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Pregnancy Timeline by SemestersFetal liver is producing blood cellsHead may position into pelvisBrain convolutions beginFull TermWhite fat begins to be madeWhite fat begins to be madeHead may position into pelvisImmune system beginningImmune system beginningPeriod of rapid brain growthBrain convolutions beginLungs begin to produce surfactantSensory brain waves begin to activateSensory brain waves begin to activateInner Ear Bones HardenBone marrow starts making blood cellsBone marrow starts making blood cellsBrown fat surrounds lymphatic systemFetal sexual organs visibleFinger and toe prints appearFinger and toe prints appearHeartbeat can be detectedHeartbeat can be detectedBasic Brain Structure in PlaceThe Appearance of SomitesFirst Detectable Brain WavesA Four Chambered HeartBeginning Cerebral HemispheresFemale Reproductive SystemEnd of Embryonic PeriodEnd of Embryonic PeriodFirst Thin Layer of Skin AppearsThird TrimesterSecond TrimesterFirst TrimesterFertilizationDevelopmental Timeline
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Home | Pregnancy Timeline | News Alerts |News Archive Dec 16, 2013

 



The eyeless cavefish Astyanas mexicanus. These fish begin to develop eyes but then lose them as the embryo matures. They are also depigmented, unlike their (below) surface-dwelling ancestors. This is one of the few cave animals in which the surface-dwelling ancestor is not extinct, which allows scientists to compare them genetically.

Image Credit: William Jeffery







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Environmental change triggers adaptation

In at least one variety of cavefish, an agent of evolutionary adaptative change is the heat shock protein known as HSP90.

In the classic view of evolution, species experience spontaneous genetic mutations that produce various new traits — some helpful, some not. Nature selects the most beneficial, passing them onto the next generation.


Natural selection is an elegant model. It's also an extremely time-consuming process likely to fail organisms needing to cope with sudden, potentially life-threatening changes in their environments. Surely some other mechanism could enable more rapid adaptive response.


In this week's edition of the journal Science, a team of researchers from Harvard Medical School and Whitehead Institute report that, at least in the case of one variety of cavefish, that other agent of change is the heat shock protein known as HSP90.

"It's a very cool story in terms of the speed of evolution," says Nicolas Rohner, lead author of the Science paper and a postdoctoral researcher in the lab of Harvard Medical School Genetics Professor Clifford Tabin.

Rohner notes that at some point many thousands of years ago, a population of Astyanax mexicanus (a fish indigenous to northeastern Mexico) was swept from its hospitable river home into the unfriendly confines of underwater caves. Facing a dramatically different environment, the fish were forced to adapt. Living in near total darkness, the fish did away with their pigmentation, developed heightened sensory systems to detect changes in water pressure and the presence of prey and, perhaps most strikingly, they lost their eyes. Although seemingly counterintuitive, the loss of eyes is thought to be an "adaptive" or beneficial trait, as the maintenance of a complex but now useless organ would come at a high metabolic cost. Thus, the fish could reallocate their finite physiological resources to biological functions more helpful in the cave setting.

Eye loss in these fish is considered to be a demonstration of an evolutionary concept known as "standing genetic variation," which argues that pools of genetic mutations—some potentially helpful—exist in a given population but are normally kept silent. The manifestations of these mutations, that is, their observable impact, won't emerge until the population encounters stressful conditions. But what exactly keeps those mutations at bay?

Whitehead member Susan Lindquist's research has shown that HSP90 silences such genetic variation in a variety of organisms, from fruit flies, to yeast, to plants. Lindquist's work found that the normally robust cellular reservoir of HSP90 becomes depleted during periods of physiological stress. The loss of HSP90 activity allowed phenotypic changes to emerge quite rapidly. Although some emergent traits found in her lab were not adaptive, some clearly were.


"The delicate balance of protein folding—especially that controlled by HSP90—holds the key.

"Moderate changes in the environment create stresses on protein folding, causing minor changes in the genome to have much larger effects. Because HSP90 governs the folding of the key regulators of growth and development it produces a fulcrum point for evolutionary change."

Susan Lindquist, professor of biology, MIT, investigator at the Howard Hughes Medical Institute.


Having seen Tabin's work on the genetics of eye loss in cavefish, Lindquist proposed a research collaboration. The Tabin and Lindquist labs devised a complex set of experiments with cavefish and surface fish of the same species. Surface fish raised in the presence of a drug that blocks HSP90 activity (thereby mimicking a stressful environment) displayed significant variation in eye size—clearly implicating HSP90's effects on this trait. Conversely, cavefish raised in the same conditions showed no increase in variation in the size of their eye orbits (although the cave fish have no eyes, their skulls retain the orbital cavity where their eyes once were). Intriguingly, however, these fish emerged with small orbits, showing that the genetics governing eye size remains responsive to HSP90.

Although impressive, these findings were chemically induced, leaving open the question of whether HSP90-related effects would have been seen in nature. To answer this, researchers examined a host of conditions—ranging from pH to oxygen content to temperature—found in the surface and cave waters that are home to these fish. They discovered a considerable difference in conductivity, as measured by salinity, between cave and surface. Because low conductivity, a condition found in the caves, can trigger a heat shock response, they raised surface fish in water whose conductivity equaled that of native caves.

The results were essentially the same: fish raised in conditions of low conductivity showed significant variation in eye size. The scientists had proved that an environmental stressor could have the same effects as the chemical inhibition of HSP90.

"This is the first time that we can see in a natural setting where the stress came from and observe the variation that results," says Tabin.

Adds Rohner: "This is the first study showing that this HSP90-mediated mechanism can be applied to vertebrates for real morphological adaptive traits."

For Dan Jarosz, a former postdoctoral researcher in Lindquist's lab, the study is an important validation of Lindquist's work on evolution. Jarosz, now Assistant Professor of Chemical and Systems Biology and of Developmental Biology at Stanford University, had been involved in much of Lindquist's work on HSP90 as a driver of evolution in yeast. He believes this latest work should help quiet those who are skeptical of the impact of this mechanism throughout the plant and animal kingdoms.


"We now have enough evidence to say that large, rapid environmental change can reveal new variation and change the outcomes of real evolution in nature,"

added Dan Jarosz, Assistant Professor of Chemical and Systems Biology and of Developmental Biology at Stanford University.


Abstract
In the process of morphological evolution, the extent to which cryptic, preexisting variation provides a substrate for natural selection has been controversial. We provide evidence that heat shock protein 90 (HSP90) phenotypically masks standing eye-size variation in surface populations of the cavefish Astyanax mexicanus. This variation is exposed by HSP90 inhibition and can be selected for, ultimately yielding a reduced-eye phenotype even in the presence of full HSP90 activity. Raising surface fish under conditions found in caves taxes the HSP90 system, unmasking the same phenotypic variation as does direct inhibition of HSP90. These results suggest that cryptic variation played a role in the evolution of eye loss in cavefish and provide the first evidence for HSP90 as a capacitor for morphological evolution in a natural setting.

Full Citation:
"Cryptic Variation in Morphological Evolution: HSP90 as a Capacitor for Loss of Eyes in Cavefish" Science, December 13, 2013

Authors:
Nicolas Rohner (1), Dan F. Jarosz (2), Johanna E. Kowalko (1), Masato Yoshizawa (3), William R. Jeffer (3,4), Richard L. Borowsky (5), Susan Lindquist (2,6,7), Clifford J. Tabin (1).

1. Department of Genetics, Harvard Medical School, Boston, MA 02115, USA.

2. Whitehead Institute for Biomedical Re-search, Cambridge, MA 02142, USA.

3. Department of Biology, University of Maryland, College Park, MD 20742, USA.

4. Marine Biological Laboratory, Woods Hole, MA 02543, USA.

5. Department of Biology, New York University, New York, NY 10003, USA.

6. Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.

7. Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02142 USA.


This work is supported by the National Institutes of Health and the Damon Runyon Cancer Research Foundation.

Susan Lindquist's primary affiliation is with Whitehead Institute for Biomedical Research, where her laboratory is located and all her research is conducted. She is also a professor of biology at Massachusetts Institute of Technology and an investigator of the Howard Hughes Medical Institute.