Host promiscuity in symbiont associations can influence exotic legume establishment and colonization of novel ranges

Aim Invasive Acacia species have negatively impacted natural areas in multiple regions around the globe. Almost 400 Acacia species have been introduced outside their native ranges in Australia; approximately 6% have become invasive, 12% are naturalized, and 82% have no record of naturalization or invasion. This variation in invasiveness provides a comparative framework in which to examine mechanisms that either promote or constrain establishment and colonization of species in novel regions. Here, we experimentally examine the role that the legume–rhizobia symbiosis plays in the differential invasiveness of acacias introduced outside their native Australian ranges. Location Canberra, Australia. Methods We paired 12 Acacia species ranging in invasiveness globally with 12 rhizobial strains ranging in average symbiotic effectiveness. We measured plant growth and nodulation success and abundance to assess whether invasive acacias were more promiscuous hosts, that is had positive growth and nodulation responses to a broader range of rhizobial strains than naturalized and non-invasive species. Results Invasive acacias had a higher growth response across more rhizobial strains (six of 12 strains) than naturalized and non-invasive species, but invasiveness categories differed only moderately with regard to the percentage of plants with nodules and nodulation abundance. Main conclusion With respect to plant growth, invasive acacias appear to be more promiscuous hosts than naturalized and non-invasive Australian Acacia species. Plant growth response to nodulation, however, is likely more important than nodulation alone in the successful invasion of species in novel ranges. Results from this study help elucidate an important mechanism in the invasive capacity of legumes

Differential plant invasiveness is not always driven by host promiscuity with bacterial symbionts

Identification of mechanisms that allow some species to outcompete others is a fundamental goal in ecology and invasive species management. One useful approach is to examine congeners varying in invasiveness in a comparative framework across native and invaded ranges. Acacia species have been widely introduced outside their native range of Australia, and a subset of these species have become invasive in multiple parts of the world. Within specific regions, the invasive status of these species varies. Our study examined whether a key mechanism in the life history of Acacia species, the legume-rhizobia symbiosis, influences acacia invasiveness on a regional scale. To assess the extent to which species varying in invasiveness correspondingly differ with regard to the diversity of rhizobia they associate with, we grew seven Acacia species ranging in invasiveness in California in multiple soils from both their native (Australia) and introduced (California) ranges. In particular, the aim was to determine whether more invasive species formed symbioses with a wider diversity of rhizobial strains (i.e. are more promiscuous hosts). We measured and compared plant performance, including aboveground biomass, survival, and nodulation response, as well as rhizobial community composition and richness. Host promiscuity did not differ among invasiveness categories. Acacia species that varied in invasiveness differed in aboveground biomass for only one soil and did not differ in survival or nodulation within individual soils. In addition, acacias did not differ in rhizobial richness among invasiveness categories. However, nodulation differed between regions and was generally higher in the native than introduced range. Our results suggest that all Acacia species introduced to California are promiscuous hosts and that host promiscuity per se does not explain the observed differences in invasiveness within this region. Our study also highlights the utility of assessing potential mechanisms of invasion in species’ native and introduced ranges

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

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

Population Processes at Multiple Spatial Scales Maintain Diversity and Adaptation in the Linum marginale - Melampsora lini Association

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Mixed infections alter transmission potential in a fungal plant pathogen

Infections by more than one strain of a pathogen predominate under natural conditions. Mixed infections can have significant, though often unpredictable, consequences for overall virulence, pathogen transmission and evolution. However, effects of mixed infection on disease development in plants often remain unclear and the critical factors that determine the outcome of mixed infections remain unknown. The fungus Zymoseptoria tritici forms genetically diverse infections in wheat fields. Here, for a range of pathogen traits, we experimentally decompose the infection process to determine how the outcomes and consequences of mixed infections are mechanistically realized. Different strains of Z. tritici grow in close proximity and compete in the wheat apoplast, resulting in reductions in growth of individual strains and in pathogen reproduction. We observed different outcomes of competition at different stages of the infection. Overall, more virulent strains had higher competitive ability during host colonization, and less virulent strains had higher transmission potential. We showed that within‐host competition can have a major effect on infection dynamics and pathogen population structure in a pathogen and host genotype‐specific manner. Consequently, mixed infections likely have a major effect on the development of septoria tritici blotch epidemics and the evolution of virulence in Z. tritici

Resistance to natural and synthetic gene drive systems

Scientists are rapidly developing synthetic gene drive elements intended for release into natural populations. These are intended to control or eradicate disease vectors and pests, or to spread useful traits through wild populations for disease control or conservation purposes. However, a crucial problem for gene drives is the evolution of resistance against them, preventing their spread. Understanding the mechanisms by which populations might evolve resistance is essential for engineering effective gene drive systems. This review summarizes our current knowledge of drive resistance in both natural and synthetic gene drives. We explore how insights from naturally occurring and synthetic drive systems can be integrated to improve the design of gene drives, better predict the outcome of releases and understand genomic conflict in general

Methods for specifying the target difference in a randomised controlled trial : the Difference ELicitation in TriAls (DELTA) systematic review

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