Development of cavefish eyes

Here's a story that Darwin got completely wrong. He had observed that certain species had profoundly reduced or rudimentary organs, and he explained them not as a consequence of natural selection, but as evidence of the inheritance of acquired characters.

But we learn from the study of our domestic productions that the disuse of parts leads to their reduced size; and that the result is inherited.
It appears probable that disuse has been the main agent in rendering organs rudimentary. It would at first lead by slow steps to the more and more complete reduction of a part, until at last it became rudimentary,- as in the case of the eyes of animals inhabiting dark caverns, and of the wings of birds inhabiting oceanic islands, which have seldom been forced by beasts of prey to take flight, and have ultimately lost the power of flying.

It's easy to feel mildly embarrassed for Darwin on reading this now; it was an honest error, though, and since he had no good model for inheritance, he fell back on an old idea, that the use or disuse of an organ in the parent would have an effect on its progeny. Blind fish lost their eyes because Mom and Dad fish lived in the dark and never used their eyes, so Junior inherited weaker eyes.

As it is difficult to imagine that eyes, though useless, could be in any way injurious to animals living in darkness, their loss may be attributed to disuse.

Well, actually, Charles…it's not difficult to imagine at all. Eyes are fragile, pulpy things that represent a significant investment in energy. I could imagine that there would be a slight selective advantage to jettisoning something an animal isn't using, that costs it effort to develop or is a weak or sensitive point of attack. Since we've long discarded the hypothesis of the inheritance of acquired characters, that's one of the primary explanations for the loss of eyes in cave animals—their absence was an advantage.

Another explanation is that eyes are effectively a neutral character in dark environments, and that there is therefore no selective advantage in maintaining them. Cave organisms acquired mutations that knocked out the eyes, and in the absence of selection to maintain sight, these mutations accumulated until the entire population was lacking eyes.

There is a third possibility, now supported by observations in blind cave fish of the genus Astyanax. Despite being wrong on the mechanisms of inheritance, Darwin was no dummy, and he almost figured this one out. If he'd had just a little more intuition about development, he might have suggested this idea. Here's the tantalizingly close passage:

By the time that an animal had reached, after numberless generations, the deepest recesses, disuse will on this view have more or less perfectly obliterated its eyes, and natural selection will often have effected other changes, such as an increase in the length of the antennae or palpi, as a compensation for blindness.

The third possibility requires that one recognize that development is not infinitely plastic, that characters are linked in development, and that maybe the only way to develop these compensatory structures is at the expense of the eyes—that is, that there is a selective advantage to developing long antennae or palpi or other organs, but that the simplest developmental process to do so involves cannibalizing eye tissue. This explanation is an example of the way knowledge of developmental biology can inform our understanding of evolutionary biology.

Continue reading "Development of cavefish eyes" (on Pharyngula)