Genetic mutations and the possible mechanisms underlying evolution have been studied in laboratory animals for decades, said David Kingsley, PhD, professor of developmental biology and assistant investigator for the Howard Hughes Medical Institute. The challenge has been to find a means of applying what scientists know to be true in the lab to systems in the natural world. In a paper published Dec. 20 in the journal Nature, Kingsley and his team propose that a small spiny fish called the three-spine stickleback, and the gene-linkage map of the fish's chromosomes that the team has developed, may be the tools evolutionary biologists have been needing.
The key, according to Kingsley, was to find two populations, that unlike laboratory bred mice and rats, would have traits that had evolved naturally and yet could still be cross-bred.
"What we needed were two species that had diverged fairly recently, had distinct morphological differences, were fast-growing and easy to keep in the laboratory," said Kingsley. It was also important to find two species, Kingsley said, that could produce viable offspring in the lab even if they would not naturally mate in the wild. The group's intent was to develop a map of the inheritance patterns showing the links between genes from one generation to another. According to Kingsley, it is a system used to study genetics in laboratory-bred mice, but he wanted to develop a system that could test inheritance patterns, mutations, and ultimately the mechanisms underlying evolution in natural populations.
"It's part of an age-old debate," Kingsley said. "Does evolution occur through infinitesimally small genetic changes involving a very large number of genes, or does it occur through changes of large effect associated with a smaller number of genes?" In the lab, according to Kingsley, much of the focus is on single gene mutations of large effect, but how does this apply to evolution as it occurs naturally? Kingsley and his team turned to the genetic architecture of two populations of sticklebacks for some answers.
"What made sticklebacks so appealing was that not only did they meet our criteria from a molecular and genetics standpoint, but their ecology and behavior has also been widely studied by many other researchers," Kingsley said.
To develop the gene-linkage map of the fish's genome, Kingsley's team first designed a marking system that would allow them to follow the inheritance patterns of various genes from one generation to the next. Using the markers, the team crossbred two populations - a near-shore invertebrate feeding species and an open-water plankton feeding species. They followed the patterns of inheritance through several generations, developing a genome-wide gene linkage map. Next, they used the map to analyze the genetic basis for a number of evolutionary changes that occurred in the two populations, such as the amount of body armor, the number of gill rakers and the length of the stickleback's spines.
Kingsley said they found a number of parallels between traditional laboratory genetics and the traits they examined in the stickleback populations. For example, many of the traits could be traced to major chromosome regions - indicating that evolution can occur through changes of large effect, not just as a series of small changes. Their findings also indicate that genetic control of body regions appears to be modular. The genes that control the length of the first dorsal spine, for instance, are located on different chromosome regions from the genes that control the length of the second dorsal spine. This is not surprising, said Kingsley, because it follows previous findings of the genetic control of mouse skeleton development. As anyone who plays with Legos can testify to, a modular body plan greatly increases the options for tweaking designs over time.
"The goal of this project was to develop a system that makes it possible to bring what we know in the laboratory about molecular genetics and begin applying it in the field to evolutionary theory and ecology," said Kingsley. The initial results, he said, suggest that these fish can now be used for detailed genetic studies of the mechanisms that control vertebrate evolution.
Other authors on the paper include first author Catherine Peichel, PhD, research associate with the Howard Hughes Medical Institute and Stanford Department of Developmental Biology, as well as Kirsten Nereng, PhD, Kenneth Ohgi, PhD, Bonnie Cole, and Pamela Colosimo, PhD, from the Stanford Department of Developmental Biology, Alex Buerkle, PhD, from the Department of Biology at the University of Wisconsin - Eau Claire, and Dolph Schluter, with the Zoology Department and Centre for Biodiversity at the University of British Columbia.
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