Abstract

The ever increasing movement of viruses around the world poses a major threat to plants growing in cultivated and natural ecosystems. Both generalist and specialist viruses move via trade in plants and plant products. Their potential to damage cultivated plants is well understood, but little attention has been given to the threat such viruses pose to plant biodiversity. To address this, we studied their impact, and that of indigenous viruses, on native plants from a global biodiversity hot spot in an isolated region where agriculture is very recent (<185 years), making it possible to distinguish between introduced and indigenous viruses readily. To establish their potential to cause severe or mild systemic symptoms in different native plant species, we used introduced generalist and specialist viruses, and indigenous viruses, to inoculate plants of 15 native species belonging to eight families. We also measured resulting losses in biomass and reproductive ability for some host–virus combinations. In addition, we sampled native plants growing over a wide area to increase knowledge of natural infection with introduced viruses. The results suggest that generalist introduced viruses and indigenous viruses from other hosts pose a greater potential threat than introduced specialist viruses to populations of native plants encountered for the first time. Some introduced generalist viruses infected plants in more families than others and so pose a greater potential threat to biodiversity. The indigenous viruses tested were often surprisingly virulent when they infected native plant species they were not adapted to. These results are relevant to managing virus disease in new encounter scenarios at the agro-ecological interface between managed and natural vegetation, and within other disturbed natural vegetation situations. They are also relevant for establishing conservation policies for endangered plant species and avoiding spread of damaging viruses to undisturbed natural vegetation beyond the agro-ecological interface.

Highlights

  • Long before plants were first domesticated at the dawn of agriculture, viruses were evolving with native plants growing within undisturbed plant communities in different regions of the world

  • When 15 native plant species belonging to eight families were inoculated with 3–12 viruses each (Table 3), 11 species developed systemic infection with 1–5 viruses each, and only localised infection occurred in three species

  • We found (i) the introduced generalist and indigenous viruses both caused severe systemic symptoms and growth reductions when they infected some native plant species, (ii) the specialist viruses caused only mild or symptomless systemic infection, and (iii) three introduced generalist viruses were detected in natural vegetation at sites distributed widely at agro-ecological interfaces in the Southwest Australian Floristic region (SWAFR)

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Summary

Introduction

Long before plants were first domesticated at the dawn of agriculture, viruses were evolving with native plants growing within undisturbed plant communities in different regions of the world. Within the undisturbed native plant communities of today, virus infections derived from this process are often considered benign, causing little in the way of damage or symptoms due to a combination of natural control measures that operate to limit epidemics and the consequences of evolution with their hosts over millennia [2,3,4,5,6,7,8,9,10,11,12,13]. Mild infection in one host species in a mixed plant species population can provide a virus reservoir for spread to more sensitive host species, and, once infected, these decline due to lack of fitness and competitive ability [25,26]

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