Barley yellow dwarf viruses (BYDVs) preserved in herbarium specimens illuminate historical disease ecology of invasive and native grasses

Abstract

Summary 1 In plant invasion ecology, viruses and other pathogens are often considered in terms of the enemy release hypothesis, which predicts that plants become invasive in new ranges if they escape pathogens from their home range. However, pathogens may sometimes facilitate host spread rather than hinder it. 2 Previously, we hypothesized that apparent competition mediated by barley and cereal yellow dwarf viruses (Luteoviridae: BYDVs, CYDVs) may have facilitated historical grassland invasion in California, USA, where Eurasian grasses displaced native grasses in the 18th and 19th centuries (the disease facilitation hypotheses). However, this could have happened only if the viruses were present during the invasion, which is unknown. 3 To investigate the historical ecology of BYDVs in California grasses, we analysed preserved virus infections in herbarium specimens and used the historical virus sequences to determine rough time estimates of relevant phylogenetic events. 4 The historical viral RNA sequences we identified in invasive and native grasses date from 1917 and are among the oldest recovered from plants thus far and the oldest from North America. 5 Herbarium evidence and phylogenetic analysis suggest that BYDVs were likely to have been present in wild grasses during the California grassland invasion and to have shared some functional characteristics with present-day isolates, supporting the disease facilitation hypothesis. 6 We found evidence of virus spread from California to Australia (or, less likely, from Australia to California) in the late 19th century, when much horticultural exchange occurred, as well as potential correspondence in the timing of virus diversification events and the beginning of extensive human exchange between the Old and New Worlds. 7 Synthesis. Increasing evidence indicates that viruses are important in the ecology of grasslands and may, in some cases, mediate apparent competition among species. Historical data provide essential insight into plant virus ecology and suggest the need to examine human influence on plant virus diversification and spread within natural ecosystems.