evidence for this is that if natural selection was the reason for the genetic level variation then the key genes responsible for the functions would be evolving faster (fix more mutations/carry more substitutions since they are advantageous and are naturally selected) but this is not the case, key genes always are same between organisms say at an evolutionary scale of metazoa for example. We should not confuse that there is no positive selection or fixation of advantageous (?) mutations in key genes, it is present but to a smaller extent as opposed to the neutral (or nearly neutral) evolution, it can be episodic events in most cases for key genes.
Another set of variation at molecular level could be due to expression differences, in time (heterochrony), in cells (heterotopy) and in amount (heterometry). But are these the only source of variation? if so (so much variety) what we see, how could we explain it? We should understand that the variation in morphological traits, physiology and behaviour is guided by natural selection and that neutral theory (or nearly neutral theory) pertains only to the molecular level. Apart from these mutation and expression level variation, there are other sources as well, the epigenetic variations, the phenotypic plasticity and the symbiont variation that can be selectable and indeed heritable, which is what the paper of our interest today says.
If the symbiont or (microbiome) of the organism and its genome are in intricate connection (then they can be considered the holobiont) then evolution of the organism cannot be separated with the co-evolution and co-development of its microbiome. Nature has examples for horizontal and vertical transfer of symbionts between generations. The symbiotic association of the luminiscent Vibrio fischeri on the ventral side of the squid Euprymna scolopes is an example of horizontal transfer and association of symbiont. We know this association is crucial for the survival of the host (to avoid predators) and the symbiont benefits by getting a safe place to live in. The cases of Wolbachia in arthropods (wasps) are perfect examples of vertical transmission of symbionts wherein the eggs contain the bacteria and any egg (treated) without the bacteria perishes or fails to develop. As we look deeper, even human guts harbor these kind of symbionts without which we would not be able to survive and is transmitted vertically from mothers. So should be every case of each and every organism, but proof is lacking since investigations in that angle is just gaining momentum.
Selection (natural selection) of the symbionts associated with the host due to environmental cues are presented in the paper as well. They present the case of coral-zooxanthillae symbiosis and selection of a specific strain of the microalgae in response to elevated temperatures to form the dominant community. The temperature tolerance of desert plants (and many other plants) and the inhibition of the HSP 90 (for temperature tolerance) is provided by external cues provided by symbiotic fungi, the paper provides a strong case of selection of the holobiont in response to the environmental cues. The aphid thermal tolerance is also an interplay between its symbionts (Buchnera being prominent), and this interaction can be disrupted by mutations, showing that the interaction is really selected for.
Reading the paper enables us t0 appreciate the importance of the symbiont in the development and evolution of organisms. Evolution and development is related to the environmental conditions the ecological interactions, the opportunities in environment can lead to adaptions, symbionts fits in nicely as a co-evolving component stressing the view that organisms are not individual units but interdependent. The molecular level selection forms the micro-level, the symbiont and selection forms the intermediate level and ecological interactions and external cues forms the macro-level, of adaptation, developmental variability and eventually evolution.
Scott F. Gilbert, Emily McDonald, Nicole Boyle, Nicholas Buttino, Lin Gyi, Mark Mai,Neelakantan Prakash, and James Robinson, 2010. Symbiosis as a source of selectable epigenetic variation: taking the heat for the big guy. Phil. Trans. R. Soc. B, 365:1540 671-678.