Evolutionary trait‐based approaches for predicting future global impacts of plant pathogens in the genus Phytophthora

Abstract

Plant pathogens are introduced to new geographical regions ever more frequently as global connectivity increases. Predicting the threat they pose to plant health can be difficult without in‐depth knowledge of behaviour, distribution and spread. Here, we evaluate the potential for using biological traits and phylogeny to predict global threats from emerging pathogens. We use a species‐level trait database and phylogeny for 179 Phytophthora species: oomycete pathogens impacting natural, agricultural, horticultural and forestry settings. We compile host and distribution reports for Phytophthora species across 178 countries and evaluate the power of traits, phylogeny and time since description (reflecting species‐level knowledge) to explain and predict their international transport, maximum latitude and host breadth using Bayesian phylogenetic generalised linear mixed models. In the best‐performing models, traits, phylogeny and time since description together explained up to 90%, 97% and 87% of variance in number of countries reached, latitudinal limits and host range, respectively. Traits and phylogeny together explained up to 26%, 41% and 34% of variance in the number of countries reached, maximum latitude and host plant families affected, respectively, but time since description had the strongest effect. Root‐attacking species were reported in more countries, and on more host plant families than foliar‐attacking species. Host generalist pathogens had thicker‐walled resting structures (stress‐tolerant oospores) and faster growth rates at their optima. Cold‐tolerant species are reported in more countries and at higher latitudes, though more accurate interspecific empirical data are needed to confirm this finding. Policy implications. We evaluate the potential of an evolutionary trait‐based framework to support horizon‐scanning approaches for identifying pathogens with greater potential for global‐scale impacts. Potential future threats from Phytophthora include Phytophthora x heterohybrida, P. lactucae, P. glovera, P. x incrassata, P. amnicola and P. aquimorbida, which are recently described, possibly under‐reported species, with similar traits and/or phylogenetic proximity to other high‐impact species. Priority traits to measure for emerging species may be thermal minima, oospore wall index and growth rate at optimum temperature. Trait‐based horizon‐scanning approaches would benefit from the development of international and cross‐sectoral collaborations to deliver centralised databases incorporating pathogen distributions, traits and phylogeny.

Pathogens co-transported with invasive non-native aquatic species: implications for risk analysis and legislation

“…While limitations exist with respect to INNS data, the increasing use of histological, eDNA, and molecular diagnostics also offer new opportunities for monitoring INNS, potentially enabling the capture of pathological data more easily. Innovative modelling approaches, such as those using evolutionary trait-based frameworks (Barwell et al 2020), can also inform horizon scanning and risk assessment to identify potentially impactful pathogens.…”

Towards a phylogenetic ecology of plant pests and pathogens

“…Phytophthora ramorum, Phytophthora nicotianae) infect plant hosts across the vascular plant tree of life-including ferns, gymnosperms, and angiosperms. Previous work on Phytophthora has found growth rate, desiccation resistance, and time since description to be important predictors of the number of host families Phytophthora species can infect [43]. We propose that host breadth could also be affected by the diversity of plant tissues the pathogens can attack (figure 3; see the electronic supplementary material, Methods).…”

PHYTO-THREATS: Addressing Threats to UK Forests and Woodlands from Phytophthora; Identifying Risks of Spread in Trade and Methods for Mitigation

“…Data were therefore insufficient for most species to model the environmental niches or landscape-scale drivers of spread. This highlights the disproportionately low global recording effort for pathogen taxa (versus plant host taxa or taxa of conservation concern) and the importance of initiatives to develop centralised, crosssectoral databases for plant pathogens to enable a comprehensive understanding of their behaviour and potential for spread between hosts and habitats [42]. The biological traits database [31] was compiled through literature review and expertise of project pathologists together with pathologists in Australia (T. Burgess and G. Hardy, Murdoch University) and New Zealand (P. Scott and N. Williams, Scion).…”

“…Ten traits were used to predict global impacts of Phytophthora (number of countries reached, latitudinal limits and number of host plant families). These traits are related to growth (i.e., minimum and optimum temperatures for growth, growth rate at optimum temperature), survival, persistence and reproduction (presence of hyphal swellings, chlamydospores, oospores and oospore wall index), dispersal, (i.e., caducous sporangia, proliferating sporangia), and disease symptoms (ability to cause root and foliar disease) [42]. Most of these traits have historically been collected for use in morphological identification of species; however, their functional significance is less well understood.…”