Classic evolutionary theories of senescence, or the evolution of the rate at which organisms deteriorate as they age, have been challenged by the findings of researchers at the University of California, Riverside.
In the 1950s, Peter Medawar, winner of a Nobel Prize for medicine, and George Williams, a renowned evolutionary biologist, developed theories for the evolution of senescence, which predicted that organisms that are exposed to high mortality imposed by external factors, like disease or predation, will evolve to deteriorate more rapidly as they get older. Their predictions have been widely accepted and are supported by some experiments. Now, a study by UC Riverside researchers comparing fish living in high- and low-predator environments has found that these classically held theories of aging fail to predict how aging has evolved in nature.
The research findings of David Reznick, a professor of biology at UCR, were published in an article titled "Effects of Extrinsic Mortality on the Evolution of Senescence in Guppies" in the Oct. 28 issue of Nature. Co-authors included UCR colleagues Michael J. Bryant and Derek Roff; and from Colorado State University, biologists Cameron K. and Dionna E. Ghalambor.
The research group studied 240 individually reared guppies, derived from four natural populations. The grandparents of these fish were collected from two watersheds in the Caribbean island of Trinidad. Each watershed held populations that lived either with or without predators and hence experienced either high or low mortality rates. The researchers evaluated aging in these fish by comparing their life spans, mortality rates, fertility, and their swimming performance. Some of their results were not predicted by theory.
"We instead found that senescence was a mosaic of traits," said Reznick. "The high-predation guppies have longer average and maximum lifespans. They have lower mortality rates throughout their lives. They have higher fecundity throughout their lives, plus the rate at which fecundity declines with age (a measure of reproductive senescence) declines less rapidly with age."
The only aspect of their results that was consistent with classical predictions was the rate of decline in acceleration and maximum swimming speed, which are analyses of neuromuscular performance. In youth, guppies from high-predation environments are faster than those from low predation environments. All guppies slowed down with age, but the rate of decline for fish in high-predation environments was faster so that, in old age, they were no longer faster than their low-predation counterparts.
The composite picture is that all of these fish deteriorate with age, but the comparative rates of deterioration is a mix of responses, most of which do not correspond to classical theory.
The researchers give three possible reasons for the unexpected results. All of these reasons are derived from newer theories for the evolution of senescence that have yet to receive serious consideration.
The first hinges on body size and fertility. Guppies in the high-predator environment grew more quickly and their rate of reproduction increased more rapidly with age, which offset some of the mortality rate differences with their low-predator counterparts.
Secondly, as predators killed guppies, they also reduced the population density of the survivors who, in turn, experienced higher food availability. More resources for the survivors can offset some of the predicted effects of higher mortality.
Thirdly, fish living in the high-predator environment may benefit from natural selection. Predators cull those who are slower and leave a higher proportion of quick fish that have high reproductive potential.
A high-predation environment therefore tends to select for fish that are quicker, live longer and maintain a higher level of performance and fertility, but whose swimming speed drops off more quickly with age. The differences between these results and the classical predictions gives cause to take the new, more derived, theories for the evolution of the aging process more seriously.
A National Science Foundation grant and the Academic Senate of the University of California supported the research.
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