Impact of high predation risk on genome-wide hippocampal gene expression in snowshoe hares

Abstract

The population dynamics of snowshoe hares (Lepus americanus) are fundamental to the ecosystem dynamics of Canada's boreal forest. During the 8- to 11-year population cycle, hare densities can fluctuate up to 40-fold. Predators in this system (lynx, coyotes, great-horned owls) affect population numbers not only through direct mortality but also through sublethal effects. The chronic stress hypothesis posits that high predation risk during the decline severely stresses hares, leading to greater stress responses, heightened ability to mobilize cortisol and energy, and a poorer body condition. These effects may result in, or be mediated by, differential gene expression. We used an oligonucleotide microarray designed for a closely-related species, the European rabbit (Oryctolagus cuniculus), to characterize differences in genome-wide hippocampal RNA transcript abundance in wild hares from the Yukon during peak and decline phases of a single cycle. A total of 106 genes were differentially regulated between phases. Array results were validated with quantitative real-time PCR, and mammalian protein sequence similarity was used to infer gene function. In comparison to hares from the peak, decline phase hares showed increased expression of genes involved in metabolic processes and hormone response, and decreased expression of immune response and blood cell formation genes. We found evidence for predation risk effects on the expression of genes whose putative functions correspond with physiological impacts known to be induced by predation risk in snowshoe hares. This study shows, for the first time, a link between changes in demography and alterations in neural RNA transcript abundance in a natural population.

Population cycles: generalities, exceptions and remaining mysteries

“…This points to the need to know what triggers changes in reproduction associated with outbreak density. As suggested for snowshoe hares, epigenetic changes to genes related to stress responses [46,94] or for grouse [95] and insects [96] to disease resistance, might be occurring.…”

Using experimentation to understand the 10‐year snowshoe hare cycle in the boreal forest of North America

“…It does not appear to be due to genetic changes (Sinclair, Chitty, Stefan, & Krebs, 2003). Changes in gene expression have been found (Lavergne, McGowan, Krebs, & Boonstra, 2014) and the most plausible hypothesis is that these changes are linked to epigenetic changes in expression of key regulatory genes, especially those affecting the stress axis (Ho & Burggren, 2010 following the decline (Figure 4). If there is stress-induced maternal programming of offspring that persists into adulthood, this could explain the low phase.…”

Ecophysiological effects of predation risk; an integration across disciplines

“…Predation is a central organizing process in ecology (Krebs et al 2001;Schmitz 2008). Since the inception of the discipline, ecologists have strived to understand the importance of the direct effects of predation-mainly the killing of prey.…”