Patterns of reproductive isolation in Eucalyptus – a phylogenetic perspective

We assess phylogenetic patterns of hybridisation in the speciose, ecologically and economically important genus Eucalyptus, in order to better understand the evolution of reproductive isolation. Eucalyptus globulus pollen was applied to 99 eucalypt species, mainly from the large commercially important subgenus, Symphyomyrtus. In the 64 species that produce seeds, hybrid compatibility was assessed at two stages, hybrid-production (at c. one month) and hybrid-survival (at nine months), and compared with phylogenies based on 8350 genome-wide DArT markers. Model fitting was used to assess the relationship between compatibility and genetic distance, and whether or not the strength of incompatibility ‘snowballs’ with divergence. There was a decline in compatibility with increasing genetic distance between species. Hybridisation was common within two closely related clades (one including E. globulus), but rare between E. globulus and species in two phylogenetically distant clades. Of three alternative models tested (linear, slowdown and snowball), we found consistent support for a snowball model, indicating that the strength of incompatibility accelerates relative to genetic distance. Although we can only speculate about the genetic basis of this pattern, it is consistent with a Dobzhansky-Muller-model prediction, that incompatibilities should snowball with divergence due to negative epistasis. Different rates of compatibility decline in the hybrid-production and hybrid-survival measures suggest that early-acting post-mating barriers developed first and are stronger than later-acting barriers. We estimated that complete reproductive isolation can take up to 21-31 million years in Eucalyptus. Practical implications for hybrid eucalypt breeding and genetic risk assessment in Australia are discussed