Thursday, July 31, 2014

MIT lab demos rapid evolution in fish, driven by natural environmental change

Photo: Two varieties of the same species of Mexican Tetra, Astyanax mexicanus - in its surface and eyeless cave forms. Although the most obvious morphological traits (changes in body structure) are the loss of pigmentation and eyes in the cave variety, a number of other traits undergo rapid changes in response to the environment.
Image: Nicolas Rohner
The long-standing view of how evolution unfolds is that organisms experience spontaneous genetic mutations; these mutations can result in new traits which are either helpful or deleterious. Beneficial traits increase the odds an individual will survive, breed and pass its traits on to offspring.
 
Though this evolutionary process unquestionably occurs, it requires substantial time. Organisms under the pressure of extreme environmental changes must adapt rapidly to survive, however, pointing to a much more rapid adaptive strategy which scientists knew must exist. An MIT-Harvard research team has discovered such a strategy in cavefish, which make use of a heat shock protein called HSP90.

Heat-shock proteins are a protein group carried by virtually every living creature, including bacteria, plants, animals and humans. They help control the folding and unfolding of other proteins. 

The numbers indicate the molecular weight of each type of heat shock protein, such as HSP90. HSP90 controls protein folding of key growth and development gene regulators. Such folding must be very precise for proteins to perform their proper functions.

Several thousands of years in the past, a Mexican tetra (Astyanax mexicanus) population was transported from its native river habitat into the radically different environs of underwater caves. Forced to adapt to almost complete darkness, they lost their pigmentation, sharpened their sensitivity to nearby prey and to water pressure fluctuations, and completely lost their eyes. 

While the latter change may seem maladaptive, it is in fact advantageous, because maintaining a set of complex but pointless sense organs is biologically "expensive". Shedding unneeded eyes allowed Astyanax to reallocate limited biological resources to functions more appropriate for a cave environment.

According to lead author Dr. Nicolas Rohner, Astyanax mexicanus' striking adaptations are an example of standing genetic variation, which says that populations carry a number of silent but potentially beneficial genetic mutations - genes which have been switched off. Under specific environmental stresses, the genes for these mutations can switch on, guiding protein manufacture that results in visible phenotypes (observable traits which come from a creature's genes).

Says MIT biology professor and Howard Hughes Medical Institute investigator Dr. Susan Lindquist, HSP90 usually keeps such genetic variations dormant in a wide range of organisms, ranging from primitive yeasts to plants and fruit flies.  

Subjecting cells to heightened temperatures or other stresses reduces HSP production; in her research, Dr. Lindquist discovered that normally large reserves of cellular HSP90 dwindle during such physiologically stressful periods. These decreases in HSP90's suppressive control result in the rapid emergence of various phenotypic changes; some of these emergent traits are neutral or deleterious, while some are clearly beneficial.

Environmental changes alter protein folding, causing minor changes in the genome which can have major effects. Because HSP90 controls folding of important gene regulators of growth and development, it acts as a fulcrum for evolutionary change.

Dr. Rohner's research on the genetic changes behind Astyanax' eye loss caught Dr. Lindquist's attention, and they began to collaborate on researching HSP90's role in the process. 

Experiments on both cave and surface fish varieties of Astyanax yielded fascinating results. Raising surface fish with a drug that suppresses HSP90 - causing the same effect as rapid environmental changes - resulted in significant eye size variation, clearly showing HSP90's central role in the trait. 

While the cavefish variety is eyeless, their skulls retain ancestral orbital cavities. Cavefish raised in the same environment displayed no increase in variation of eye orbit size, but they grew smaller orbits, showing that eye size can vary based upon the presence of HSP90.

Because the team used artificial means to achieve their results, however, it was uncertain whether or not such (HSP90-altered) conditions would in fact naturally arise in the environment. 

To determine the answer, the team looked into the factors of the fish's two different natural environments, including oxygen levels, temperatures, and pH levels (potential Hydrogen, the tendency for water to be acidic - containing more positively-charged hydrogen ions - or alkaline - to contain more negatively charged OH hydroxide ions). 

The biggest difference between the surface and cave water environments was in conductivity - the ability of salts to transfer electrical charges. The cave environment had low salinity (conductivity levels), which induced a heat shock protein response, naturally generating lower levels of HSP90 protein, and thereby lifting the protein's constraints on growth and development regulators. As a result, surface fish raised in water with the same low salinity as the cave fish environment showed significant variations in eye sizes. This demonstrated that a natural environmental stressor could induce the same effects as artificially suppressing HSP90 activity.

This study expands upon Dr. Lindquist's previous experiments with HSP90-induced evolutionary changes in yeast, and showing the same mechanism comes into play throughout the plant and animal kingdoms.

Source: Rapid evolution of novel forms: Environmental change triggers inborn capacity for adaptation, press release, December 12, 2013, Matt Fearer, Whitehead Institute for Biomedical Research, Massachusetts Institute of Technology

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