CHAMPAIGN, Ill. - Any owner of a freshwater aquarium likely has had guppies (Poecilia reticulata), those small brightly colored fish with a propensity for breeding. Now guppy populations manipulated in natural habitats in Trinidad have taught researchers an evolutionary lesson on the survival of a rare genetic trait.
Reporting in the June 1 issue of the journal Nature, scientists from six institutions detail how male guppies with the most colorful - and most rare - patterns are more likely than their more commonly colored counterparts to survive in the wild.
"This study provides very solid support for frequency-dependent survival," said principal investigator Kimberly A. Hughes, an animal biologist at the University of Illinois at Urbana-Champaign. "We found that rare color patterns of these guppies had a highly significant survival advantage."
In evolutionary terms, frequency-dependent survival means that individuals with rare gene variants have a survival advantage relative to common variants, simply as a function of being rare. This process is important because it leads to the maintenance of many different variants (polymorphism) in the same population.
The same process could be important in the maintenance of genetic variants in humans, said Hughes, who also is a member of the Institute for Genomic Biology at Illinois.
For example, she said, it has been hypothesized that genes involved in pathogen resistance (the Human Leukocyte Antigen or HLA genes) are highly polymorphic because pathogens are most successful at attacking individuals with common variants, and individuals with rare variants have higher survival.
However, the theory is difficult to test, and, in general, frequency-dependent survival has been difficult to document as an important process in nature, Hughes said.
The guppy system provided a way to test whether this kind of selection could really promote polymorphism in a natural setting, because guppies are highly polymorphic for a visible trait and they are easy to work with in field experiments.
Researchers conducted 34 separate manipulations across 19 replicate pools in three streams over four years. They collected guppies from two tributaries of the Quare River and the main branch of the Mausica River, sorted the males and females, and then returned them to the streams.
"We had two different color patterns at a particular site," Hughes said. "In half the replicates we made pattern 1 rare and pattern 2 common, and in the other replicates we made pattern 2 rare and pattern 1 common. This allowed us to determine that it was rarity itself, and not any specific aspect of the color pattern that had the biggest effect on survival. No matter which pattern was rare or common, the rare type had higher survival."
After 15 or 17 days, depending on location, the researchers again sought and captured all adult-sized guppies from the streams. The rare males had higher survival at all three sites. Overall, 84 percent of the rare-type males survived to the end of the experiment, while only 69 percent of the common-type males survived.
The most important source of mortality in wild guppies is predation by larger fish species that live in the same streams. "It's possible that guppy predators, which are known to hunt visually, may be more focused on common color patterns," Hughes said.
"Predators can form 'search images' of the most common prey types, and can be less efficient at locating and capturing prey that look different from the norm," she said. "These predators have limited attention. Perhaps this generates a frequency-dependent predation pattern that by its very operation acts to maintain polymorphism."
An alternative theory is that male guppies altered their own behavior in response to the manipulated changes in their common vs. rare numbers, and that the changed behaviors affected predation, the authors wrote. They suggest new experiments to study behaviors in both predators and prey to determine which theory is at work.
In earlier studies, Hughes and colleagues had shown that female guppies prefer to mate with males with color patterns novel to the females. It could be, the authors surmise in the Nature paper, that females might prefer the rare males because mating with them lowers their own risk to predation.
The six co-authors with Hughes were: Robert Olendorf, a postdoctoral researcher in the School of Integrative Biology at Illinois; F. Helen Rodd and David Punzalan, department of zoology at the University of Toronto; Anne E. Houde, department of biology at Lake Forest College in Illinois; Carla Hurt of the Smithsonian Tropical Research Institute, Naos Marine Laboratory, Panama City, Panama; and David N. Reznick, department of biology, University of California at Riverside.
The work was supported by grants from the National Science Foundation to Hughes, Houde and Reznick, and by a grant from the Natural Sciences and Engineering Research Council of Canada to Rodd. During 1996, Hughes also was supported by a National Research Service Fellowship from the National Institutes of Health, and Rodd by a grant from the Center for Population Biology at the University of California at Davis.