Cover stories (110:9): Can disease resistance evolve independently at different ages? 

The cover image for our September issue features a pollinator approaching flowers of an alpine carnation with anthers carrying dark spores of  the anther-smut pathogen. This image relates to the research article: Can disease resistance evolve independently at different ages? Genetic variation in age-dependent resistance to disease in three wild plant species, by Emily Bruns et al. Here, Emily tells us the story behind the image.

A pollinator approaches flowers of an alpine carnation (Dianthus pavonius) with anthers carrying dark spores of  the anther-smut pathogen (Microbotryum dianthorum). This host-pathogen system from the Parco Naturale Del Marguareis, in north western Italy is used in the experimental described in our paper showing that resistance to this pollinator-transmitted disease varies significantly with host age and genotype. (Photo: Michael Hood)

Our paper in this issue of Journal of Ecology explores genetic variation in age-specific resistance to a sterilizing infectious disease in three wild plant species. A common pattern in animals and plants alike is that disease resistance increases with age. In agriculture, breeding for such ‘mature plant resistance’ can be a useful tool in disease control. Yet we know very little about how and why age-specificity in resistance evolves. One key question is whether resistance can evolve independently at juvenile and adult stages. In the paper we use greenhouse inoculation experiments to compare the correlations in susceptibility to anther-smut disease at different ages in three different host species in the carnation family (Caryophyllaceae). We show that in all three species, there are strong age-by-family interactions in infection rate, supporting the hypothesis that independent resistance evolution is possible. 

This study came about as a consequence of over 10 years of work studying the distribution and transmission dynamics of anther-smut diseases and their host plants in the Maritime Alps region of north western Italy (specifically within the Parco Naturale del Marguareis). Anther-smut pathogens that affect these plants, caused by fungi in the genus Microbotryum, are fascinating pathogens that reproduce by hijacking host flowering, forcing infected plants to produce spores in place of pollen and sterilizing their ovaries.  In the process, anther smut causes permanent and full sterilization of the host plants, without strongly impacting mortality. Transmission of the disease can occur through pollinator movement between adult plants or, as we are increasingly learning, through passive wind dispersal that can deliver the spores to seedlings and juveniles in proximity to the disease plants. In infected plants, the pathogen resides in the meristems asymptomatically until reproduction. Hence, if infection does occur at the seedling stage, it results in life-long sterilization. A wide range of perennial species in the Caryophyllaceae are infected by these anther-smut pathogens. In the current paper we investigated three of them: Silene latifolia, Silene vulgaris, and Dianthus pavonius.

Anther smut disease on three different host species near Valle Pesio, Cueno Province. From right to left: Silene latifolia, S. vulgaris, D. pavonius. (Photo: Emme Bruns)

The Parco Naturale del Marguareis, located within the Ente di gestione delle Aree Protette Alpi Marittime, is home to a rich diversity of caryophyllaceous species and their associated anther-smut fungi, including the three focal species in the current paper. In this regional park, there are two high alpine botanic gardens overseen by the park botanist, Dr. Bruno Gallino, and accessible from the nearby alpine refuge, Rifugio Garelli. Our work out there has been facilitated by an amazing team of botanists at the park’s biodiversity center, including Dr. Valentina Carasso and Ivan Pace, who have collaborated with us on this and other projects. Additional collaborators and many undergraduate students regularly participate in the fieldwork, including the three co-authors on the current paper, Indigo Ballistar, Liz Troy, and Jae-Hoon Cho.

Dianthus pavonius study site near Rifugio Garelli in the Parco Naturale del Marguareis.  Here mix of Italian and American scientists and students are setting up a transmission experiment. (Photo: Emme Bruns)

Our interest in age-specificity of resistance arose specifically from our long-term studies of anther-smut on Dianthus pavonius near Rifugio Garelli in the Parco Naturale del Marguareis. The plant species is endemic to the area but locally widespread in alpine meadows above 1500m. Our work over the last decade has shown that D. pavonius is commonly and persistently infected with anther-smut disease throughout its geographic range. Some of the highest rates of infection come from the population near the Rifugio Garelli, where the disease has been maintained a prevalence >40% for over a decade.

In this natural population of D. pavonius, we found that transmission occurs as much through passive aerial transmission to juvenile plants as by pollinator transmission to adult flowering plants. Inoculation studies showed that this dynamic is driven by the high susceptibility of plants in the seedling stage compared with stronger resistance of mature plants.

In our prior work, we had detected heritable variation in seedling resistance to anther-smut in three different host species (Silene latifolia, S. vulgaris, and D. pavonius), but had not investigated resistance variation at the adult stage. In the current paper, we quantified family-level variation in resistance at both juvenile and adult stages in all three species. We asked both whether resistance tends to increase overall as plants age, but also whether there are age-by-family interactions that would indicate that independent genetic control over age-specific resistance. We were specifically interested in this question, because strong age-by-family independent genetic control of resistance at different ages, would allow hosts to respond to selection independently at the juvenile and adult stages. We expect this potential to be important because, depending upon the host population’s spatial and demographic structure, there can be different selective pressures on when resistance is manifested during the host’s life cycle. We were therefore excited to find strong age-by-family interactions in resistance in all three focal host species.

While it has been frequently assumed that the susceptibility of juvenile individuals to infectious disease is due either to their small size and/or incomplete development, our study shows that this is unlikely to be the whole explanation. Resistance can be genetically determined, and independently so, at different ages and stages of development. Understanding how this variation responds to disease exposure that is often also age-specific is a major goal of our current studies.   

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