Divergent life history shapes gene expression in brains of salmon

Roughly 15 percent of genes are expressed differently among males of same species

Scientists working with salmon have found that gene expression in the brain can differ significantly among members of a species with different life histories. Their study indicates that roughly 15 percent of Atlantic salmon genes show differential expression in males who migrate from their freshwater birthplaces to mature in oceans versus those who do not leave the freshwater environment to mature.

The researchers, at Harvard University, the University of Massachusetts and the US Geological Survey, report the finding in the current issue of Proceedings of the Royal Society B. They compared female salmon, male salmon that will eventually undertake the well-known journey from their river birthplaces to oceans –- and then migrate heroically back upstream one to three years later to spawn –- and males of the same age known as “sneakers” that mature at greatly reduced size without leaving freshwater.

“The finding that hundreds of the nearly 3,000 genes we studied were expressed differently in the brains of sneakers and other male salmon came as a surprise,” says Nadia Aubin-Horth, a postdoctoral researcher in the Bauer Center for Genomics Research in Harvard’s Faculty of Arts and Sciences. “Since these males of the same species in the same wild environment differed only in their life history, we did not expect the expression of so many of their genes to differ.”

Aubin-Horth and her colleagues were also surprised by some of the 17 separate classes of genes demonstrating differing activity levels.

“It makes sense that growth genes are suppressed in sneakers and genes associated with reproduction are expressed more, since these fish essentially trade bodily size for faster reproductive maturity,” she says. “However, it was unexpected, for instance, that genes associated with learning and memory would be expressed at higher levels in the brains of sneakers. It’s not yet clear why disparities like this would arise.”

Aubin-Horth says it is impossible to tell as of yet whether the changes in gene expression are a cause or effect of the various physiological differences between sneakers and other salmon. Their work suggests that the “default” life cycle, in which male salmon spend several years in oceans before returning to freshwater to reproduce, may actually result from active inhibition of development into a sneaker. Previous studies have found that the proportion of sneakers in various salmon populations varies wildly; it appears that males that grow fastest early in life go on to become sneakers.

The study by Aubin-Horth and her colleagues differed from most examinations of divergent life histories, in any vertebrate species, in that it combined the use of wild individuals, caught in a tributary of the Connecticut River in western Massachusetts, with new functional genomics technologies to simultaneously monitor thousands of genes in individual tissues.

“Research like this was very difficult in the past because we lacked adequate tools to measure gene expression,” Aubin-Horth says. “As a result almost nothing is known about the molecular basis of developmental plasticity such as that seen among ’sneaker’ salmon.”