Testing the 'hybrid susceptibility' and 'phenological sink' hypotheses using the P. balsamifera - P. deltoides hybrid zone and septoria leaf spot [Septoria musiva

Jared M Leboldus,Peter Blenis,Nathalie Isabel,Kevin D Floate,Barb R Thomas,Daniel Ballhorn

doi:10.1371/journal.pone.0084437

Abstract

Hybrid genotypes that arise between plant species frequently have increased susceptibility to arthropod pests and fungal pathogens. This pattern has been attributed to the breakdown of plant defenses (‘Hybrid susceptibility’ hypothesis) and (or) to extended periods of susceptibility attributed to plant phenologies in zones of species overlap and (or) hybridization (‘phenological sink’ hypothesis). We examined these hypotheses by assessing the susceptibility of parental and hybrid Populus host genotypes to a leaf spot disease caused by the fungal pathogen Septoria musiva. For this purpose, 214 genotypes were obtained from morphologically pure zones of P. balsamifera and P. deltoides, and from an intervening zone of overlap and hybridization on the drainage of the Red Deer River, Alberta, Canada. Genotypes were identified as P. balsamifera, P. deltoides, or hybrid using a suite of 27 species-specific SNP markers. Initially the genetic structure of the hybrid zone was characterized with 27.7% of trees classified as admixed individuals. To test the hybrid susceptibility hypothesis, a subset of 52 genotypes was inoculated with four isolates of S. musiva. Levels of susceptibility were P. balsamifera > F1 hybrid > P. deltoides. A further 53 genotypes were grown in a common garden to assess the effect of genotype on variation in leaf phenology. Leaf phenology was more variable within the category of hybrid genotypes than within categories of either parental species. Leaf phenology was also more variable for the category of trees originating in the hybrid (P. balsamifera – P. deltoides [hybrid and parental genotypes combined]) zone than in adjacent pure zones of the parental species. The results from the inoculation experiment support the hybrid intermediacy hypothesis. The results from the common garden experiment support the ‘phenological sink’ hypothesis. These findings have greatly increased our understanding of the epidemiology and ecology of fungal pathogens in plant hybrid zones.

Highlights

Natural hybrid zones frequently have been observed to support greater abundances of insects and pathogens than the parental host species [1]
Using the drainage of the Red Deer River as a model system, we examined the susceptibility of the two pure parental species, P. balsamifera and P. deltoides, and their hybrids to different isolates of S. musiva
Source trees were collected in zones of pure P. balsamifera (B), pure P. deltoides (D) and hybridization (P. balsamifera – P. deltoides; hereafter designated B – D) as defined by Floate [8] based on leaf morphology

Summary

Introduction

Natural hybrid zones frequently have been observed to support greater abundances of insects and pathogens than the parental host species [1]. Within these zones, hybrid genotypes may be comprised of F1 intermediates and a range of complex backcrosses [2], [3] with different levels of susceptibility both within and among hybrid categories. The genetic models do not apply to the inheritance of specific genes or groups of genes, but rather to overall changes in resistance and susceptibility They are defined as follows: (i) hybrid susceptibility: hybrids are more susceptible than either parental species; (ii) hybrid resistance: hybrids are more resistant than either parental species; (iii) ‘additive hypothesis’: hybrids are intermediate in resistance as compared to both parental species; and (iv) the ‘dominance hypothesis’: hybrids have the same resistance or susceptibility as one of the parental species [2]

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Conclusion