Search

Theoretical models suggest that infectious diseases could play a substantial role in determining the spatial extent of host species, but few studies have collected the empirical data required to test this hypothesis. Pathogens that sterilize their hosts or spread through frequency-dependent transmission could have especially strong effects on the limits of species' distributions because diseased hosts that are sterilized but not killed may continue to produce infectious stages and frequency-dependent transmission mechanisms are effective even at very low population densities. We collected spatial pathogen prevalence data and population abundance data for alpine carnations infected by the sterilizing pathogen M. violaceum, a parasite that is spread through both frequency-dependent (vector-borne) and density-dependent (aerial spore transmission) mechanisms. Our 13-year study reveals rapid declines in population abundance without a compensatory decrease in pathogen prevalence. We apply a stochastic, spatial model of parasite spread that accommodates spatial habitat heterogeneity to investigate how the population dynamics depend on multimodal (frequency-dependent and density-dependent) transmission. We found that the observed rate of population decline could plausibly be explained by multimodal transmission, but is unlikely to be explained by either frequency-dependent or density-dependent mechanisms alone. Multimodal pathogen transmission rates high enough to explain the observed decline predicted that eventual local extinction of the host species is highly likely. Our results add to a growing body of literature showing how multimodal transmission can constrain species distributions in nature.

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.

This article examines the relationship between John Leigh (1812–1888) and Lydia Becker (1827–1890). Leigh was a prominent figure in the scientific circles of Manchester in the mid-nineteenth century and the city's Medical Officer for Health. Becker was a botanist and Leigh's second cousin. She corresponded with Charles Darwin and became a pioneer in the women's suffrage movement. Previous studies have argued that Leigh patronized and discouraged Becker's botanical interests. However, newly-discovered correspondence shows that Leigh respected her abilities and encouraged her development as a botanist, including attendance at the British Association for the Advancement of Science meetings where she presented one of the first scientific papers by a female botanist in Britain. While social and institutional norms in the Victorian era discouraged women from entering science, these norms could be transgressed in interactions involving specific individuals.

Theoretical models suggest that infectious diseases could play a substantial role in determining species’ ranges, but few studies have collected the empirical data required to test this hypothesis. Pathogens that sterilize their hosts or spread through frequency-dependent transmission could have especially strong effects on the limits of species’ distributions because sterilized hosts can serve as long-lived disease reservoirs and frequency-dependent transmission mechanisms are effective even at very low population densities. We collected spatial disease prevalence data and population abundance data for alpine carnations infected by the sterilizing pathogen M. violaceum, a disease that is spread through both frequency-dependent (vector-borne) and density-dependent (aerial spore transmission) mechanisms. Our 13-year study reveals rapid declines in population abundance without a compensatory decrease in disease prevalence. We apply a stochastic, spatial model of disease spread that accommodates spatial habitat heterogeneity to investigate how the population dynamics depend on multimodal (frequency-dependent and density-dependent) transmission. We found that the observed rate of population decline can be readily explained by multimodal transmission, but is unlikely to be explained by either frequency-dependent or density-dependent mechanisms alone. Multimodal disease transmission rates high enough to explain the observed decline predicted that eventual local extinction of the host species is highly likely. Our results add to a growing body of literature showing how multimodal transmission can constrain species distributions in nature.Open ResearchAll scripts associated with the analyses in this manuscript, as well as the data we collected, are available at https://github.com/uricchio/antherSmutDis.

A recent study by Sugiura and coworkers reported the non-symbiotic growth and spore production of an arbuscular mycorrhizal (AM) fungus, Rhizophagus irregularis, when the fungus received an external supply of certain fatty acids, myristates (C:14). This discovery follows the insight that AM fungi receive fatty acids from their hosts when in symbiosis. If this result holds up and can be repeated under nonsterile conditions and with a broader range of fungi, it has numerous consequences for our understanding of AM fungal ecology, from the level of the fungus, at the plant community level, and to functional consequences in ecosystems. In addition, myristate may open up several avenues from a more applied perspective, including improved fungal culture and supplementation of AM fungi or inoculum in the field. We here map these potential opportunities, and additionally offer thoughts on potential risks of this potentially new technology. Lastly, we discuss the specific research challenges that need to be overcome to come to an understanding of the potential role of myristate in AM ecology.

1. Species interactions and diversity are strongly impacted by local processes, with both the density of a focal species and its frequency in the community having an impact on its growth, survival and fecundity. Yet, studies that attempt to control for variation in both frequency and density have traditionally required a large number of replicates. 2. Hexagonal fan designs can include a range of both densities and frequencies in a single plot, providing large economies in space and material for studying local interactions such as competition and disease transmission. However, in practice such experiments can be difficult to plan and implement. 3. This study presents an R program whereby the user can rapidly view a variety of designs and determine the configurations that work best with their space and material constraints. Simple instructions for implementing the fan in any design setting are also provided. 4. We illustrate the implementation of a simple form of the hexagonal fan design in a field experiment to assess the impact of host density on pollinator movement and disease transmission.

Juveniles are typically less resistant (more susceptible) to infectious disease than adults, and this difference in susceptibility can help fuel the spread of pathogens in age-structured populations. However, evolutionary explanations for this variation in resistance across age remain to be tested.One hypothesis is that natural selection has optimized resistance to peak at ages where disease exposure is greatest. A central assumption of this hypothesis is that hosts have the capacity to evolve resistance independently at different ages. This would mean that host populations have (a) standing genetic variation in resistance at both juvenile and adult stages, and (b) that this variation is not strongly correlated between age classes so that selection acting at one age does not produce a correlated response at the other age.Here we evaluated the capacity of three wild plant species (

Significance Energy limitation is a widespread phenomenon that governs microbial processes ranging from the metabolism of individual cells to the functioning of the biosphere. By tracking the population dynamics of diverse bacterial taxa under prolonged starvation, we identified common strategies that sustain life. Although bacteria have the capacity to reproduce on timescales of minutes to hours, we predict that populations can persist for hundreds to thousands of years, placing upper bounds on microbial lifespans. While the dynamics observed in our long-term experiment were driven by a reduction in death rates, cryptic birth events generated mutations that fueled evolution. Our findings shed light on cellular longevity with implications for biodiversity in extreme environments that dominate vast expanses of Earth., Microorganisms commonly inhabit energy-limited ecosystems where cellular maintenance and reproduction is highly constrained. To gain insight into how individuals persist under such conditions, we derived demographic parameters from a collection of 21 heterotrophic bacterial taxa by censusing 100 populations in an effectively closed system for 1,000 d. All but one taxon survived prolonged resource scarcity, yielding estimated times to extinction ranging over four orders of magnitude from 100 to 105 y. Our findings corroborate reports of long-lived bacteria recovered from ancient environmental samples, while providing insight into mechanisms of persistence. As death rates declined over time, lifespan was extended through the scavenging of dead cells. Although reproduction was suppressed in the absence of exogenous resources, populations continued to evolve. Hundreds of mutations were acquired, contributing to genome-wide signatures of purifying selection as well as molecular signals of adaptation. Consistent ecological and evolutionary dynamics indicate that distantly related bacteria respond to energy limitation in a similar and predictable manner, which likely contributes to the stability and robustness of microbial life.

Summary We report a four-year study of the dynamics of a population of Salvia lyrata L., growing in a greenhouse. The study exemplifies the population cage approach, which has been the basis of many long-term studies of dynamics of animal populations for over 50 years, but which has been overlooked by plant population biologists. The cohort of plants that founded the population had a very high probability of survival and, as adults, produced the greatest numbers of seeds and seedlings. Thereafter, the numbers of individuals in each stage class declined. This decline appeared to be a consequence of density-dependent processes. At the conclusion of the study, the population density was far lower than at the onset. The behaviour of the population differed from that of the population of S. lyrata studied in a nearby mown field in several respects, including timing of seedling emergence, average size of individuals and final density. Likely causes of these differences are discussed. We recommend the use of population cages in further studies of plant populations. Because it facilitates long-term observation, this approach can be of great use in elucidating the dynamic consequences of demography.

Behavioural resistance to parasites is widespread in animals, yet little is known about the evolutionary dynamics that have shaped these strategies. We show that theory developed for the evolution of physiological parasite resistance can only be applied to behavioural resistance under limited circumstances. We find that accounting explicitly for the behavioural processes, including the detectability of infected individuals, leads to novel dynamics that are strongly dependent on the nature of the costs and benefits of social interactions. As with physiological resistance, evolutionary dynamics of behavioural resistance can also lead to mixed strategies that balance these costs and benefits.

Behavioral resistance to parasites is widespread in animals, yet little is known about the evolutionary dynamics that have shaped these strategies. We show that theory developed for the evolution of physiological parasite resistance can only be applied to behavioral resistance under limited circumstances. We find that accounting explicitly for the behavioral processes, including the detectability of infected individuals, leads to novel dynamics that are strongly dependent on the nature of the costs and benefits of social interactions. As with physiological resistance, the evolutionary dynamics can also lead to mixed strategies that balance the costs of disease risk and the benefits of social interaction, with implications for understanding avoidance strategies in human disease outbreaks.

This paper examines the rise and fall of Carl Linnaeus's ideas on living contagion, focusing on his work with plant smut diseases. Early in his career, Linnaeus named a plant altered by anther-smut disease as a separate species, but then, probably realizing it was a diseased specimen, demoted it to a variety. He later drew direct parallels between minute insects attacking plants and infectious diseases in humans, but did not yet draw an analogy to smut diseases. After Otto von Münchhausen had sent Linnaeus the first instalment of his book Der Hausvater (1764) , Linnaeus realized smuts were contagious. He carried out his own investigations that appeared to confirm Münchhausen's conclusion that smut spores germinated to produce living and mobile animalcules. This cemented Linnaeus's view that animalcules caused contagion in human diseases, a view which he expressed forcefully, urging further studies. However, his results were questioned and discounted by others, especially John Ellis. An analysis of correspondence between Linnaeus and other microscopists shows that it is likely Linnaeus did actually see “animalcules” emerging from cereal grains. He was unaware that smut-like symptoms in wheat could also be caused by seed-gall nematodes in the genus Anguina. Linnaeus himself came to doubt the connection between fungi and contagion, and did not pursue these studies further. The presumption that Linnaeus was fanciful in his observations of animalcules may partly explain why his views had only a tangential impact on the germ-theory of disease, and why his insights remain unappreciated to this day.

Premise of the study Plant pathogens that form persistent systemic infections within plants have the potential to affect multiple plant life history traits, yet we tend to focus only on visible symptoms. Anther smut of Silene latifolia caused by the fungus Microbotryum lychnidis-dioicae induces the anthers of its host to support fungal spore production instead of pollen, and the pathogen is primarily transmitted among flowering plants by pollinators. Nevertheless, most of its life cycle is spent in the asymptomatic vegetative phase, and spores falling on seedlings or nonflowering plants can also infect the host. The purpose of this study was to ask whether the fungus also had an effect on its host plant in the juvenile vegetative phase before flowering as this is important for the disease dynamics in species where infection of seedlings is commonplace. Methods Leaf length and leaf number of inoculated and uninoculated juvenile plants were compared in greenhouse experiments, and in one experiment, disease status of the plants at flowering was determined. Key results Inoculated plants had shorter but more leaves, and reduced root mass at the early juvenile (preflowering) stage. Some of these effects were detectable in plants that were inoculated but showed no disease symptoms at flowering. Conclusions These results show that pathogenic fungi can have endophyte-like effects even in the total absence of their typical and more charismatic symptoms, and conversely that the assessment of endophyte effects on the fitness of their hosts should include all stages of the host life cycle.

Summary Theory has shown that sterilizing diseases with frequency-dependent transmission (characteristics shared by many sexually transmitted diseases) can drive host populations to extinction. Anther-smut disease (caused by Microbotryum sp.) has become a model plant pathogen system for studying the dynamics of vector- and sexually transmitted diseases: infected individuals are sterilized, producing spores instead of pollen, and the disease is spread between reproductive individuals by insect pollinators. We investigated anther-smut disease in a heavily infected population of Dianthus pavonius (alpine carnation) over an 8-year period to determine disease impacts on host population dynamics. Over the 8 years, disease prevalence remained consistently high (>40%), while the host population numbers declined by over 50%. The observed rate of vector transmission to reproductive, adult hosts was inadequate to explain the high disease prevalence. Additional density-dependent aerial transmission to highly susceptible juveniles, indicated from experimental field and greenhouse studies, is likely to play a key role in maintaining the high disease prevalence. Epidemiological models that accounted for the mixed transmission mode predicted an eventual decline in disease. Synthesis. Our results demonstrate that high prevalence of a sterilizing disease does not necessarily drive host populations towards extinction and also highlights the importance of demographic studies for establishing the presence of alternative transmission modes.

Vector-borne diseases threaten human and agricultural health and are a critical component of the ecology of plants and animals. While previous studies have shown that pathogen spread can be affected by vector preferences for host infection status, less attention has been paid to vector preference for host sex, despite abundant evidence of sex-specific variation in disease burden. We investigated vector preference for host infection status and sex in the sterilizing "anther-smut" pathogen (Microbotryum) of the alpine carnation, Dianthus pavonius. The pathogen is transferred among hosts by pollinators that visit infected flowers and become contaminated with spores produced by infected anthers. The host plant has a mixed breeding system with hermaphrodites and females. In experimental floral arrays, pollinators strongly preferred healthy hermaphrodites over both females and diseased plants, consistently across different guilds of pollinators and over multiple years. Using an agent-based model, we showed that pollinator preferences for sex can affect pathogen spread in populations with variable sex ratios, even if there is no preference for infection status. Our results demonstrate that vector preferences for host traits other than infection status can play a critical role in pathogen transmission dynamics when there is heterogeneity for those traits in the host population.

The impact of infectious diseases in natural ecosystems is strongly influenced by the degree of pathogen specialization and by the local assemblies of potential host species. This study investigated anther‐smut disease, caused by fungi in the genus Microbotryum, among natural populations of plants in the Caryophyllaceae. A broad geographic survey focused on sites of the disease on multiple host species in sympatry. Analysis of molecular identities for the pathogens revealed that sympatric disease was most often due to co‐occurrence of distinct, host‐specific anther‐smut fungi, rather than localized cross‐species disease transmission. Flowers from sympatric populations showed that the Microbotryum spores were frequently moved between host species. Experimental inoculations to simulate cross‐species exposure to the pathogens in these plant communities showed that the anther‐smut pathogen was less able to cause disease on its regular host when following exposure of the plants to incompatible pathogens from another host species. These results indicate that multi‐host/multi‐pathogen communities are common in this system and they involve a previously hidden mechanism of interference between Microbotryum fungi, which likely affects both pathogen and host distributions.

Awareness that our planet is a self-supporting biosphere with sunlight as its major source of energy for life has resulted in a long-term historical fascination with the workings of self-supporting ecological systems. However, the studies of such systems have never entered the canon of ecological or evolutionary tools and instead, have led a fringe existence connected to life support system engineering and space travel. We here introduce a framework for a renaissance in biospherics based on the study of matter-closed, energy-open ecosystems at a microbial level (microbial biospherics). Recent progress in genomics, robotics, and sensor technology makes the study of closed systems now much more tractable than in the past, and we argue that the time has come to emancipate the study of closed systems from this fringe context and bring them into a mainstream approach for studying ecosystem processes. By permitting highly replicated long-term studies, especially on predetermined and simplified systems, microbial biospheres offer the opportunity to test and develop strong hypotheses about ecosystem function and the ecological and evolutionary determinants of long-term system failure or persistence. Unlike many sciences, ecosystem ecology has never fully embraced a reductionist approach and has remained focused on the natural world in all its complexity. We argue that a reductionist approach to ecosystem ecology, using microbial biospheres, based on a combination of theory and the replicated study of much simpler self-enclosed microsystems could pay huge dividends.

International audience; The impact of infectious diseases in natural ecosystems is strongly influenced by the degree of pathogen specialization and by the local assemblies of potential host species. This study investigated anther-smut disease, caused by fungi in the genus Microbotryum, among natural populations of plants in the Caryophyllaceae. A broad geographic survey focused on sites of the disease on multiple host species in sympatry. Analysis of molecular identities for the pathogens revealed that sympatric disease was most often due to co-occurrence of distinct, host-specific anther-smut fungi, rather than localized cross-species disease transmission. Flowers from sympatric populations showed that the Microbotryum spores were frequently moved between host species. Experimental inoculations to simulate cross-species exposure to the pathogens in these plant communities showed that the anther-smut pathogen was less able to cause disease on its regular host when following exposure of the plants to incompatible pathogens from another host species. These results indicate that multi-host/multi-pathogen communities are common in this system and they involve a previously hidden mechanism of interference between Microbotryum fungi, which likely affects both pathogen and host distributions.

The evolution of resistance to antibiotics in disease causing pathogens is a major world-wide threat to human health. This paper explores why regulatory, funding and institutional structures have inadequately addressed this issue, focusing on data from the US, but emphasizing that these issues are of global scope and applicability. There is an increasing call for serious acceptance of evolutionary biology by the medical community, but the failure to apply evolutionary ideas to the problem of antibiotic resistance continues. These ideas are deceptively simple in their basic formulation, but require sophisticated expertise when it comes to applying them in practice and to human health. The divergent histories of evolutionary biology and medical research have self-referential constituencies in each field. The field of evolutionary biology does not see the applied issues associated with antibiotic resistance as part of its remit. At the biomedical research level, funding for research on evolution of antibiotic resistance is paltry compared to its importance as a health threat, regulatory requirements do not address evolutionary issues, institutional structures dealing with the issue are undeveloped, and there is even avoidance of the word ‘evolution’ in the context of antibiotic resistance. Current approaches to antibiotic resistance invoke evolutionary principles at a such a naive level that what is put forward are ineffective seat-of-the-pants rules that have no strong theoretical basis and are almost always in desperate need of justification through evidence-based research. Clear solutions exist but their implementation remains problematic.

This study used existing databases to test the hypothesis that fern species harbor fewer pathogen species than angiosperm species. Analysis was limited to fungal pathogens because of their visibility and to herbaceous perennial dicots (forbs) because they have a similar growth form to ferns. From complete listings in the United States Department of Agriculture plant-fungal database, the number of pathogen species recorded on 200 randomly chosen ferns and herbaceous perennial dicot species were assessed. To control for differences in study effort, the number of citations to these species in the Web of Science was determined. The results showed that the major predictor of the number of fungal pathogen species known to occur on a plant species was study effort, but after controlling for this, the likelihood of a fern species being recorded as having a fungal pathogen species was much less than that for a forb. When pathogens were present, there were approximately 50% fewer pathogen species recorded on fern species than on forb species. This pattern is present even though fern species were cited on average more often than forb species, and it is consistent with impressions in the literature from studies in other parts of the world. Testable hypotheses to explain this difference are evaluated in the context of evolutionary processes leading to variation for pathogen incidence in different phylogenetic lineages, but the physiological or molecular processes that determine the higher resistance of ferns to fungal pathogens remain unknown.

In flowering plants, the evolution of females is widely hypothesized to be the first step in the evolutionary pathway to separate male and female sexes, or dioecy. Natural enemies have the potential to drive this evolution if they preferentially attack hermaphrodites over females. We studied sex-based differences in exposure to anther-smut (Microbotryum), a sterilizing pollinator-transmitted disease, in Dianthus pavonius, a gynodioecious perennial herb. We found that within a heavily diseased population, females consistently had lower levels of Microbotryum spore deposition relative to hermaphrodites and that this difference was driven by rapid floral closing in females following successful pollination. We further show that this protective closing behavior is frequency-dependent; females close faster when they are rare. These results indicate that anther-smut disease is an important source of selection for females, especially since we found in a common garden experiment no evidence that females have any inherent fecundity advantages over hermaphrodites. Finally, we show that among populations, those where anther-smut is present have a significantly higher frequency of females than those where the disease is absent. Taken together our results indicate that anther-smut disease is likely an important biotic factor driving the evolution and maintenance of females in this gynodioecious species.

BGPI : équipe 5; International audience; The competitive exclusion principle postulates that different species can only coexist in sympatry if they occupy distinct ecological niches. The goal of this study was to understand the geographical distribution of three species of Microbotryum anther-smut fungi that are distantly related but infect the same host plants, the sister species Silene vulgaris and S. uniflora, in Western Europe. We used microsatellite markers to investigate pathogen distribution in relation to host specialization and ecological factors. Microbotryum violaceo-irregulare was only found on S. vulgaris at high elevations in the Alps. Microbotryum lagerheimii could be subdivided into two genetically differentiated clusters, one on S. uniflora in the UK and the second on S. vulgaris in the Alps and Pyrenees. The most abundant pathogen species, M. sile-nes-inflatae, could be subdivided into four genetic clusters, co-occurring in the Alps, the UK and the Pyrenees, and was found on both S. vulgaris and S. uniflora. All three fungal species had high levels of homozygosity, in agreement with the selfing mating system generally observed in anther-smut fungi. The three pathogen species and genetic clusters had large range overlaps, but occurred at sites with different elevations , temperatures and precipitation levels. The three Microbotryum species thus do not appear to be maintained by host specialization or geographic allopatry, but instead may occupy different ecological niches in terms of environmental conditions.

Microbial communities are enigmatically diverse. We propose a novel view of processes likely affecting microbial assemblages, which could be viewed as the Great American Interchange en miniature: the wholesale exchange among microbial communities resulting from moving pieces of the environment containing entire assemblages. Incidental evidence for such 'community coalescence' is accumulating, but such processes are rarely studied, likely because of the absence of suitable terminology or a conceptual framework. We provide the nucleus for such a conceptual foundation for the study of community coalescence, examining factors shaping these events, links to bodies of ecological theory, and we suggest modeling approaches for understanding coalescent communities. We argue for the systematic study of community coalescence because of important functional and applied consequences.

Many mutualisms involve reciprocal exploitation, such that each species in a mutualism is a consumer of a resource provided by the other. Frequently, such mutualisms are reformed each generation, and where they involve close physiological contact, such as between mycorrhizal fungi and plants, they can be considered as examples of reciprocal parasitism. Here we place such interactions in the framework of the Prisoner's Dilemma, and examine the conditions for the spread of mutualism using a population genetics model analogous to that used for understanding the genetic and numerical dynamics of host-parasite interactions. Genetic variants within each of two species determine whether the interaction is mutualistic or selfish, the latter being represented by resistance to being exploited or parasitized. We assume that there are fitness costs to resistance which are present even in the absence of the interaction. Just as in host-parasite interactions, we examine the effect of assuming that encounter rates between potential mutualists (and therefore entry into the Prisoner's Dilemma 'game') depend on the density and frequency of the different types interacting individuals. These elements of ecological realism greatly facilitate the evolution of mutualism even in the absence of spatial structure or iterative encounters. Moreover, stable genetic polymorphisms for resistant (selfish) and susceptible (mutualistic) alleles can be maintained, something that is not possible with the classical Prisoner's Dilemma formulation. The sensitivity of the outcomes to levels of density-dependence and mortality rate suggests environmental as well as genetic processes are likely to be important in determining directions in this pathway to mutualism.

Fungal ecology lags behind in the use of traits (i.e. phenotypic characteristics) to understand ecological phenomena. We argue that this is a missed opportunity and that the selection and systematic collection of trait data throughout the fungal kingdom will reap major benefits in ecological and evolutionary understanding of fungi. To develop our argument, we first employ plant trait examples to show the power of trait-based approaches in understanding ecological phenomena such as identifying species allocation resources patterns, inferring community assembly and understanding diversityeecosystem functioning relationships. Second, we discuss ecologically relevant traits in fungi that could be used to answer such ecological phenomena and can be measured on a large proportion of the fungal kingdom. Third, we identify major challenges and opportunities for widespread, coordinated collection and sharing of fungal trait data. The view that we propose has the potential to allow mycologists to contribute considerably more influential studies in the area of fungal ecology and evolution, as has been demonstrated by comparable earlier efforts by plant ecologists. This represents a change of paradigm, from community profiling efforts through massive sequencing tools, to a more mechanistic understanding of fungal ecology.

Recent theoretical work has shown that long-lived hosts are expected to evolve higher equilibrium levels of disease resistance than shorter-lived hosts, but questions of how longevity affects the rate of resistance evolution and the maintenance of polymorphism remain unanswered. Conventional wisdom suggests that adaptive evolution should occur more slowly in long-lived organisms than in short-lived organisms. However, the opposite may be true for the evolution of disease-resistance traits where exposure to disease, and therefore the strength of selection for resistance increases with longevity. In a single locus model of innate resistance to a frequency-dependent, sterilizing disease, longer lived hosts evolved resistance more rapidly than short-lived hosts. Moreover, resistance in long-lived hosts could only be polymorphic for more costly and more extreme resistance levels than short-lived hosts. The increased rate of evolution occurred in spite of longer generation times because longer-lived hosts had both a longer period of exposure to disease as well as higher disease prevalence. Qualitatively similar results were found when the model was extended to mortality-inducing diseases, or to density-dependent transmission modes. Our study shows that the evolutionary dynamics of host resistance is determined by more than just levels of resistance and cost, but is highly sensitive to the life-history traits of the host.

Many important and rapidly emerging pathogens of humans, livestock and wildlife are ‘vector-borne’. However, the term ‘vector’ has been applied to diverse agents in a broad range of epidemiological systems. In this perspective, we briefly review some common definitions, identify the strengths and weaknesses of each and consider the functional differences between vectors and other hosts from a range of ecological, evolutionary and public health perspectives. We then consider how the use of designations can afford insights into our understanding of epidemiological and evolutionary processes that are not otherwise apparent. We conclude that from a medical and veterinary perspective, a combination of the ‘haematophagous arthropod’ and ‘mobility’ definitions is most useful because it offers important insights into contact structure and control and emphasizes the opportunities for pathogen shifts among taxonomically similar species with similar feeding modes and internal environments. From a population dynamics and evolutionary perspective, we suggest that a combination of the ‘micropredator’ and ‘sequential’ definition is most appropriate because it captures the key aspects of transmission biology and fitness consequences for the pathogen and vector itself. However, we explicitly recognize that the value of a definition always depends on the research question under study.This article is part of the themed issue ‘Opening the black box: re-examining the ecology and evolution of parasite transmission’.

Classification schemes have been popular to tame the diversity of root-infecting fungi. However, the usefulness of these schemes is limited to descriptive purposes. We propose that a shift to a multidimensional trait-based approach to disentangle the saprotrophic–symbiotic continuum will provide a better framework to understand fungal evolutionary ecology. Trait information reflecting the separation of root-infecting fungi from free-living soil relatives will help to understand the evolutionary process of symbiosis, the role that species interactions play in maintaining their large diversity in soil and in planta , and their contributions at the ecosystem level. Methodological advances in several areas such as microscopy, plant immunology, and metatranscriptomics represent emerging opportunities to populate trait databases.

Understanding the factors determining the distribution of parasites and pathogens in natural systems is essential for making predictions about the spread of emerging infectious disease. Here, we report the distribution of the fungal anther-smut disease, caused by Microbotryum spp., on populations of the European wildflower Silene vulgaris over a range of elevations. A survey of several geographically distinct mountains in the southern French alps found that anther-smut disease was restricted to high elevations, rarely observed below 1300 m despite availability of hosts below this elevation. Anther smut causes host-sterility, and is recognized as a model system for natural host–pathogen interactions, sharing common features with vector-borne and sexually-transmitted disease in animals. In such systems, many biotic and abiotic factors likely to change over ecological gradients can influence disease epidemiology, including host spatial structure, pathogen infectivity, host resistance, and vector behavior. Here, we tested whether host population size, density, or connectivity also declined across elevation, and whether these epidemiologically relevant factors explained the observed disease distribution. We found that while none of these factor means changed across elevation, disease was significantly more likely to occur at both higher elevations and in larger populations, the majority of which were found above 1300 m. The break in disease incidence was also associated with an apparent scarcity of these larger host populations between 1000 and 1300 m in elevation. Examining variation in climatic factors among host populations, we also showed that the probability of disease was higher in areas with historically colder, wetter, and more stable conditions. The restricted distribution of anther-smut disease in high-elevation S. vulgaris provides an opportunity for empirical study on range limits and disease distribution in natural alpine communities that are considered particularly sensitive to the effects of climate change.

This study presents the first translation from Latin to English of the Linnaean dissertationMundus invisibilisorThe Invisible World, submitted by Johannes Roos in 1769. The dissertation highlights Linnaeus's conviction that infectious diseases could be transmitted by living organisms, too small to be seen. Biographies of Linnaeus often fail to mention that Linnaeus was correct in ascribing the cause of diseases such as measles, smallpox and syphilis to living organisms. The dissertation itself reviews the work of many microscopists, especially on zoophytes and insects, marvelling at the many unexpected discoveries. It then discusses and quotes at length the observations of Münchhausen suggesting that spores from fungi causing plant diseases germinate to produce animalcules, an observation that Linnaeus claimed to have confirmed. The dissertation then draws parallels between these findings and the contagiousness of many human diseases, and urges further studies of this ‘invisible world’ since, as Roos avers, microscopic organisms may cause more destruction than occurs in all wars.

This article reviews research on the evolutionary mechanisms leading to different transmission modes. Such modes are often under genetic control of the host or the pathogen, and often in conflict with each other via trade-offs. Transmission modes may vary among pathogen strains and among host populations. Evolutionary changes in transmission mode have been inferred through experimental and phylogenetic studies, including changes in transmission associated with host shifts and with evolution of the unusually complex life cycles of many parasites. Understanding the forces that determine the evolution of particular transmission modes presents a fascinating medley of problems for which there is a lack of good data and often a lack of conceptual understanding or appropriate methodologies. Our best information comes from studies that have been focused on the vertical versus horizontal transmission dichotomy. With other kinds of transitions, theoretical approaches combining epidemiology and population genetics are providing guidelines for determining when and how rapidly new transmission modes may evolve, but these are still in need of empirical investigation and application to particular cases. Obtaining such knowledge is a matter of urgency in relation to extant disease threats. This article is part of the themed issue ‘Opening the black box: re-examining the ecology and evolution of parasite transmission’.

The genus Silene, studied by Darwin, Mendel and other early scientists, is re-emerging as a system for studying interrelated questions in ecology, evolution and developmental biology. These questions include sex chromosome evolution, epigenetic control of sex expression, genomic conflict and speciation. Its well-studied interactions with the pathogen Microbotryum has made Silene a model for the evolution and dynamics of disease in natural systems, and its interactions with herbivores have increased our understanding of multi-trophic ecological processes and the evolution of invasiveness. Molecular tools are now providing new approaches to many of these classical yet unresolved problems, and new progress is being made through combining phylogenetic, genomic and molecular evolutionary studies with ecological and phenotypic data. Heredity (2009) 103, 5-14; doi: 10.1038/hdy.2009.34; published online 15 April 2009

Community coalescence is a recently introduced term describing the interaction of entire communities and their environments. We here explicitly place the concept of community coalescence in a soil microbial context, exploring intrinsic and extrinsic drivers of such coalescence events. Examples of intrinsic events include the action of earthworms and the dynamics of soil aggregates, while extrinsic events are exemplified by tillage, flooding, litter-fall, outplanting, and the addition of materials containing microbial communities. Aspects of global change may alter the frequency or severity of coalescence events. We highlight functional consequences of community coalescence in soil, and suggest ways to experimentally tackle this phenomenon. Soil ecology as a whole stands to benefit from conceptualizing soil biodiversity in terms of dynamic coalescent microbial assemblages.

The occurrence of multiple pathogen species on a shared host species is unexpected when they exploit the same micro-niche within the host. One explanation for such observations is the evolution of pathogen-specific resistances that segregate the host population into sites that are differentially occupiable by the competing pathogens. This study used experimental inoculations to test whether specific resistances may contribute to the maintenance of two anther-smut fungi, Microbotryum silenes-inflatae and Microbotryum lagerheimii, in natural populations of Silene uniflora in England and Wales. Overall, resistance to the two pathogens was strongly positively correlated among host populations and to a lesser degree among host families within populations. A few instances of specific resistance were also observed and confirmed by replicated inoculations. The potential for specific resistances to maintain both M. lagerheimii and M. silenes-inflatae on S. uniflora appears unlikely. However, there are important implications of the observed general resistance in that selection by an endemic pathogen may protect the host from the emergence via host shifts of related pathogens and interspecific competition between pathogens for susceptible hosts is expected to be intensified.

There is growing evidence that successful infection of hosts by pathogens requires a series of independent steps. However, how multistep infection processes affect host-pathogen coevolution is unclear. We present a coevolutionary model, inspired by empirical observations from a range of host-pathogen systems, where the infection process consists of the following two steps: the first is for the pathogen to recognize and locate a suitable host, and the second is to exploit the host while evading immunity. Importantly, these two steps conform to different models of infection genetics: inverse-gene-for-gene (IGFG) and gene-for-gene (GFG), respectively. We show that coevolution under this scenario can lead to coupled gene frequency changes across these two systems. In particular, selection often favors pathogens that are infective at the first, IGFG, step and hosts that are resistant at the second, GFG, step. Hence, there may be signals of positive selection between functionally independent systems whenever there are multistep processes determining resistance and infectivity. Such multistep infection processes are a fundamental, but overlooked feature of many host-pathogen interactions, and have important consequences for our understanding of host-pathogen coevolution.