Virus coinfection in plants determined by ecological responses to environmental heterogeneity

Abstract

Community ecology is acknowledged as a relevant causative agent of epidemiological processes of plant viruses and has consequences for coinfection and virus and host evolution. Plant virus coinfection is common, but factors that promote non-random virus interactions above the population-level are unknown. Here, we analyse intrinsic and extrinsic factors in virus-host and virus-virus interactions by eighteen generalist virus species of a diverse multi-host-multi-virus system. Coinfection among viruses with broad host ranges, diverse modes of horizontal transmission, and interspecific variation in responses to environmental heterogeneity is expected to be shaped by ecological as well as evolutionary constraints. We analyse patterns of coinfection from 1,931 individual plants in 94 species from multiple plant communities of distinct habitat types and show that above 50% of plants were coinfected by 2-8 viruses. To analyse the role of environmental variables on the observed virus associations we used Markov and conditional random fields modelling. Results showed that a large majority of coinfections were random interactions, consistent with ecological fitting, and only a minor fraction being non-random associations. Random field models underscored the relevance of common responses to environmental heterogeneity driving coinfection, and strongly suggest mode of horizontal transmission as a causal agent. Results highlighted a major role of between-host, rather than within-host processes in driving coinfection. This study is a considerable addition to the understanding of drivers of virus coinfection and, hence, of virus community ecology and epidemiology.