From generalist to specialists: Variation in the host range and performance of anther-smut pathogens on Dianthus

Abstract

Determining the processes that drive the evolution of pathogen host range can inform our understanding of disease dynamics and the potential for host shifts. In natural populations, patterns of host range could be driven by genetically based differences in pathogen infectivity or ecological differences in host availability. In northwestern Italy, four reproductively isolated lineages of the fungal plant-pathogen Microbotryum have been shown to co-occur on several species in the genus Dianthus. We carried out cross-inoculation experiments to determine whether patterns of realized host range in these four lineages were driven by differences in infectivity and to test whether there was evidence of a trade-off between host range and within-host reproduction. We found strong concordance between field patterns of host range and pathogen infectivity on different Dianthus species using experimental inoculation, indicating that infection ability is a major driving force of host range. However, we found no evidence of a trade-off between the ability to infect a wider range of host species and spore production on a shared host.

Keywords: Generalist; Microbotryum; host range; infectivity; specialist; trade-offs.

Fig. 1.

Distribution and sampling locations for pathogen and host accessions used in Experiment 1. A) Distribution of three Dianthus host species (data from Bruns et al. 2018). Colors and shapes indicate host species identity. Points were jittered randomly to minimize overlap. The six locations where seeds were collected are shown in the brighter outlined shapes and labeled by locality. The yellow line is the border with France (where we do not have distribution data). The inset shows the general location in Italy. The closest city, Cuneo, is marked for reference. Inset: the general location in Italy. B) Distribution of the four Microbotryum lineages (L1-L4) in the Mediterranean Alps (data from Petit et al. 2017). The location of the 19 Microbotryum isolates tested in Experiment 1 are shown in white (see Table 1).

Fig. 2.

Comparison of the A) potential and B) realized host range of four Microbotryum lineages (L1-L4). A) Infection results from Experiment 1. Bars show the proportion of each host species infected by pathogen lineages L1-L4. Colors indicate host species: Dianthus pavonius (pink), D. seguieri (green), or D. furcatus (blue). Numbers indicate the total number that flowered and were scored. B) Field collections of the distribution of Microbotryum lineages on Dianthus species are shown for reference (data redrawn from Petit et al. 2017). Bars show the proportion of isolates from each lineage that were found on each host. Numbers of isolates in each category are indicated at the bottom. Error bars are 1 SEM.

Fig. 3.

Infectivity of Lineage 2 isolates collected from three different hosts-of-origin in Experiment 1. Asterisks indicate combinations where the pathogen was tested on its own host-of-origin. Numbers indicate the total number of inoculated plants that flowered and were scored for disease. Error bars 1 SEM.

Fig. 4.

Spore production of four pathogen lineages on Dianthus pavonius of infected plants in Experiment 1 that flowered in the first year. Colors and shapes indicate host-of-origin: Pink circles-Dianthus pavonius, Green squares- D. seguieri, Blue triangles-D. furcatus. Neither lineage nor host-of-origin was a significant predictor of spore production (Table 3).

Fig. 5.

Infectivity of a single isolate of Lineage 1 (pink) and a single isolate of Lineage 2, (blue) on eight different D. seguieri populations in Experiment 2. Large numbers indicate the population ID number (Table 1B), small numbers indicate the sample size of each treatment. Error bars are 1 SEM.