Friday, February 16, 2007

 

The Nature of 'Regressive Evolution' in Cavefish Untangled

"Regressive evolution," or the reduction of traits over time, is the result of either natural selection or genetic drift, according to a study on cavefish by researchers at New York University's Department of Biology, the University of California at Berkeley's Department of Integrative Biology, and the Harvard Medical School.

Previously, scientists could not determine which forces contributed to regressive evolution in cave-adapted species, and many doubt the role of natural selection in this process. Darwin himself, who famously questioned the role of natural selection in eye loss in cave fishes, said, "As it is difficult to imagine that eyes, although useless, could be in any way injurious to animals living in darkness, I attribute their loss wholly to disuse."

A Blind Mexican Cave Tetra, along with its eyed surface relatives.

The research appears in the most recent issue of the journal Current Biology [A].

[Image: New York University]

Cave adaptations have evolved in many species independently, and each cave species can be considered a replicate of the same evolutionary experiment that asks how species change in perpetual darkness. This makes cavefish a rich source for the examination of the evolutionary process.

In this study, the researchers examined the genetic basis of regressive evolution in the eyes and pigmentation of Mexican cavefish. To do so, they mapped the quantitative trait loci (QTL) determining differences in eye and lens sizes as well as the melanophore - or pigment cell - number between cave and surface fish. These QTL represent genes where new mutations arose in cave populations. To better understand the genetic basis for regressive evolution, they focused on two alternative explanations for regression: natural selection, in which beneficial DNA mutations become more common over time, and genetic drift, in which the frequencies of these mutations can rise or fall over time due solely to statistical variation.

Their results suggested that eyes and pigmentation regressed through different mechanisms. Mutations in cave populations that affected eye or lens size invariably caused size reductions. This observation is consistent with evolution by natural selection and inconsistent with evolution by genetic drift. By contrast, mutations in cave populations that affected pigmentation sometimes caused increases instead of decreases in pigment cell density, consistent with evolution by random processes and genetic drift.

Allaying Darwin's doubts about the role of natural selection in eye loss, the researchers suggest that the high metabolic cost of maintaining the retina is the source of selection against eyes in the cave. By contrast, no such great cost is associated with pigmentation - thus, the two traits regress for different reasons.

Source: New York University Thursday, Feb 15, 2007 (N-280, 2006-07)

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[A] Based on the Current Biology paper:

Regressive Evolution in the Mexican Cave Tetra, Astyanax mexicanus

Meredith Protas, Melissa Conrad, Joshua B. Gross, Clifford Tabin, and Richard Borowsky
Current Biology
10.1016/j.cub.2007.01.051

The evolutionary forces driving the reduction of eyes and pigmentation in cave-adapted animals are unknown; Darwin famously questioned the role of natural selection in eye loss in cave fishes: "As it is difficult to imagine that eyes, although useless, could be in any way injurious to animals living in darkness, I attribute their loss wholly to disuse" [1]. We studied the genetics of eye and pigmentation regression in the Mexican cave tetra, Astyanax mexicanus, by mapping and quantitative trait loci (QTL) analysis. We also mapped QTL for the putatively constructive traits of jaw size, tooth number, and numbers of taste buds. The data suggest that eyes and pigmentation regressed through different mechanisms. Cave alleles at every eye or lens QTL we detected caused size reductions, consistent with evolution by natural selection but not with drift. QTL polarities for melanophore number were mixed, however, consistent with genetic drift. Arguments against a role for selection in the regression of cave-fish eyes cited the insignificant cost of their development [2, 3], but we argue that the energetic cost of their maintenance is sufficiently high for eyes to be detrimental in the cave environment. Regression can be caused either by selection or drift.

[1] Darwin, Charles. (1859). On the Origin of Species by Means of Natural Selection, or The Preservation of Favoured Races in the Struggle for Life (London: John Murray).

[2] Culver, D.C. (1982). Cave Life: Evolution and Ecology (Cambridge, MA: Harvard University Press).

[3] Eigenmann, C.H. (1909). Cave Vertebrates of America: A Study in Degenerative Evolution (Washington, D.C.: Carnegie Institution of Washington).

See Richard Borowsky's webpage The Evolutionary Biology of Cave Fishes

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Also see:

Embryonic Lens Prompts Eye Development
Elizabeth Pennisi
Science 28 July 2000: 522
DOI: 10.1126/science.289.5479.522b

A blind cave fish is providing new insight into how eyes come to be. In work reported on page 631 [B], two developmental biologists show that the lens plays a leading role in eye development in this fish. If it doesn't form properly, the researchers found, the embryo will not go on to make the cornea and other eye structures.

A copy of the above is available from www.bio.net/bionet/mm/cellbiol/2000-August/012893.html:

..The Maryland team has been studying the fish, which is called Astyanax mexicanus, for the past 6 years. Several dozen isolated populations of the species exist in northeastern Mexico, with some living in surface ponds and streams and others in caves and underground waterways. Over the past million years or so, the eyes of the underground fish have degenerated to varying degrees, while the surface fish have retained their large eyes.

To begin to understand this difference, Jeffery and Yamamoto first monitored eye development in the blind fish. They observed a precursor lens and the rudiments of the optic cup forming during the embryo's first 24 hours. But soon afterward, they found, the cells in the embryonic lens underwent programmed cell death. Other eye structures, such as the cornea and the iris, never appeared, and the retina never developed distinct, organized layers, as it does in normal eyes. The eyeball gradually sank back into the socket and was covered by a flap of skin.

Because eye development seemed to progress normally until the lens degenerated, Jeffery and Yamamoto wondered whether this disintegration was triggered by a signal from the embryo or from the lens itself. To find out, Yamamoto removed the embryonic lens from one eye of a blind cave fish embryo and replaced it with a lens from a surface fish embryo. He also did the opposite experiment, replacing the lens of an embryonic surface fish with one from a cave fish embryo. In all cases, he labeled the transplanted tissue with dye so he could track what happened to it. "It's not a complicated experiment, but it really [was] very elucidative," says Mathers.

In both types of transplants, the lens behaved as if it were still in its original embryo. The one from the cave fish degenerated, even though it was in an environment conducive to further development, whereas the lens from the surface fish thrived in the cave fish embryo and the eye differentiated, forming a cornea, anterior chamber, and iris. These results show that "the lens plays a central role" in determining whether the eye develops, comments David Beebe, a developmental biologist at Washington University School of Medicine in St. Louis. Jeffery doesn't know, however, whether the fish can actually see, as a vision test is quite difficult to devise..

[B] Related paper:

Central Role for the Lens in Cave Fish Eye Degeneration
Yoshiyuki Yamamoto, William R. Jeffery

Science 28 July 2000:
Vol. 289. no. 5479, pp. 631 - 633
DOI: 10.1126/science.289.5479.631

Astyanax mexicanus is a teleost with eyed surface-dwelling and eyeless cave-dwelling forms. Eye formation is initiated in cave fish embryos, but the eye subsequently arrests and degenerates. The surface fish lens stimulates growth and development after transplantation into the cave fish optic cup, restoring optic tissues lost during cave fish evolution. Conversely, eye growth and development are retarded following transplantation of a surface fish lens into a cave fish optic cup or lens extirpation. These results show that evolutionary changes in an inductive signal from the lens are involved in cave fish eye degeneration.

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