Taxonomic similarity, more than contact opportunity, explains novel plant–pathogen associations between native and alien taxa

Abstract

Novel associations between plants and pathogens can have serious impacts on managed and natural ecosystems world-wide. The introduction of alien plants increases the potential for biogeographically novel plant-pathogen associations to arise when pathogens are transmitted from native to alien plant species and vice versa. We quantified biogeographically novel associations recorded in New Zealand over the last 150 yr between plant pathogens (fungi, oomycetes and plasmodiophorids) and vascular plants. We examined the extent to which taxonomic similarity, pathogen traits, contact opportunity and sampling effort could explain the number of novel associates for host and pathogen species. Novel associations were common; approximately one-third of surveyed plants and pathogens were recorded with at least one biogeographically novel associate. Native plants had more alien pathogens than vice versa. Taxonomic similarity between the native and alien flora and the total number of recorded associations (a measure of sampling effort) best explained the number of novel associates among species. The frequency of novel associations and the importance of sampling effort as an explanatory variable emphasize the need for effective monitoring and risk assessment tools to mitigate the potential environmental and economic impact of novel pathogen associations.

Invasion Science: A Horizon Scan of Emerging Challenges and Opportunities

“…For example, Eurasian field pennycress (Thlaspi arvense) is proposed for widespread commercial production in North America [21]. Introductions of such new crops will enable plant pathogens to jump from cultivated hosts to native species [22]. Two other emerging trends of food production pose novel risks.…”

The emerging science of linked plant–fungal invasions

“…Heteroecious fungal pathogens, which require more than one plant host to complete their life cycle, face a particularly high barrier to invasion. The invasion success of rusts (Desprez‐Loustau et al ., ; Bufford et al ., ), which are often heteroecious and highly host‐specific, may thus seem puzzling. In this case, other fungal traits, including high dispersal ability and ability to undergo multiple asexual cycles on alternate hosts, may reduce the importance of host specificity in limiting invasion (Philibert et al ., ).…”

“…Novel associations occur where an alien plant or fungus interacts with symbionts not found in its native range. The extent of novel associations may be influenced by the degree of phylogenetic relatedness between the invasive plant and resident species in the area of introduction (Vacher et al, 2010;Bufford et al, 2016), as phylogenetically close species tend to share more pathogens (Parker et al, 2015;Gilbert & Parker, 2016) and, potentially, mutualists.…”

Novel interactions between alien pathogens and native plants increase plant–pathogen network connectance and decrease specialization

“…In plant-pathogen networks, modules are often correlated with host phylogeny when groups of related plant species tend to be colonized by a shared suite of pathogens TA B L E 1 A brief description of common metrics that describe network architecture and function and the predicted relative values of these metrics in networks of novel interactions, as compared with the metrics in non-novel networks (Andreazzi et al, 2017) (Elias, Fontaine, & van Veen, 2013;Vacher, Piou, & Desprez-Loustau, 2008). We expect module composition in novel native plant-alien pathogen networks to show a strong signal of host phylogeny if alien pathogens are pre-adapted to colonize novel hosts in the new range that are closely related to hosts from the pathogen's native range (Bufford et al, 2016;Gilbert, Magarey, Suiter, & Webb, 2012;Parker et al, 2015). However, over time pathogens may also shift to colonize co-occurring, but less closely related, plant species (Parker & Gilbert, 2004).…”