Sci. Aging Knowl. Environ., 27 October 2004
Vol. 2004, Issue 43, p. nf97
[DOI: 10.1126/sageke.2004.43.nf97]


Prey for Long Life

The hunted don't necessarily age quickly

R. John Davenport

An inspirational guest on the Sally Jesse Raphael show might tell viewers to make the most of the time they have. Organisms naturally follow that advice, at least according to classical evolutionary theory: To maximize their chances of passing their genes to offspring, they fall apart at different rates, depending on their prospects for survival. But a new study suggests that the simple rule doesn't always apply. Belying the theory, tropical guppies menaced by ravenous predators age more slowly than do guppies from more peaceful waters. The work suggests that scientists need to use more refined theories to describe how evolution shapes life span.

When predators abound, investing energy in long-term survival is wasteful, classical evolutionary theory predicts (see Williams Classic Paper). Instead, animals should mature quickly and reproduce prolifically. As a result, creatures that have predators gnawing at their tails should evolve to mature--and age--rapidly. Studies in the wild and in the lab have supported the idea. For instance, opossum populations that live on islands die at a slower rate than do animals on the mainland, where predators lurk. And when scientists kill off high proportions of lab fruit flies, the insect population gradually evolves to age more rapidly. But some scientists have proposed that theories need to incorporate factors besides predation in order to describe most real-world situations.

To examine that idea more closely, evolutionary biologist David Reznick of the University of California, Riverside, and colleagues studied guppies that ply streams on the Caribbean island of Trinidad. Waterfalls sequester large predator fish such as cichlids in the lower reaches of the stream, but guppies live throughout. Reznick previously found that upstream fish die at a rate 20 to 30 times lower than that of downstream fish, suggesting that guppies might allow researchers to put the evolutionary theory of predation and aging to the test.

He and his team wanted to gauge guppies' internal aging clock. They captured upstream and downstream fish and bred each group separately in the lab for two generations. Then they calculated the aging rate, a measure that included the likelihood of a young fish dying and how rapidly that probability rises over a fish's lifetime. Animals from streams riddled with guppy-hungry predators aged more slowly than did fish from environments with fewer predators, an apparent contradiction to the classical theory. The downstream guppies' mortality rate rose more quickly than did the upstream guppies'. However, their initial mortality rate was lower, and their death rate never caught up to that of upstream guppies of the same age. Researchers traditionally use the slope of the curve--how mortality increases with age--as a gauge of senescence rate, says Reznick, but they need to take the starting point--initial mortality--into consideration when trying to compare the aging rates among different populations.

Next, the team assessed other aspects of guppy physiology. They measured how quickly fish sped out of a dead stop, a gauge of their ability to evade approaching predators. This capability declined more quickly as downstream fish aged than as upstream fish aged, matching classical theory. Guppies from high-predation environments matured more quickly and had more offspring than did those from low-predation regions, in agreement with classical theories. However, fish from high-predation environments reproduced for longer periods than did those from low-predation regions, contradicting the conventional view. "What it says is that the importance of [predation] depends on the context," says Reznick. Predation does more than just increase mortality. It lowers population density, leaving more resources for the fish that survive, for instance. "The classical theory didn't consider the context," he says.

"The original theory is really simplified," says comparative gerontologist Steven Austad of the University of Texas Health Sciences Center in San Antonio. "It makes tons of assumptions, and in previous studies those assumptions have been met." The new work shows that "the universe of outcomes is really quite complicated," he says. The study "moves the whole field forward by testing these ideas [of evolutionary theory] in the wild," says evolutionary biologist Daniel Promislow of the University of Georgia in Athens. "Is this a refutation of classical thinking? Not really," says evolutionary biologist Stephen Stearns of Yale University in New Haven, Connecticut. "But it's a useful guide to how we should think in a more sophisticated way." Guppies might have some more wisdom to share about how lurking danger--and other forces--shape aging.

October 27, 2004
  1. D. N. Reznick, M. J. Bryant, D. Roff, C. K. Ghalambor, D. E. Ghalambor, Effect of extrinsic mortality on the evolution of senescence in guppies. Nature 431, 1095-1099 (2004).
Citation: R. J. Davenport, Prey for Long Life. Sci. Aging Knowl. Environ. 2004 (43), nf97 (2004).

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