Online edition of
November 29, 1999

The perfect love nest: Research shows habitat's role in fish reproduction

BY ANNE M. ROSENTHAL

Mark E. Benson was working as a fish caretaker in neurobiologist Russell Fernald's laboratory a few years ago when he stumbled on a key observation: The growth rate of the male African cichlid fish, Haplochromis burtoni, which live in the shallow pools that rim Lake Tanganyika, seemed to be related to territoriality.

As Benson, who had joined the Fernald laboratory after participating in a Stanford summer research program for minority students, cleaned the lab's fish tanks, he inadvertently disrupted the habitat -- changing the social order and, in a sense, informally carrying out some of the preliminary experiments in a research project that has resulted in new findings published in the Nov. 23 issue of the Proceedings of the National Academy of Sciences.

When nature alters the environment, the social hierarchy within an animal population may change as a result. In Lake Tanganyika, daily strong winds, falling banana leaves and even cavorting baby hippos keep the structural habitat in these ponds in constant flux.

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Dominant male cichlid fish attract females who enter to graze the territories males defend. A research team led by Fernald has shown that, in the laboratory, habitat rearrangements cause male cichlids to challenge the top guy more often, causing greater turnover in the dominant male position. As a result, environmental changes give a larger number of males mating opportunities.

The new work highlights the critical role of habitat instability in triggering social interactions that may change social status and affect reproduction. The research was conducted by Fernald, the Benjamin Scott Crocker Professor of Human Biology, director of Stanford's human biology program, a member of the neurosciences program faculty and a professor of psychology; postdoctoral student Hans A. Hofmann, who joined the research group after doctoral studies at the Max Planck Institute for Behavioral Physiology in Germany; and Benson, now a medical student at Dartmouth College.

"All animals have to reproduce to make it in the evolutionary world," says Fernald. "They must weigh present versus future reproductive opportunity. In this case, the males have different phenotypes -- physical traits -- depending on the opportunity."

This picture shows a non-dominant cichlid fish above and dominant cichlid fish below. Note the distinctive coloration of the dominant territorial male. Photo courtesy Russell Fernald

"Dynamic habitat may give animals a chance to change social status," Fernald adds. This could be an important issue in conservation programs. "Making habitats more constant may result in consequences for animals we can't possibly anticipate."

While a number of laboratories study how changes in the brain alter behavior, the Fernald group is one of the few laboratories worldwide looking at the opposite process -- how behavioral interactions can modify cells in the brain.

The striking changes in appearance that accompany dominance in male African cichlids make social status easy to track. Within seconds of beating out another male, the victor sports an eye stripe and bright yellow or blue coloration, controlled by cells like those in a chameleon. Then, over the course of a week or so, the dominant fish develops extra muscles plus a dashing appearance: vertical black bars along the body, a dorsal fin tipped with red, a black spot on the tip of each gill cover and a reddish splotch in back of each gill. There also is an approximate eightfold increase in brain cells that produce gonadotropin-releasing hormone (GnRH), a chemical messenger governing sexual development. This leads to maturation of the sex organs, which become capable of producing sperm.

Importantly, these changes occur only after a male has proved his muster, and result from his change in social position rather than causing it. Interestingly, delayed maturation of gonads in the presence of a dominant territorial male is not unusual in the animal kingdom. Creatures as different as mandrills and stoplight parrot fish are others that exhibit this phenomenon. However, in African cichlids, if another fish defeats the dominant male, the physiological changes reverse, changing the previously territorial fish back to a muted, female-like appearance. Later on, the loser may win back his dominant position and regain his flashy features and sexual potency. So far, African cichlids are the sole species in which a cyclical pattern of dominance and sexual maturity has been documented.

When a male does become a winner, his behavioral encounters somehow modify GnRH-producing brain cells, which in turn trigger changes in body structures. Cortisol, the stress-triggered fight-or-flight hormone, appears to play a role as a mediator.

Previous work by the Fernald laboratory has shown that continuous high levels of cortisol keep non-dominant males in a female-like appearance, a nondescript coloration unlikely to attract predators. Conversely, cortisol levels in dominant fish plummet once the social system stabilizes.

A parallel exists in humans known as stress-related dwarfism, or "Peter Pan syndrome." In these cases, children subjected to psychologically toxic conditions fail to grow even with normal caloric intake. Removing them to a more positive environment results in rapid catch-up of height. The stunting of growth by high cortisol levels in cichlids could represent the evolutionary underpinnings of this condition.

"At some time in the course of human evolution, it may have been adaptive to modulate growth depending on psychosocial conditions," speculates Hofmann.

Win some, lose some

To test the effect of social dominance on growth rate, the investigators placed individually tagged males into aquaria with approximately the same number of females. To mimic the pools of Lake Tanganyika, the aquaria were carpeted with gravel, and flowerpots, some broken in two, were arranged as fish hideouts in the tanks. The researchers then followed the social structure of the fish communities through changes in coloration, at the same time noting the change in the length of each fish over the period of one week.

From their experiments, the researchers concluded that an alternating pattern of weight gain and loss underlies the cyclical pattern of being the winner and then the loser in male African cichlids. Non-territorial males grew faster than average, while territorial males showed slower growth, and in some cases shrank in size. With the losers gaining weight faster than the winners -- who were too involved in territory defense and mating to eat properly -- the losers soon became physically stronger. Once they gained a territory, the cascade of other physical changes began.

"With the same genes, you can get profound phenotypic changes, probably through differences in gene expression," says Hofmann.

The Fernald laboratory will continue to investigate how information about social status acts on an animal's body. "The transduction of social information into physiological consequences is very important to understand," Fernald says.

The information gained about a small African fish may be broadly applicable across the animal kingdom because of the conservation of genetic code through evolution, Fernald adds. In other words, the gene coding for a hormone in fish may be extremely similar to that in humans, and the mechanisms of hormonal control also may be similar. The African cichlid offers the Fernald team a versatile biological model, easily studied in its natural shallow pond habitat as well as in laboratory aquaria, where investigators can set up social systems under controlled conditions and can measure hormonal levels.

"We can capture the essence of how the system works in this fish model," says Fernald. SR

Anne M. Rosenthal is a freelance science writer.