In Fish, Social Status Goes Right to the Brain
By NATALIE ANGIER
Published: November 12, 1991
AMONG males of many species, from elephant seals to human beings, the struggle to prevail over competing males often seems to dwarf all other tasks -- and perhaps with good reason.
A scientist has discovered that how a male fish interacts with other males, and whether it is socially dominant or a tremulous wimp, has such a profound effect on the creature that it changes the brain cells in charge of the fish's capacity to breed.
Studying the African cichlid fish, Dr. Russell Fernald, a neurobiologist at Stanford University, has discovered that in aggressive males that command large territories and keep contending males at bay, brain cells in the hypothalamus that allow the fish to mate are six to eight times larger than are equivalent cells in mild-mannered males with no social clout.
What is more, Dr. Fernald has found that the dimensions of those cells are extremely plastic. Should the domineering male be confronted by a larger male able to bully it, the neurons of the defeated fish will rapidly shrink. And after the hypothalamic cells have shrunk, the male's testes follow suit, eventually robbing the fish of its desire and ability to breed.
The discovery is the first persuasive evidence of how social behavior can help sculpt the structure of the brain, and how the altered brain, in turn, influences animal behavior.
"It's a big jump conceptually to ask how behavior might affect cellular and molecular events," said Dr. Fernald, "but now we can look at it directly." 'A Marvelous Example'
In laboratory experiments that change the social status of the fish, he said, "we can push the males forward or backward, from macho to wimp and back again." Some of the findings appeared in a recent issue of The Journal of Molecular Endocrinology.
The results provide powerful evidence that the old nature-nurture argument, pitting the influence of biology on behavior against that of the environment, is far too simplistic.
Instead, researchers said, an animal's body, its behavior and its social milieu very likely represent interdependent points on a giant feedback loop, with one alternately affecting the other.
"This is a marvelous example of how the social environment influences animal biology," said Dr. Darcy B. Kelley, a biologist at Columbia University who studies frog mating songs. "Here you have this animal whose social state is translated into changes in the cells of the hypothalamus, which then contribute to the animal's augmented reproductive capacity. This goes a long way toward solving the nature-nurture debate, which was a false debate to begin with."
The findings may also have implications for a few finless creatures, including people. Because the brain molecules under study are highly conserved across the evolutionary spectrum, Dr. Fernald suggests that the architecture of the human brain may also be affected by a person's behavior.
Indeed, Dr. Simon LeVay of the Salk Institute in La Jolla, Calif., who stirred an acrimonious debate recently when he said he had detected a difference in the hypothalamus between homosexual and heterosexual men, has expressed great interest in Dr. Fernald's new study.
But researchers concur that it will be far more difficult to decipher the meaning of brain differences in people than it is to investigate the neurobiology of fish.
Dr. Fernald began his research at Lake Tanganyika in Africa, home to 150 species of cichlid fish. Studying the species Haplochromis burtoni, he noticed that only 10 percent of the males controlled all the feeding territory and all access to females. Those few males, he realized, differed spectacularly from their timid counterparts. Dominant males are larger and more brilliantly colored, with bold orange stripes and fins that gleam like rainbows, and they are extremely aggressive. By contrast, both females and subordinate males have cryptic, sand-colored scales and are unlikely to pick a fight. The Price of Glory
But it turns out that the flamboyance of machismo has its price. The colorful fish are easily seen and predated upon, and once a dominant male disappears, a remarkable event occurs. All the meek males in the neighborhood rush over, seeking to fill the vacancy, and a series of violent battles commences.
"They're surprisingly vigorous fighters," said Dr. Fernald. "They chase each other, they bite, they hit each other with their tails. It really looks painful."
Eventually, a winner emerges and promptly begins flaunting his success through telltale displays of dominance and territoriality. At that point a welter of physical changes begins. The male grows bigger and gains a bright coat; its gonads swell and it starts making sperm.
Taking the fish back to his laboratory, Dr. Fernald traced the molecular sequence of events from new-found social dominance to full-fledged sexual prowess. He found that the behavioral changes occur first, and that they in turn spur dramatic growth in brain cells responsible for producing a compound called gonadotropin-releasing hormone. That substance tweaks the pituitary gland to produce hormones that in turn stimulate the fish's testes and switch on sperm production.
Conversely, in experiments where a dominant male is stripped of its pre-eminence by the introduction of a bigger, nastier male, the chastened fish stops making dominant displays and slinks off, and the brain changes follow. Within days, its bright colors have disappeared and its testicles have withered.
"The behavior is what's driving it," said Dr. Fernald. "The failure to play a socially dominant role is the key, which ultimately down-regulates testes size."
That may seem a sad fate for a male who has savored the spoils of power. But then again, said Dr. Fernald, the fish regain their cryptic coloring and hence a potentially longer lease on life.
Photo: In a species of African cichlid, the social status of a dominant male fish, at bottom, is translated into bigger brain cells and greater ability to mate, illustrating the interaction between brain and behavior. (Dr. Russell Fernald) (pg. C12) Diagram: "The Mind-Body Connection" In cichlid fish, males battle each other for breeding territory. Dominant males, which gain special colors, have now been found to have distinctly larger cells in the brain region known as the hypothalamus. If these males are defeated, the cells shrink and the fish lose their colors and breeding behavior. (pg. C1)