Emergence of novel fungal pathogens by ecological speciation: importance of the reduced viability of immigrants

Expanding global trade and the domestication of ecosystems have greatly accelerated the rate of emerging infectious fungal diseases, and host-shift speciation appears to be a major route for disease emergence. There is therefore an increased interest in identifying the factors that drive the evolution of reproductive isolation between populations adapting to different hosts. Here, we used genetic markers and cross-inoculations to assess the level of gene flow and investigate barriers responsible for reproductive isolation between two sympatric populations of Venturia inaequalis, the fungal pathogen causing apple scab disease, one of the fungal populations causing a recent emerging disease on resistant varieties. Our results showed the maintenance over several years of strong and stable differentiation between the two populations in the same orchards, suggesting ongoing ecological divergence following a host shift. We identified strong selection against immigrants (i.e. host specificity) from different host varieties as the strongest and likely most efficient barrier to gene flow between local and emerging populations. Cross-variety disease transmission events were indeed rare in the field and cross-inoculation tests confirmed high host specificity. Because the fungus mates within its host after successful infection and because pathogenicity-related loci prevent infection of nonhost trees, adaptation to specific hosts may alone maintain both genetic differentiation between and adaptive allelic combinations within sympatric populations parasitizing different apple varieties, thus acting as a ‘magic trait’. Additional intrinsic and extrinsic postzygotic barriers might complete reproductive isolation and explain why the rare migrants and F1 hybrids detected do not lead to pervasive gene flow across years

Magic traits drive the emergence of pathogens

An important branch of evolutionary biology strives to understand how divergent selection for an ecologically important trait can foster the emergence of new species specialized on different niches. Such ecological speciation is usually difficult to achieve because recombination between different subsets of a population that are adapting to different environments counteracts selection for locally adapted gene combinations. Traits pleiotropically controlling adaptation to different environments and reproductive isolation are therefore the most favourable for ecological speciation, and are thus called “magic traits”. We used genetic markers and cross-inoculations to show that pathogenicity-related loci are responsible for both host adaptation and reproductive isolation in emerging populations of Venturia inaequalis, the fungus causing apple scab disease. Because the fungus mates within its host and because the pathogenicity-related loci prevent infection of the non-host trees, host adaptation pleiotropically maintains genetic differentiation and adaptive allelic combinations between sympatric populations specific to different apple varieties. Such “magic traits” are likely frequent in fungal pathogens, and likely drive the emergence of new diseases.

Neurospora from natural populations: Population genomics insights into the Life history of a model microbial Eukaryote

The ascomycete filamentous fungus Neurospora crassa played a historic role in experimental biology and became a model system for genetic research. Stimulated by a systematic effort to collect wild strains initiated by Stanford geneticist David Perkins, the genus Neurospora has also become a basic model for the study of evolutionary processes, speciation, and population biology. In this chapter, we will first trace the history that brought Neurospora into the era of population genomics. We will then cover the major contributions of population genomic investigations using Neurospora to our understanding of microbial biogeography and speciation, and review recent work using population genomics and genome-wide association mapping that illustrates the unique potential of Neurospora as a model for identifying the genetic basis of (potentially adaptive) phenotypes in filamentous fungi. The advent of population genomics has contributed to firmly establish Neurospora as a complete model system and we hope our review will entice biologists to include Neurospora in their research

Host-specific differentiation among populations of Venturia inaequalis causing scab on apple, pyracantha and loquat

Patterns of multilocus DNA sequence variation within and between closely related taxa can provide insights into the history of divergence. Here, we report on DNA polymorphism and divergence at six nuclear loci in globally distributed samples of the ascomycete Venturia inaequalis, responsible for scab on apple, loquat, and pyracantha. Isolates from different hosts were differentiated but did not form diagnosable distinct phylogenetic species. Parameters of an Isolation-with-Migration model estimated from the data suggested that the large amount of variation shared among groups more likely resulted from recent splitting than from extensive genetic exchanges. Inferred levels of gene flow among groups were low and more concentrated toward recent times, and we identified two potentially recent one-off shifters from apple and pyracantha to loquat. These findings support a scenario of recent divergence in allopatry followed by introgression through secondary contact, with groups from loquat and pyracantha being the most recently differentiated

Glacial Refugia in Pathogens: European Genetic Structure of Anther Smut Pathogens on Silene latifolia and Silene dioica

Climate warming is predicted to increase the frequency of invasions by pathogens and to cause the large-scale redistribution of native host species, with dramatic consequences on the health of domesticated and wild populations of plants and animals. The study of historic range shifts in response to climate change, such as during interglacial cycles, can help in the prediction of the routes and dynamics of infectious diseases during the impending ecosystem changes. Here we studied the population structure in Europe of two Microbotryum species causing anther smut disease on the plants Silene latifolia and Silene dioica. Clustering analyses revealed the existence of genetically distinct groups for the pathogen on S. latifolia, providing a clear-cut example of European phylogeography reflecting recolonization from southern refugia after glaciation. The pathogen genetic structure was congruent with the genetic structure of its host species S. latifolia, suggesting dependence of the migration pathway of the anther smut fungus on its host. The fungus, however, appeared to have persisted in more numerous and smaller refugia than its host and to have experienced fewer events of large-scale dispersal. The anther smut pathogen on S. dioica also showed a strong phylogeographic structure that might be related to more northern glacial refugia. Differences in host ecology probably played a role in these differences in the pathogen population structure. Very high selfing rates were inferred in both fungal species, explaining the low levels of admixture between the genetic clusters. The systems studied here indicate that migration patterns caused by climate change can be expected to include pathogen invasions that follow the redistribution of their host species at continental scales, but also that the recolonization by pathogens is not simply a mirror of their hosts, even for obligate biotrophs, and that the ecology of hosts and pathogen mating systems likely affects recolonization patterns

Genetic signatures of variation in population size in a native fungal pathogen after the recent intensive plantation of its host tree

Historical fluctuations in forests’ distribution driven by past climate changes and anthropogenic activities can have large impacts on the demographic history of pathogens that have a long co-evolution history with these host trees. Using a population genetic approach, we investigated that hypothesis by reconstructing the demographic history of Armillaria ostoyae, one of the major pathogens of the maritime pine (Pinus pinaster), in the largest monospecific pine planted forest in Europe (south-western France). Genetic structure analyses and approximate Bayesian computation approaches revealed that a single pathogen population underwent a severe reduction in effective size (12 times lower) 1080–2080 generations ago, followed by an expansion (4 times higher) during the last 4 generations. These results are consistent with the history of the maritime pine forest in the region characterized by a strong recession during the last glaciation (~19 000 years ago) and massive plantations during the second half of the nineteenth century. Results suggest that recent and intensive plantations of a host tree population have offered the opportunity for a rapid spread and adaptation of their pathogens

Nuclear and Chloroplast Microsatellites Show Multiple Introductions in the Worldwide Invasion History of Common Ragweed, Ambrosia artemisiifolia

BACKGROUND: Ambrosia artemisiifolia is a North American native that has become one of the most problematic invasive plants in Europe and Asia. We studied its worldwide population genetic structure, using both nuclear and chloroplast microsatellite markers and an unprecedented large population sampling. Our goals were (i) to identify the sources of the invasive populations; (ii) to assess whether all invasive populations were founded by multiple introductions, as previously found in France; (iii) to examine how the introductions have affected the amount and structure of genetic variation in Europe; (iv) to document how the colonization of Europe proceeded; (v) to check whether populations exhibit significant heterozygote deficiencies, as previously observed. PRINCIPAL FINDINGS: We found evidence for multiple introductions of A. artemisiifolia, within regions but also within populations in most parts of its invasive range, leading to high levels of diversity. In Europe, introductions probably stem from two different regions of the native area: populations established in Central Europe appear to have originated from eastern North America, and Eastern European populations from more western North America. This may result from differential commercial exchanges between these geographic regions. Our results indicate that the expansion in Europe mostly occurred through long-distance dispersal, explaining the absence of isolation by distance and the weak influence of geography on the genetic structure in this area in contrast to the native range. Last, we detected significant heterozygote deficiencies in most populations. This may be explained by partial selfing, biparental inbreeding and/or a Wahlund effect and further investigation is warranted. CONCLUSIONS: This insight into the sources and pathways of common ragweed expansion may help to better understand its invasion success and provides baseline data for future studies on the evolutionary processes involved during range expansion in novel environments