Population Dynamics and Genetics of Plant Disease: A Case Study of Anther-Smut Disease

This is the publisher's version, also available electronically from http://www.jstor.org/stable/info/2265569A model by Levin and Udovic (1977) emphasizes the need for integration of studies of the numerical abundances and genetic composition of host and pathogen species. We use their conceptual framework to summarize our collaborative research on the ecological genetics of the anther-smut disease of Silene alba caused by the fungus Ustilago violacea. Our theoretical investigations have revealed the importance of the rate and mode of disease transmission on the likelihood of coexistence between host and pathogen. Our empirical studies have quantified patterns of disease spread on local and regional spatial scales and have shown that host genotypes differ greatly in resistance. Comparable genetic variation in pathogen virulence has not yet been demonstrated. The genetic composition of host populations alters numerical dynamics in experimental populations: disease declines in resistant populations, while host and pathogen appear to coexist in susceptible populations. Ecological outcomes also may be affected by the negative relationship between disease incidence and host flowering time, which may constitute a "cost" to resistance. We are currently expanding our work on the ecology and genetics of metapopulation dynamics of host and pathogen

The Distribution of Mating-Type Bias in Natural Populations of the Anther-Smut Ustilago violacea on Silene alba in Virginia

This is the publisher's version, also available electronically from http://www.jstor.org/stable/info/3761395.Complete individual-wide mating-type bias (retrieval of sporidia of only one mating type from germinated teliospores of one fungal individual) was observed to be a common and widespread feature of the anther-smut fungus, Ustilago violacea, collected from natural populations of its host, Silene alba. The bias was usually to mating type A1, but the frequency of bias and its spatial distribution varied from region to region. Populations with high frequencies of bias still showed high rates of disease transmission. Crosses between A1 mating type sporidial lines from completely biased individuals and A2 mating types from unbiased individuals showed no bias in the progeny. During teliospore germination, biased individuals often showed conjugation among adjacent cells of the promycelium, suggesting that both mating types are present in the germinating teliospore but one mating type is unable to grow as free-living sporidia. The complete bias was most readily interpreted as evidence of "haploid lethals" linked to mating type that cause poor survival or growth of the sporidial stage. The results show that such "haploid lethals" may be a common occurrence in natural populations, and that fungal mating systems may vary considerably over short distances

Do Transmission Mechanisms or Social Systems Drive Cultural Dynamics in Socially Structured Populations?

Cultural traits spread via multiple mechanisms among individuals within social groups, including via transmission biases that occur when subordinates copy from dominants (prestige transmission), or via common cultural trait variants that are favoured over rare ones (consensus transmission). Most animal populations are subdivided into social groups where cultural learning occurs, yet theoretical studies of cultural trait transmission have tended to focus on within-group transmission dynamics. We developed an agent-based model of cultural transmission in socially structured populations in which a trait arises in one individual and either persists until a stable population equilibrium is reached, or goes extinct. With this model, we systematically varied group size, rates of dispersal among groups, mortality rates, transmission characteristics, the benefit of the cultural trait (including possibly negative benefits), and whether individuals disperse locally or randomly. We used generalized linear models to examine how changes in these parameters influence trait extinction, equilibrium prevalence and time to equilibrium. Four traits increased the probability of extinction: smaller group size, higher background mortality, lower transmission rate and more costly traits (although costly traits sometimes reached an equilibrium). Local dispersal and biased transmission mechanisms (prestige and consensus) had no significant effects on extinction probability, and similar patterns were found for equilibrium prevalence. We found that a lower dispersal rate and local dispersal slowed the time required for a trait to reach equilibrium, as did smaller groups, lower transmission rates and lower costs. Collectively, these analyses reveal that prestige and consensus transmission have weaker effects than other factors associated with demographic and social conditions.Human Evolutionary Biolog

Genetic analysis reveals long-standing population differentiation and high diversity in the rust pathogen Melampsora lini

A priority for research on infectious disease is to understand how epidemiological and evolutionary processes interact to influence pathogen population dynamics and disease outcomes. However, little is understood about how population adaptation changes across time, how sexual vs. asexual reproduction contribute to the spread of pathogens in wild populations and how diversity measured with neutral and selectively important markers correlates across years. Here, we report results from a long-term study of epidemiological and genetic dynamics within several natural populations of theLinum marginale-Melampsora liniplant-pathogen interaction. Using pathogen isolates collected from three populations of wild flax (L.marginale) spanning 16 annual epidemics, we probe links between pathogen population dynamics, phenotypic variation for infectivity and genomic polymorphism. Pathogen genotyping was performed using 1567 genome-wide SNP loci and sequence data from two infectivity loci (AvrP123,AvrP4). Pathogen isolates were phenotyped for infectivity using a differential set. Patterns of epidemic development were assessed by conducting surveys of infection prevalence in one population (Kiandra) annually. Bayesian clustering analyses revealed host population and ecotype as key predictors of pathogen genetic structure. Despite strong fluctuations in pathogen population size and severe annual bottlenecks, analysis of molecular variance revealed that pathogen population differentiation was relatively stable over time. Annually, varying levels of clonal spread (0-44.8%) contributed to epidemics. However, within populations, temporal genetic composition was dynamic with rapid turnover of pathogen genotypes, despite the dominance of only four infectivity phenotypes across the entire study period. Furthermore, in the presence of strong fluctuations in population size and migration, spatial selection may maintain pathogen populations that, despite being phenotypically stable, are genetically highly dynamic. Author summary Melampsora liniis a rust fungus that infects native flax,Linum marginalein south-eastern Australia where its epidemiology and evolution have been intensively studied since 1987. Over that time, substantial diversity in the pathotypic structure ofM.linihas been demonstrated but an understanding of how genetic diversity in pathogen populations is maintained through space and time is lacking. Here we integrated phenotypic, genotypic and epidemiological datasets spanning 16 annual epidemics across three host populations to examine long-term pathogen genetic dynamics. The results show that host ecotype is the dominant selective force in the face of strong bottlenecks and annual patterns of genetic turnover. Results from previous studies indicate that in this geographic region,M.linilacks the capacity to reproduce sexually-we thus expected to find limited genetic diversity and evidence for strong clonality influencing genetic dynamics within growing seasons. However, the breadth of genomic coverage provided by the SNP markers revealed high levels of genotypic variation withinM.linipopulations. This discovery contrasts with observed phenotypic dynamics as the epidemics of this pathogen were largely dominated by four pathotypes across the study period. Based on a detailed assessment and comparison of pathotypic and genotypic patterns, our study increases the understanding of how genetic diversity is generated and maintained through space and time within wild pathogen populations. The implications for the management of resistance to pathogens in agricultural or conservation contexts are significant: the appearance of clonality may be hiding high levels of pathogen diversity and recombination. Understanding how this diversity is generated could provide new and unique ways to mitigate or suppress the emergence of infectious strains, allowing to efficiently combat harmful diseases.Peer reviewe

Availability of soil mutualists may not limit non‐native Acacia invasion but could increase their impact on native soil communities

The availability of compatible mutualistic soil microbes could influence the invasion success of non-native plant species. Specifically, there may be spatial variation in the distribution of compatible microbes, and species-specific variation in plant host ability to associate with available microbes. Although either or both factors could promote or limit invasion, the scale over which most studies are conducted makes it difficult to examine these two possibilities simultaneously. However, this is critical to identifying a role of soil microbes in invasion. A series of recent research projects focused on interactions between Australian Acacia and nitrogen-fixing bacteria (rhizobia) at multiple spatial scales, from the local to the inter-continental, has allowed us to evaluate this question. Collectively, this research reveals that nodulation, performance and rhizobial community composition are all broadly similar across spatial scales and differentially invasive species. Synthesis and applications. We argue that current research provides convincing evidence that interactions with rhizobia do not determine invasion success in Acacia, but instead highlights key knowledge gaps that remain unfilled. Importantly, the ease with which non-native Acacia species form mutualistic associations with rhizobia, regardless of invasive status, highlights the critical need to understand the impacts of all non-native Acacia on native soil communities

Phylogenetic signals and predictability in plant-soil feedbacks

There is strong evidence for a phylogenetic signal in the degree to which species share co-evolved biotic partners and in the outcomes of biotic interactions. This implies there should be a phylogenetic signal in the outcome of feedbacks between plants and soil microbiota they cultivate. However, attempts to identify a phylogenetic signal in plant-soil feedbacks have produced mixed results. We clarify how phylogenetic signals could arise in plant-soil feedbacks and use a recent compilation of data from feedback experiments to identify: 1) whether there is a phylogenetic signal in the outcome of plant-soil feedbacks; and 2) whether any signal arises through directional or divergent changes in feedback outcomes with evolutionary time. We find strong evidence for a divergent phylogenetic signal in feedback outcomes. Distantly related plant species show more divergent responses to each other's soil microbiota than closely related plant species. The pattern of divergence implies occasional co-evolutionary shifts in how plants interact with soil microbiota, with strongly contrasting feedback responses among some plant lineages. Our results highlight that it is difficult to predict feedback outcomes from phylogeny alone, other than to say that more closely related species tend to have more similar responses

Wildfire impact : natural experiment reveals differential short-term changes in soil microbial communities

A wildfire which overran a sensor network site provided an opportunity (a natural experiment) to monitor short-term post-fire impacts (immediate and up to three months post-fire) in remnant eucalypt woodland and managed pasture plots. The magnitude of fire-induced changes in soil properties and soil microbial communities was determined by comparing (1) variation in fire-adapted eucalypt woodland vs. pasture grassland at the burnt site; (2) variation at the burnt woodland-pasture sites with variation at two unburnt woodland-pasture sites in the same locality; and (3) temporal variation pre- and post-fire. In the eucalypt woodland, soil ammonium, pH and ROC content increased post-fire, while in the pasture soil, soil nitrate increased post-fire and became the dominant soluble N pool. However, apart from distinct changes in N pools, the magnitude of change in most soil properties was small when compared to the unburnt sites. At the burnt site, bacterial and fungal community structure showed significant temporal shifts between pre- and post-fire periods which were associated with changes in soil nutrients, especially N pools. In contrast, microbial communities at the unburnt sites showed little temporal change over the same period. Bacterial community composition at the burnt site also changed dramatically post-fire in terms of abundance and diversity, with positive impacts on abundance of phyla such as Actinobacteria, Proteobacteria and Firmicutes. Large and rapid changes in soil bacterial community composition occurred in the fire-adapted woodland plot compared to the pasture soil, which may be a reflection of differences in vegetation composition and fuel loading. Given the rapid yet differential response in contrasting land uses, identification of key soil bacterial groups may be useful in assessing recovery of fire-adapted ecosystems, especially as wildfire frequency is predicted to increase with global climate change

Symbiosis limits establishment of legumes outside their native range at a global scale

Microbial symbiosis is integral to plant growth and reproduction, but its contribution to global patterns of plant distribution is unknown. Legumes (Fabaceae) are a diverse and widely distributed plant family largely dependent on symbiosis with nitrogen-fixing rhizobia, which are acquired from soil after germination. This dependency is predicted to limit establishment in new geographic areas, owing to a disruption of compatible host-symbiont associations. Here we compare non-native establishment patterns of symbiotic and non-symbiotic legumes across over 3,500 species, covering multiple independent gains and losses of rhizobial symbiosis. We find that symbiotic legume species have spread to fewer non-native regions compared to non-symbiotic legumes, providing strong support for the hypothesis that lack of suitable symbionts or environmental conditions required for effective nitrogen-fixation are driving these global introduction patterns. These results highlight the importance of mutualisms in predicting non-native species establishment and the potential impacts of microbial biogeography on global plant distribution