Feb. 20, 1998 Timing is everything, as lovers know. Susan Brawley, a University of Maine marine biologist, leads a research team which has used that truth, along with the results of biochemical studies with seaweed, to overturn a widely-held principle of reproduction in aquatic organisms.
Their work demonstrates a heretofore unknown biochemical mechanism which makes organisms "exquisitely sensitive" to environmental cues such as water motion and salinity, according to a 1996 paper co-authored by Brawley and her research team.
Brawley gave a presentation today about her team's work at the annual meeting of the American Association for the Advancement of Science in Philadelphia.
The organisms in question are those which reproduce in the water by external fertilization -- some species of fish, corals, and plants such as seaweeds. The results of previous experiments and modeling studies have concluded that, when it comes to fertilization, these organisms don't have that knack for good timing, i.e., that their rate of fertilization success borders on one percent or less.
These studies have used an underlying assumption that reproductive cells, or gametes, are released when water is turbulent. As a result, gametes would be diluted and dispersed. Few would find their target under such conditions.
In light of the evolutionary success of seaweeds and other organisms which use external fertilization, this line of reasoning struck Brawley as odd. "Selection pressure should act quickly on any characteristic that allows an organism to have fertilization success," she says. The hypothesis of an extremely low success rate doesn't meet this evolutionary test.
Isle of Man
During a 1990 sabbatical on the Isle of Man, Brawley became interested in Fucus , a globally common family of brown seaweeds. Fucus species were the only seaweed known to thrive equally well in saline waters as well as low salinity environments such as the Baltic Sea.
In following years, she received support from the National Science Foundation for field studies and laboratory experiments to find out how Fucus adapted to such different chemical conditions. Her primary concern was the mechanism which allowed Fucus to avoid polyspermy, a lethal condition in which an egg is fertilized by more than one sperm. Seaweeds normally depend on high concentrations of sodium to prevent polyspermy, but the Baltic Sea populations didn't have much sodium to work with.
Brawley worked closely on this question with researchers at the University of Stockholm and University of Umeå in Sweden. During her work, she also noticed that Fucus vesiculosis didn't release its gametes until slack high tide. She suspected that the plants were responding to water motion and, perhaps, to accompanying changes in salinity.
Back at the University of Maine in Orono, Brawley worked with Gareth Pearson, a post-doctoral researcher, and Esther Serrao, a graduate student, to study this possibility in earnest. They used Baltic specimens Brawley had brought from Scandinavia, and they collected plants from tide pools along the Maine coast. They also received plants from researchers in California.
"We were able to simulate in the laboratory that high salinity is one of the cues for the release of gametes, and all of that was done under calm conditions," says Brawley. "In the back of my mind, I kept thinking about the affect of water motion. Nearly every introductory biology book you read will have some statement that organisms that use external fertilization have to release lots and lots of gametes because fertilization success is low.
"Now with five different fucoid algae in California, the Baltic and here in Maine, we've found that the adults were waiting to release their gametes under conditions that were less turbulent. When the gametes aren't diluted, fertilization success is high. I think that's going to stand in most cases."
Carbon is the key
In a subsequent series of experiments, Brawley, Pearson and Serrao delved into the biochemical mechanism underlying gamete release. Levels of dissolved inorganic carbon such as carbon dioxide and bicarbonate, they hypothesized, might provide a key.
While the sun is shining, plants take up carbon as they carry out photosynthesis. Brawley and her team reasoned that when water is being churned by waves or tidal currents, the plants are constantly receiving new supplies of carbon. Gametes are not released under such circumstances.
That changes, however, when the water is calm. Without turbulence, the carbon supply begins to run out. The UMaine experiments have shown that the carbon deficit is the chemical signal for plants to release their gametes. It is the green light which tells the plants that the water is calm and the time is right for reproduction.
"We did two types of experiments," says Brawley. "One was a series of tests to see what was involved with dissolved inorganic carbon." In those tests, the researchers varied the levels of carbon in the water. They also agitated the water to simulate turbulent conditions. In reach case, the results were consistent with the team's predictions.
"It is a boundary layer disturbance. That's important to show. Many cells have a mechanical response to pushing, bending, something like that, but this is chemical sensing," Brawley says.
"What I expect is that external fertilization is going to be found to be very successful in these organisms. The caveat is that we always have to remember that we're looking at a snapshot of evolution and that not every species is at its heyday. It may be a species that is on its way out, or it may be one that is recent. We have to keep in mind where it is relative to selective mechanisms or how well adapted it is to the community it lives in."
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