Adaptive Assumptions

I recently read a thought-provoking Eco-Evo Evo-Eco blog post based on the idea that adaptation and constraint can be equally good at explaining change depending on how "deep" within a population you search (i.e. within or among species):

Thesis of the post: "...for functional traits, null hypotheses for variation among species should be adaptive ones (such that the non-adaptive hypothesis bears the onus of proof), whereas null hypotheses for variation within populations should be non-adaptive ones (such that the adaptive hypothesis bears the onus of proof)"

I can see how this would make sense. I suppose it is more likely that differences between two separate populations are caused when each adapts to its separate environment. It seems this would only apply for allopatric populations. On the other hand, if there are differences within a population, you could argue it is more likely that this is just due to random variation or phenotypic plasticity. So the null hypothesis for differences between populations is that they adapted to different environments, and the null for differences within populations is that they have plastic traits. 

I feel this conclusion largely relies on the assumption that allopatric speciation is simpler and much more likely to occur. Which may not be the case. As one commenter put it: "Simplicity always has to depend on the context and is therefore not general."

Why couldn't some Mytilus californianus in a group adapt 

and change more than others?

 Why couldn't there be speciation within a tight cluster 

of Pollicipes polymerus?

Yesterday, on the beach, I was discussing possibilities of evolution between tidepool populations with a friend and how dispersal is basically infinite when the tide comes in. All species can disperse gametes and larvae into the ocean and boom!, essentially infinite dispersal. (This depends on the currents that are depositing the gamestes/larvae, of course. The ocean is not just one big toilet bowl, swirling everything together.) With infinite gene flow, it is hard to develop reproductive barriers that could lead to evolution. After I mentioned this to him, my friend commented, "ah, so they could only speciate sympatrically, then." I had not thought of this. Might all tidepool organisms speciate within populations? This would certainly be a counter example to the above hypotheses. 
This idea is not fully developed in my head yet, but it is something to think about! Thanks, Joseph.

Mytilus californianus 

covered in Balanus glandula

Anthopleura xanthogrammica