On the evolution of blind cave fish.

Astyanax mexicanus cave dwelling form.

Evolution requires variation in traits among individuals to act. If evolutionary fitness is determined by a given trait, and everyone in a population has the trait, then there is no basis for natural selection to discriminate among individuals. Furthermore, when variation does exist, it must be genetically based so that it can be passed down by successful parents to their offspring. The trait variation on which selection acts can either come from genetic variation existing in a population before selection begins or it can result from new mutations. Because natural selection acts to eliminate unfavorable variation, there is a question as to how selection in a changing environment could reverse change, or remove a trait it had previously favored. Where would the necessary variation come from?

One controversial hypothesis is that genetic variation for a given trait can be masked from selection by very stable (or “canalized”) developmental processes. These canalized processes result in highly uniform traits within a population despite underlying genetic variation. Under certain environmental conditions (in particular, stressful ones), they can be destabilized, allowing underlying genetic variation to cause traits to vary, thus providing grist for natural selection’s mill.

This hypothesis is attractive for a couple reasons: it seems to provide a mechanism for rapid adaptation beyond the scope of existing variation within a population, and it seems intuitive that rapid changes in natural selection (resulting from climate change or the colonization of a new habitat, for example) might also be very stressful, even to organisms that make the cut. A possible problem with the hypothesis is that if the stressor that destabilizes development ends, or if organisms are able to acclimatize to it, the trait variation should disappear in subsequent generations, masked again by canalized development. To solve this it has been proposed that this developmentally induced variation can be “assimilated”, a process that requires selection to favor the constitutive expression of formerly masked genetic variation.

A new paper by Nicolas Rohner and colleagues (Dec. 2013) seek to provide evidence this mechanism operates in nature by examining the evolution of eye loss in a species of fish that has colonized caves in North America (Astyanax mexicanus). When vertebrates become exclusive cave dwellers, they often evolve a suite of traits, including the reduction or loss of both eyes and pigmentation. These cave dwellers make interesting study systems because they are frequently recently derived from nearby surface dwelling species, providing a natural comparison. In this case,  A. mexicanus has both eyeless cave populations, and sighted surface populations. Rohner et al. were interested in whether the process of developmental destabilization followed by assimilation could have facilitated the evolution of eye loss in cave populations of A. mexicanus. 

It had been previously discovered that morphological development in some organisms is buffered by the protein HSP90. Under stressful conditions, HSP90 can lose efficacy and allow trait variation to emerge. In A. mexicanus, the researchers found that it appeared to buffer eye development. Under typical circumstances, A. mexicanus shows little variation in eye size. When fish were treated with Radicicol, however, a chemical that mimics stress by specifically inhibiting HSP90, increased variation in eye size emerged. The researchers then treated both surface and cave fish with Radicicol and measured their responses. Surface fish treated with Radicicol showed increased variability in both the size of the eye and eye socket. Treated cave fish (which do not have eyes) showed a significant decrease in eye socket size, but not an increase in variability. This difference suggests that selection may have eliminated the upper registers of genetic variation for eye size in the cave dwelling fish, and that genetic variation relevant to eye loss is sensitive to the buffering effects of HSP90.

Next, Rohner et al. asked whether colonization of the cave environment could conceivably produce the kind of stress response that would unmask this genetic variation. They found that water in the caves had much lower conductivity (lower concentrations of dissolved inorganic solids) than the river water inhabited by surface fish. Prior research suggested large changes in conductivity could elicit a stress response in fish, so they challenged surface populations with low conductivity water. They found that it did indeed provoke a stress response, causing an upregulation of HSP90 and associated proteins and an increase in eye size variation in fish reared under these conditions.

Finally, the researchers asked if these developmentally induced changes could be genetically assimilated. To address this they conducted a selection experiment. They treated surface fish with Radicicol, selected the individuals with the smallest eyes, interbred them and raised their offspring without Radicicol. They found that the offspring had significantly smaller eyes than the untreated adult population.

To me, this a very interesting study, but falls short of providing convincing evidence that HSP90-regulated development has actually played an important role in the evolution of eye loss in A. mexicanus. I am convinced that eye development is buffered by HSP90, that the stress response results in exaggeration of heritable eye size variation, and that said variation has probably been selected upon in the cave populations. What I think is lacking is a proper control for the last piece, the test of genetic assimilation. What is needed is a simple selection experiment on eye size in untreated surface fish. If selection for smaller eyes in the natural, untreated population produced a substantial response, the need for the more complex explanation invoking cryptic variation, stress and assimilation is obviated. Alternatively, if there is very little response to selection, the story becomes much more compelling. I think the real power of this kind of mechanism lies in its potential to allow substantively different traits to arise, ones that don’t already have a clear evolutionary path laid out to them.

If you’re interested in reading more on this subject, there is a nice (open access!) review by Pigliucci et al. (2006).

References:

Pigliucci, Massimo, Courtney J. Murren, and Carl D. Schlichting. “Phenotypic plasticity and evolution by genetic assimilation.” Journal of Experimental Biology 209.12 (2006): 2362-2367.
Rohner, Nicolas, et al. “Cryptic Variation in Morphological Evolution: HSP90 as a Capacitor for Loss of Eyes in Cavefish.” Science 342.6164 (2013): 1372-1375.
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