Epistasis causes outbreeding depression in eucalypt hybrids

The genetic architecture underlying species differentiation is essential for understanding the mechanisms of speciation and post-zygotic reproductive barriers which exist between species. We undertook line-cross analysis of multiple hybrid (F-1, F-2 and backcrosses) and pure-species populations of two diploid eucalypt species from different subseries, Eucalyptus globulus and Eucalyptus nitens, to unravel the genetic architecture of their differentiation. The populations were replicated on two sites and monitored for growth and survival over a 14-year period. The hybrids exhibited severe outbreeding depression which increased with age. Of the composite additive, dominance and epistatic effects estimated, the additive x additive epistatic component was the most important in determining population divergence in both growth and survival. Significant dominance x dominance epistasis was also detected for survival at several ages. While favourable dominance and, in the case of survival, dominance x dominance epistasis could produce novel gene combinations which enhance hybrid fitness, at the population level, these effects were clearly overridden by adverse additive x additive epistasis which appears to be a major driver of overall outbreeding depression in the hybrid populations. The lack of model fit at older ages suggested that even high-order epistatic interactions may potentially have a significant contribution to outbreeding depression in survival. The estimated composite genetic parameters were generally stable across sites. Our results argue that the development of favourable epistasis is a key mechanism underlying the genetic divergence of eucalypt species, and epistasis is an important mechanism underlying the evolution of post-zygotic reproductive barriers.