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Unleashing genetic diversity

Mutation in hormonal pathway can reveal environment-dependent phenotypes

By | February 3, 2006

In this week's Science, researchers report that polyphenisms - distinct phenotypes emerging from identical genomes - can evolve through genetic stabilization of a stress-induced phenotype. The authors suggest that complex traits, such as color change, may evolve suddenly when a mutation in a developmental hormone reveals previously hidden genetic diversity. The study makes an important contribution to understanding how polyphenic systems could evolve, according to David Pfennig of the University of North Carolina at Chapel Hill, who was not involved in the study. "We don't know a lot about the origins of these kinds of polyphenisms," Pfennig said. As part of the study, Yuichiro Suzuki and H. Frederik Nijhout of Duke University in North Carolina artificially selected for coloration change in response to heat stress in tobacco hornworm larvae. Ten generations of selection resulted in caterpillars polyphenic for larval color, with corresponding changes in levels of a developmental hormone. In the hornworm Manduca quinquemaculata, larvae are black if they develop at 20oC, but green if they develop at 28oC. The authors reasoned that they might be able to evolve this polyphenism by putting thermal stress on the closely related non-polyphenic species Manduca sexta, Suzuki said, "because there might be some underlying genetic mechanisms that are conserved." Wild-type M. sexta are green, while the black mutant strain contains a sex-linked recessive allele that reduces secretion of juvenile hormone (JH). Reduced JH results in upregulated melanin, and the caterpillars become black. The black mutation probably allows increased heat absorption, Suzuki said, while the wild-type green blends with the animals' environment. "It's a tradeoff between thermoregulation and camouflage," he told The Scientist. The authors heat-shocked these black mutants during larval development, producing a wide array of phenotypes, from black to nearly normal green. They then selected for two different lines of caterpillars: those that became most green after heat shocks, and those that remained most black. A control line was heat-shocked every generation but not selected. They found that selection resulted in heritable color changes among the caterpillars. Color variation was continuous, indicating that coloration is under control of multiple genes. The line selected for black color lost its response to heat shocks after about the seventh generation of selection, and thereafter remained completely black in all temperatures. The line selected for greenness, however, developed a polyphenism: the larvae from this line turn green abruptly at about 28oC. The researchers found that the critical period for heat shock application corresponded to the developmental time point when juvenile hormone (JH) normally determines epidermal color, Suzuki said. They also found that heat-shocked polyphenic larvae had significantly higher JH titer during the critical period than did monophenic larvae. "They're artificially selecting on other gene loci that then affect patterns of juvenile hormone release," said Wade Hazel of DePauw University in Indiana, who was not involved in the study. Their results suggest that changes in hormonal regulation may underlie polyphenism evolution, the authors say. In wild-type caterpillars, JH is present at such a high level that the larvae are green at every temperature. But when the black mutation brings JH concentration closer to a threshold level, Suzuki said, then environmental changes in temperature can determine coloration phenotype. "There may have already been genetic mutations to produce this phenotype, but they were basically being masked" by high levels of JH, UNC's Pfennig said. "It's a pretty convincing demonstration and it's a really nice model," said Hazel, and their results fit well with previous theoretical work. Still, Hazel noted that he would have liked to see "whether these hormonal changes that they document in their selected lines actually occur in the species that exhibits the polyphenism in the wild." Besides examining the evolution of a polyphenism, "the more general issue that this paper touches on is: where do novel traits come from?" Pfennig said. Although there are not yet many examples of novel complex traits emerging from mutations in developmental pathways, Suzuki said, "I think we are going to find that that might be more common than is currently appreciated." Melissa Lee Phillips mlp@nasw.org Links within this article Y. Suzuki, H.F. Nijhout, "Evolution of a polyphenism by genetic accommodation," Science, February 3, 2006. http://www.sciencemag.org J.B. Weitzman, "Making ant wings," The Scientist, July 16, 2002. http://www.the-scientist.com/article/display/20528/ David Pfennig http://www.bio.unc.edu/faculty/pfennig/ Yuichiro Suzuki https://fds.duke.edu/db/aas/Biology/grad/ys16 H. Frederik Nijhout http://www.biology.duke.edu/nijhout/ T. Toma, "Genes for jobs", The Scientist, September 26, 2003. http://www.the-scientist.com/article/display/21622/ Wade Hazel http://www.depauw.edu/acad/biology/Websites/Wade%20Hazel/wade_hazel.htm W. Hazel et al., "The ecological genetics of conditional strategies," American Naturalist, June 2004. PM_ID: 15266386
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