Which came first?

Oct 30, 2003, vol. 28, no. 5
By Diane Luckow



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Which came first, the butterfly or the caterpillar, the tadpole or the frog? The mystery of metamorphosis - the amazing transformation of a larva into a very different adult animal form - has long perplexed humankind.

“It's an interesting question to understand how an animal can have such very different forms in its life cycle,” says SFU professor of molecular biology, Bruce Brandhorst. “During evolution one form had to precede the other, they couldn't have arisen simultaneously.”

Now, Brandhorst and SFU post-doctoral fellow Cory Bishop have an interesting new theory on the subject that was published in a recent edition of the scholarly journal Evolution and Development.

The duo, both in the department of molecular biology and biochemistry, have discovered that a simple gas called nitric oxide controls when metamorphosis occurs in some animals. “From that, we speculated that since nitric oxide also controls the timing of life cycle changes in the stages of other simple organisms, it may have a long evolutionary history of controlling life cycle transitions,” explains Brandhorst, “allowing organisms to regulate when they become sexually mature, which in many animals involves going through metamorphosis from the larval stage to a juvenile or adult stage.”

The big quandary scientists have always pondered is how the larval stage came to be so different from the adult and whether, in their early evolutionary phase, adults used to look like the much simpler present day larvae, or whether the larval stage was somehow inserted into the life cycle.

Based on their findings that nitric oxide allows larvae to delay metamorphosis, Brandhorst and Bishop propose that larval forms were an evolutionary insertion that arose because animals could delay their adult formation. Forming swimming larvae allowed them to more easily escape predation or to grow bigger and therefore produce more or bigger eggs, providing a selective advantage in the struggle for survival of the species.

“We also suggest that it then became advantageous for adults to protect those eggs and so they started to evolve larger and more complicated bodies with protective devices such as shells,” says Brandhorst. “This co-evolution between larvae and adult protective devices would help explain why so many different adult body forms appeared suddenly in the fossil record 540 million years ago.” Because there is little fossil evidence of animal life before this evolutionary period, called the cambrian explosion, it is recognized as the most important period in the history of animal life on earth.

The scientists' theory arises out of Bishop's doctoral research into a protein called HSP90. He found that inhibiting the activity of HSP90 induced metamorphosis, an unexpected revelation. Further research into the literature revealed that nitric oxide might also be involved in regulating metamorphosis and that HSP90 activity is required for production of this gas.

Nitric oxide is a widely used physiological regulator (and the basis for the drug Viagra). It has an interesting set of properties which include its solubility in water and lipids (or fats), allowing its easy passage between cells.

Its production in cells is extremely sensitive to levels of both nitrogen and oxygen. Nitric oxide production is thus linked to the nutritional state of an organism and can act as a switch to rapidly respond to environmental inputs and stress. It is the unique and versatile nature of nitric-oxide-based cellular comm-unication that makes it ideally suited to orchestrate complex events like life cycle transitions.

As a result, says Brandhorst, “We predicted that inhibition of nitric oxide production would trigger metamorphosis, while chemical generators of nitric oxide should inhibit induction of metamorphosis.” When they experimented on sea urchins and sea squirts, this did indeed occur.

The theory may hold a key to unlocking the mystery surrounding the evolution of complex life cycles.

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