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Host evolutionary relationships explain tree mortality caused by a generalist pest-pathogen complex.

ABSTRACT: The phylogenetic signal of transmissibility (competence) and attack severity among hosts of generalist pests is poorly understood. In this study, we examined the phylogenetic effects on hosts differentially affected by an emergent generalist beetle-pathogen complex in California and South Africa. Host types (non-competent, competent and killed-competent) are based on nested types of outcomes of interactions between host plants, the beetles and the fungal pathogens. Phylogenetic dispersion analysis of each host type revealed that the phylogenetic preferences of beetle attack and fungal growth were a nonrandom subset of all available tree and shrub species. Competent hosts were phylogenetically narrower by 62 Myr than the set of all potential hosts, and those with devastating impacts were the most constrained by 107 Myr. Our results show a strong phylogenetic signal in the relative effects of a generalist pest-pathogen complex on host species, demonstrating that the strength of multi-host pest impacts in plants can be predicted by host evolutionary relationships. This study presents a unifying theoretical approach to identifying likely disease outcomes across multiple host-pest combinations.

SUBMITTER: Lynch SC

PROVIDER: S-EPMC8061262 | biostudies-literature | 2021 Apr

REPOSITORIES: biostudies-literature

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Host evolutionary relationships explain tree mortality caused by a generalist pest-pathogen complex.

Lynch Shannon Colleen SC Eskalen Akif A Gilbert Gregory S GS

Evolutionary applications 20210105 4

The phylogenetic signal of transmissibility (competence) and attack severity among hosts of generalist pests is poorly understood. In this study, we examined the phylogenetic effects on hosts differentially affected by an emergent generalist beetle-pathogen complex in California and South Africa. Host types (non-competent, competent and killed-competent) are based on nested types of outcomes of interactions between host plants, the beetles and the fungal pathogens. Phylogenetic dispersion analys ...[more]

PMID: 33897822

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Project description:The several meanings for the term “symbiosis” create confusion, which can be avoided when the author provides details of the interrelationships between the symbiotic organism and the “host” so that a reader can clearly understand what definition is implied in each case. For example, we, as opposed to many other mentioned readers, consider a symbiont as an organism living in an association with another regardless of whether it causes a pathologic response or not, but from our title, the reader may incorrectly infer that we consider a parasite to be different from a symbiont. A symbiont is an organism that uses another organism as a habitat. This chapter discusses the primary associations and associated conflicts involving the terminology. It also provides both differentiation between and conflicting views regarding the interpretation of the terms “infect” and “infest,” “infection” and “disease,” and other terms. Many seemingly harmless symbionts of a wide array of taxonomic groups are triggered to become pathogenic or virulent, and we provide several examples of the provoking (stimulating) triggers, with the understanding that in most cases, the conditions for the triggered activities are much more complex and complicated than presented. Examples of triggers follow: environmental ones like temperature, toxic chemicals (dose), chemotherapeutics, dietary changes, and geographic habits; internal ones like host site, host resistance or susceptibility, and host modifications; and combinations of these and other conditions. We provide examples involving multiple triggers for organisms associated with termites, for an endemic virus being affected by multiple factors and having multiple effects on its commercial penaeid shrimp hosts, and for contrasting variables associated with two exotic viruses in wild and cultured commercial penaeid shrimps with an emphasis on hypothesizing how the pathogenicity developed in these two viruses. The chapter ends by trying to answer the question of why would a symbiont become pathogenic in some hosts and not in others from an evolutionary perspective. It uses two hypotheses to explain the increased virulence.

Project description:The degree to which plant pathogen infestation occurs in a host plant is expected to be strongly influenced by the level of species diversity among neighbouring host and non-host plant species. Since pathogen infestation can negatively affect host plant performance, it can mediate the effects of local biodiversity on ecosystem functioning.We tested the effects of tree diversity and the proportion of neighbouring host and non-host species with respect to the foliar fungal pathogens of Tilia cordata and Quercus petraea in the Kreinitz tree diversity experiment in Germany. We hypothesized that fungal pathogen richness increases while infestation decreases with increasing local tree diversity. In addition, we tested whether fungal pathogen richness and infestation are dependent on the proportion of host plant species present or on the proportion of particular non-host neighbouring tree species.Leaves of the two target species were sampled across three consecutive years with visible foliar fungal pathogens on the leaf surface being identified macro- and microscopically. Effects of diversity among neighbouring trees were analysed: (i) for total fungal species richness and fungal infestation on host trees and (ii) for infestation by individual fungal species.We detected four and five fungal species on T. cordata and Q. petraea, respectively. High local tree diversity reduced (i) total fungal species richness and infestation of T. cordata and fungal infestation of Q. petraea and (ii) infestation by three host-specialized fungal pathogen species. These effects were brought about by local tree diversity and were independent of host species proportion. In general, host species proportion had almost no effect on fungal species richness and infestation. Strong effects associated with the proportion of particular non-host neighbouring tree species on fungal species richness and infestation were, however, recorded.Synthesis. For the first time, we experimentally demonstrated that for two common forestry tree species, foliar fungal pathogen richness and infestation depend on local biodiversity. Thus, local tree diversity can have positive impacts on ecosystem functioning in managed forests by decreasing the level of fungal pathogen infestation.

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Host evolutionary relationships explain tree mortality caused by a generalist pest-pathogen complex.

Publications

Host evolutionary relationships explain tree mortality caused by a generalist pest-pathogen complex.

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