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Table 1 Different theories for eye loss proposed by scientists today plus the limitations of each theory

From: Losing Sight of Regressive Evolution

Theory Lamarckian evolution Neo-Darwinian evolution
"Use and disuse" and inheritance of acquired characteristics Neutral mutation Direct natural selection Indirect natural selection: genetic hitchhiking and pleiotropy
Relaxed selection and mutation as an evolutionary force Positive natural selection Negative natural selection Efficient metabolism Increased olfaction Increased taste Modified brain Neuron plasticity of visual cortex
Description The interaction of organisms with their environment powers an alchemical adaptive force so that the permanent disuse of any organ imperceptibly weakens, deteriorates, and progressively diminishes its functional capacity, until it finally disappears Once genes for eyes neither enhance nor hinder the organism’s survival, the forces of natural selection that once maintained those genes in good working order no longer operate. The genes accumulate mutations that impair their function and so, the unnecessary structures degenerate Fish without eyes survive or reproduce more because they do not waste energy making an eye or maintaining a functional retina Fish with eyes have decreased survival rates or reproduce less because they are more likely to receive wounds and get infections in these delicate organs The gene that causes blindness is closely linked or is the same gene that may control a favorable metabolism for living in caves Throughout embryological development, the craniofacial patterning is mediated by the physical presence or absence of an eye. When there is no eye, bones shift position and the olfactory pit is enlarged Master–control Sonic hedgehog (Shh) gene has an inverse effect on the development of eyes and taste buds: the smaller the eyes, the more taste buds produced Master–control gene Sonic hedgehog (shh) has a large effect on the anterior part of the brain. The shh expression that makes small eyes may generate a brain whose structure is more efficient in the darkness Neurons that do not receive visual input may be more easily recruited and sequestered by other systems than neurons that are receiving information which translates into, “I detect no light. I detect no light. I detect no light”
Limitations Use and disuse is not an evolutionary force. Mice whose tails are cut for many generations do not produce tailless offspring According to the theory, all genes not being maintained should accumulate mutations and degenerate. Lens transplanting experiments show that after thousands of years of evolution in caves, most eye genes remain perfectly functional. Instead, blindness seems to be caused by mutations on a reduced number of master genes that control eye development The energy needed to make an eye, which is basically a globule of protein that encapsulates water, may be less than what is needed to make the plug of fat and bone in blind cave fish. There are more calories in a gram of fat than in a gram of protein or water. Complexity is not always synonymous with energy expenditure This theory does not take into account that surface fish also have means to protect their eyes from wounds and a lateral line effective enough to prevent damaging crashes that may happen in the darkness of the night. Furthermore, caves with unsanitary or copious amounts of bat guano can actually have fish with less eye degeneration In a controlled laboratory experiment where eyed and blind F2 fish had to compete for food while in complete darkness, blind fish did not do better than eyed fish. Also, the exact gene that causes blindness in cave fish has not yet been identified, so it is unknown how it may affect metabolism Although the olfactory pit is 13% wider in fish that lack eyes during their development, no experiment has been done to see if it correlates with an increased sense of smell. It may be that a “deformed” nose may not smell better, even when the deformation involves an increase of size Although the number of taste buds is larger in fish with shh expression for small eyes, no experiment has been done to see if this correlates with the fish’s ability to find more food. It may be that a “deformed” gustatory organ does not have improved chemoreception, even when the deformation involves an increase in the number of taste buds Although the effect of shh in the development of the anterior part of the brain is well documented, there is no a priori reason for why such changes would be better for blind fish. Experiments need to test how changes in the brain translate into a more effective behavior for the cave environment Experiments show that neurons in the visual cortex of cave fish actively respond to tactile stimuli. We need to test if optical neurons are sequestered more in eyed fish that have been enucleated early on in their development versus eyed fish that have been raised in darkness. Until then, the hypothesis is purely speculative
Suggested reading Darwin, C. On the Origin of Species. (Conveniently available in its entirety on the web at Chapter 5, Section 2: Effects of the increased use and disuse of parts, as controlled by natural selection. Also, Chapter 14, Section 6: Rudimentary, atrophied, and aborted organs Wilkens, H. 1988. Evolution and genetics of epigean and cave Astyanax fasciatus (Characidae, Pisces). Support for the neutral. mutation theory. Evol. Biol. 23:271–367 Sadoglu, P. 1967. The selective value of eye and pigment loss in Mexican Cave Fish. Evolution 21(3): 541-549 Breder, C. M. 1942. Descriptive ecology of La Cueva Chica, with especial reference to the blind fish, Anoptichthys. Zoologica 27: 7–15 Borowsky, R. and Wilkens, H. 2002. Mapping a Cave Fish Genome: Polygenic Systems and Regressive Evolution The Journal of Heredity 93(1): 19–21 Yamamoto, Y., Espinasa, L., Stock, D. W. & Jeffery, W. R. 2003. Development and evolution of craniofacial patterning is mediated by eye-dependent and eye-independent processes in the cavefish Astyanax. Evolution & Development 5(5):435–446 Jeffery, W., et al. 2000. Prox 1 in eye degeneration and sensory organ compensation during development and evolution of the cavefish Astyanax. Dev. Genes Evol. 210: 223–230 Menuet, A. et al. 2007. Expanded expression of Sonic Hedgehog in Astyanax cavefish: multiple consequences on forebrain development and evolution. Development 134: 845–855 J. Voneida, T. J. and Fish, S. E. 1984. Central Nervous System Changes Related to the Reduction of Visual Input in a Naturally Blind Fish. American Zoologist 24(3):775–782