Evolutionary history shapes the susceptibility of an island tree flora to an exotic pathogen

• The exotic rust Puccinia psidii is threatening Australia’s rich myrtaceous flora.
• Seedlings of all Tasmanian eucalypt species were inoculated with P. psidii.
• Differences in response were detected among species and populations.
• Host species varied in susceptibility mainly due to subgeneric differences.
• Phylogeny better predicts susceptibility than endemism, habitat or range size.

With globalisation, the world’s native biotas are increasingly exposed to disease, parasitism, herbivory and competition from exotic organisms. The vulnerability of native biota to these exotic invasions is exacerbated by human disturbance and global climate change. Rust pathogens are some of the most important plant pathogens, including Puccinia psidii (myrtle rust or guava rust) that is now spreading worldwide at an alarming rate. P. psidii is native to South America and affects species in the family Myrtaceae, including the economically and ecologically important eucalypts. The Australian continent has a rich myrtaceous flora and is the centre of origin of most eucalypt species. P. psidii was first detected in Australia in 2010 and has since rapidly spread along its east coast. We assess the risk this exotic pathogen poses to the eucalypt flora of the southern Australian island of Tasmania, where the first incursion of P. psidii was detected in early 2015. Specifically, we tested the relative importance of phylogenetic history, habitat, endemism, and range size in predicting host susceptibility.Rust screening of seedlings from one to four populations of each of the 30 eucalypt species which are native to Tasmania, revealed significant genetic-based variation in response among host species and populations within the species. Significant population differences in susceptibility were detected in threatened, rare and endemic eucalypt species, as well as Australia’s main plantation eucalypt (Eucalyptus globulus) and the world’s tallest angiosperm species (Eucalyptus regnans). A significant proportion of the variation in host species susceptibility to this exotic pathogen was explained by phylogenetic history, while factors such as habitat, endemism and range size had no detectable effect. Species from subgenus Eucalyptus (13 species) were more susceptible than those from subgenus Symphyomyrtus (17 species) due to differences between the subgenera in the proportion of plants showing a symptomless response. These subgenera are here shown to differ in their leaf oil and wax chemistry. The potential contribution of these differences and other possible mechanisms causing these subgeneric differences in susceptibility are discussed. This study demonstrates the power of a phylogenetic approach to risk assessment for biosecurity and highlights the need for broader resistance screening within and between populations of species of high conservation or economic value.