Long-distance Spore Dispersal Research Articles

Developing Predictive Models and Early Warning Systems for Invading Pathogens: Wheat Rusts.

Innovations in aerobiological and epidemiological modeling are enabling the development of powerful techniques to infer connectivity networks for transboundary pathogens in ways that were not previously possible. The innovations are supported by improved access to historical and near real-time highly resolved weather data, multi-country disease surveillance data, and enhanced computing power. Using wheat rusts as an exemplar, we introduce a flexible modeling framework to identify characteristic pathways for long-distance spore dispersal within countries and beyond national borders. We show how the models are used for near real-time early warning systems to support smallholder farmers in East Africa and South Asia. Wheat rust pathogens are ideal exemplars because they continue to pose threats to food security, especially in regions of the world where resources for control are limited. The risks are exacerbated by the rapid appearance and spread of new pathogenic strains, prodigious spore production, and long-distance dispersal for transboundary and pandemic spread.

Genetic Characteristics and Metabolic Interactions between Pseudocercospora fijiensis and Banana: Progress toward Controlling Black Sigatoka.

The international importance of banana and severity of black Sigatoka disease have led to extensive investigations into the genetic characteristics and metabolic interactions between the Dothideomycete Pseudocercospora fijiensis and its banana host. P. fijiensis was shown to have a greatly expanded genome compared to other Dothideomycetes, due to the proliferation of retrotransposons. Genome analysis suggests the presence of dispensable chromosomes that may aid in fungal adaptation as well as pathogenicity. Genomic research has led to the characterization of genes and metabolic pathways involved in pathogenicity, including: secondary metabolism genes such as PKS10-2, genes for mitogen-activated protein kinases such as Fus3 and Slt2, and genes for cell wall proteins such as glucosyl phosphatidylinositol (GPI) and glycophospholipid surface (Gas) proteins. Studies conducted on resistance mechanisms in banana have documented the role of jasmonic acid and ethylene pathways. With the development of banana transformation protocols, strategies for engineering resistance include transgenes expressing antimicrobial peptides or hydrolytic enzymes as well as host-induced gene silencing (HIGS) targeting pathogenicity genes. Pseudocercospora fijiensis has been identified as having high evolutionary potential, given its large genome size, ability to reproduce both sexually and asexually, and long-distance spore dispersal. Thus, multiple control measures are needed for the sustainable control of black Sigatoka disease.

Diversity, Dispersal and Mode of Reproduction of Amanita exitialis in Southern China.

Amanita exitialis is a poisonous mushroom and has caused many deaths in southern China. In this study, we collected 118 fruiting bodies of A. exitialis from seven different sites in Guangdong Province in southern China and investigated their genetic relationships using 14 polymorphic molecular markers. These 14 markers grouped the 118 fruiting bodies into 20 multilocus genotypes. Among these 20 genotypes, eight were each found only once while the remaining 12 were each represented by two to 54 fruiting bodies. Interestingly, among the 12 shared genotypes, four were shared between/among local populations that were separated by as far as over 80 km, a result consistent with secondary homothallic reproduction and long-distance spore dispersal. Despite the observed gene flow, significant genetic differentiations were found among the local populations, primarily due to the over-representation of certain genotypes within individual local populations. STRUCTURE analyses revealed that the 118 fruiting bodies belonged to three genetic clusters, consistent with divergence within this species in this geographic region. Interestingly, we found an excess of heterozygous individuals at both the local and the total sample level, suggesting potential inbreeding depression and heterozygous advantage in these populations of A. exitialis. We discuss the implications of our results for understanding the life cycle, dispersal, and evolution of this poisonous mushroom.

First report of stem rust, caused by Puccinia graminis, and crown rust, caused by Puccinia coronata var. avenae f. sp. avenae, on tall fescue (Festuca arundinacea) in Georgia, USA.

Stem rust, caused by Puccinia graminis, and crown rust, caused by P. coronata, are common rust diseases on cool-season grasses (Karakkat et al. 2018), for which long-distance spore dispersal was recorded in northern US (Harder and Haber 1992). During the summers of 2019 and 2020, severe infection of stem rust and crown rust was observed on > 60% of tall fescue (Festuca arundinacea) germplasm plants in a breeding nursery located at the University of Georgia, Griffin GA. Rust-infected leaves first presented uredinia pustules, then black telia towards the end of the season. The uredinia pustules of stem rust and crown rust were brick-red and, yellow and arranged along the host veins, respectively. The urediniospores were one-celled, round to ovoid and measured from 20.75±2.44 μm (crown rust) to 27±3.60 μm long (stem rust). The teliospores were two-celled and measured from 45.75±10.14 μm (stem rust) to 51.60±4.0 μm long (crown rust) (Leonard et al. 2005; Cummins 1971). Urediniospores of both rusts were collected from infected plants in the field in April of 2020 using a Piston vacuum pump (Welch by Gardner Denver Ltd.) and stored at -80 °C in 1.5 ml Eppendorf tubes. Genomic DNA was extracted by grinding the urediniospores in liquid nitrogen using mortar and pestle, followed by the cetyltrimethylammonium bromide method (Doyle and Doyle 1987). The internal transcribed spacer (ITS) region of the ribosomal DNA was amplified using the ITS5-ITS4 primers (White et al. 1990). BLASTn and phylogenetic analyses revealed that the sequence of stem rust (GenBank acc. no. MW430963) and crown rust (GenBank acc. no. MW431324) pathogens had >99% similarity with P. graminis (GenBank acc. no. HQ317538) and P. coronata var. avenae f. sp. avenae (clade V; Liu and Hambleton 2013) (GenBank acc. no. EU014044), respectively. Pathogenicity tests were conducted on the tall fescue cultivar 'Bandit'. For each rust, 12 pots (10 cm × 10 cm) were planted, each containing 13 seeds in a Sungro professional growing mix soil (Sun Gro Horticulture Distribution Inc.). The plant materials were kept in the greenhouse at 20°C/ 25°C (night/day),15-hrs of light, and watered twice a week for 4-weeks. Urediniospores were recovered from -80°C and allowed to acclimate at room temperature for 1 h. For each rust, 20 ml of suspension containing 1×105 urediniospores ml-1 and 5 μl of Tween-twenty (Agdia Inc. Elkhart, IN) were used to inoculate 6 pots; while 6 control pots were sprayed with sterile water. After inoculation, plants were allowed to dry for 1 h and then transferred to a dark chamber at 20°C and 90% of humidity for 12-15 h. At 10-days post inoculation, all inoculated plants developed rust symptoms identical to those observed in the field, whereas control plants had no symptoms. Stem and crown rust pathogens were re-isolated from the artificially inoculated tall fescue plants. Based on form, size, color and numbers of cells forming the spores, a 1947 Festuca elatior specimen from Georgia mentioning Puccinia coronata (Hanlin 1966), held at the Julian H. Miller Mycological Herbarium (Catalog No. GAM00013162), was discarded as an earlier record of P. coronata var. avenae and could have been misdiagnosed. Due to the fragile integrity of the original infected plant sample as well as the incipient infection, DNA identification was unsuccessful. To our knowledge, this is the first morphological, genetic and taxonomic report of P. graminis and P. coronata var. avenae f. sp. avenae on tall fescue in Georgia, USA.

Population Genetics of Species in the Genera Botrychium and Botrypus (Ophioglossaceae)

The population genetics of ferns, which results from initiation of individuals in a new location (often via long-distance dispersal) plus a wide range of mating systems, merit continued study. In the case of species in the subfamily Botrychioideae (specifically the genera Botrychium and Botrypus), previous work using allozyme and isozyme techniques revealed low genetic diversity and weak population genetic structure. This lack of genetic differentiation between populations is in spite of underground fertilization in the genus resulting in high levels of inbreeding and primarily fixed heterozygosity in tetraploids. In the present study, Amplified Fragment-Length Polymorphisms (AFLPs) were used to examine population genetics and structure of three species in the genus Botrychium and one species in the genus Botrypus. Measures of population genetic diversity were generally low, with the highest measures in the relatively common Botrypus virginianus. Across all species, measures of population differentiation were low and most genetic variation was contained within populations. Bayesian analysis of population structure using the program STRUCTURE corroborated these findings, with inferred genetic clusters that generally did not correspond to geographic collecting locations. These results agree with previous studies, with low genetic diversity within and among populations likely due to self-fertilization that limits outcrossing and long-distance spore dispersal that results in genetically similar populations.

Stenogrammitis myosuroides (Polypodiaceae): a new addition to the European flora from southwest Ireland

The occurrence of the fern Stenogrammitis myosuroides (Sw.) Labiak in Europe is reported for the first time. A small population was discovered on two boulders beside a stream in Atlantic oak woodland in the Killarney National Park, Co. Kerry, in southwest Ireland. The main identification features of this taxa and features that distinguish it from other similar taxa are laid out and discussed. S. myosuroides is elsewhere known to occur in the Neotropics, in Cuba, Jamaica and the Dominican Republic, and is thought to have colonised its Irish site through long-distance spore dispersal. Two Grammitid species of similar ecology have been discovered in the Azores in the past five decades and a number of bryophyte species share a similar disjunct distribution between Ireland and the Neotropics, all of which supports the theory that long-distance dispersal is the most plausible explanation for the occurrence of S. myosuroides in Ireland. It is not clear how long S. myosuroides has been present in Ireland, although morphological differences suggest that it may have been separated from the Neotropical populations for a long period. However, molecular analysis is required to elucidate this.

Detection of Diplodia corticola spores in Ontario and Québec based on High Throughput Sequencing (HTS) methods

A total of 252 aerial spore samples from the provinces of Quebec and Ontario were obtained during an extensive research programme focusing on aerobiology of fungal spores. Samples were collected on 95 sticky rods from rotary arm spore collectors and 157 filters from passive rain collectors. DNA from samples was PCR-amplified for fungal ribosomal ITS and sequenced using High Throughput Sequencing (HTS) methods. After bioinformatics analysis of DNA sequences, the presence of Diplodia corticola, an emerging tree pathogen in North America, was observed. In total, 313 DNA sequence reads from aerial spores of D. corticola were found in the Illumina data set, and 199 DNA sequence reads were obtained from the Ion Torrent data set. DNA of D. corticola was found in 16 of the 32 sampled sites, always less than 10 reads per site, with the exception of three sites – Quebec City, Aylmer and Ottawa – where 287, 125 and 73 DNA reads, respectively, were detected. This is not a first report of the presence of D. corticola causing a tree disease in Canada as symptomatic trees have not been identified. Typically, like many other species of the Botryosphaeriaceae, this fungal pathogen is believed to be an opportunistic plant endophyte capable of living asymptomatically for several years before showing up as a pathogen when conducive conditions arise. Its presence as singletons in nearly half the sampled sites in Quebec and Ontario may be the result of long-distance spore dispersal originating from known infected sites in Massachusetts, Maine and other unknown sites in the north-eastern USA. However, its much higher read counts in three sites may indicate the possibility of a few trees being asymptomatically infected and spreading conidia locally.

On the Origin of the Genus Psilocybe and Its Potential Ritual Use in Ancient Africa and Europe1

On the Origin of the Genus Psilocybe and Its Potential Ritual Use in Ancient Africa and Europe. The role of altered states of consciousness in the production of geometric and figurative art by prehistoric cultures in Africa and Europe has been hotly debated. Helvenston and Bahn have tried to refute the most famous hypothesis, Lewis-Williams’ neuropsychological model, by claiming that appropriate visual hallucinations required the ingestion of LSD, psilocybin, or mescaline, while arguing that none of these compounds were available to the cultures in question. We present here mycological arguments that tell another story. A prehistoric worldwide distribution of the mushroom genus Psilocybe, and therefore of psilocybin, is supported by the existence of endemic species in America, Africa, and Europe, the disjunct distribution of sister species, and the possibility of long-distance spore dispersal. It is more difficult to point to instances of actual prehistoric ritual use in Africa and Europe, but there are a growing number of suggestive findings.

Genet dynamics and ecological functions of the pioneer ectomycorrhizal fungi Laccaria amethystina and Laccaria laccata in a volcanic desert on Mount Fuji

To understand the reproduction of the pioneer ectomycorrhizal fungi Laccaria amethystina and Laccaria laccata in a volcanic desert on Mount Fuji, Japan, the in situ genet dynamics of sporocarps were analysed. Sporocarps of the two Laccaria species were sampled at fine and large scales for 3 and 2 consecutive years, respectively, and were genotyped using microsatellite markers. In the fine-scale analysis, we found many small genets, the majority of which appeared and disappeared annually. The high densities and annual renewal of Laccaria genets indicate frequent turnover by sexual reproduction via spores. In the large-scale analysis, we found positive spatial autocorrelations in the shortest distance class. An allele-clustering analysis also showed that several alleles were distributed in only a small, localised region. These results indicate that Laccaria spores contributing to sexual reproduction may be dispersed only short distances from sporocarps that would have themselves been established via rare, long-distance spore dispersal. This combination of rare, long-distance and frequent, short-distance Laccaria spore dispersal is reflected in the establishment pattern of seeds of their host, Salix reinii.

Meiospores produced in sori of nonsporophyllous laminae of Macrocystis pyrifera (Laminariales, Phaeophyceae) may enhance reproductive output.

Different lamina of Macrocystis pyrifera sporophytes (i.e., sporophylls, pneumatocyst-bearing blades, and apical scimitars) in a wave-sheltered site were found to be fertile. We quantified their sorus surface area, reproductive output (number of spores released) and the viability of released spores (germination rate). Sorus area was greatest on the sporophylls, with sporangia developing on >57% of the total area and smallest on the pneumatocyst-bearing blades with 21% of the total area bearing sporangia. The apical scimitar released the greatest number of meiospores (cells·mL(-1) ·cm(-2) ) and the sporophylls the least. Meiospores produced from all types of fertile laminae were equally viable. This reproductive plasticity may enhance reproductive output, and contribute to short and long-distance spore dispersal and the cryptic gametophyte propagule bank for the next generation of sporophytes.

Ploidy level, genetic diversity, and differentiation in two closely related mosses, Scorpidium cossonii and S. revolvens (Calliergonaceae)

As ploidy level and mating system can affect genetic diversity and differentiation, we conducted population genetic analyses of two closely related mosses, Scorpidium cossonii (Schimp.) Hedenäs, and S. revolvens (Sw. ex Anonymo) Rubers which differ in ploidy level and sexual system. We collected 315 specimens in total from five populations of S. cossonii and four populations of S. revolvens in the Swiss Alps. Ploidy level, genetic diversity within populations, and genetic differentiation between populations and species were estimated using nine microsatellite markers. In each S. cossonii sample, each locus bore only one allele, while in S. revolvens, seven out of the nine loci were fixed or nearly fixed for two alleles per locus per individual. These findings are consistent with a gametophytic haploid S. cossonii and allodiploid S. revolvens. The haploid and dioicous S. cossonii was genetically more diverse than the (allo)diploid and monoicous S. revolvens. Differences in genetic diversity between the two species may be explained by different mating systems, different population sizes, and different population histories. Genetic differentiation among populations of S. cossonii was higher than among those of S. revolvens. The low genetic differentiation among populations of the monoicous species was not unexpected, since monoicous species frequently produce sporophytes, long-distance spore dispersal is more likely and leads to low differentiation.

Spatial genetic structure of aquatic bryophytes in a connected lake system

Using genetic markers, we investigated the genetic structure of three clonal aquatic moss species, Calliergon megalophyllum Mikut., Fontinalis antipyretica Hedw. and F.hypnoides Hartm. on two scales: among populations in a connected lake system (large-scale spatial genetic structure) and among individuals within populations (fine-scale spatial genetic structure). Mean genetic diversities per population were 0.138, 0.247 and 0.271, respectively, and total diversities equalled 0.223, 0.385 and 0.421, respectively. Relative differentiation levels (FST values of 0.173, 0.280 and 0.142, respectively) were significant but showed that there is a moderate amount of gene flow taking place within the lake system connected with narrow streams. Bayesian STRUCTURE analysis provided some indication that the direction of water flow influences population genetic structuring in the studied aquatic mosses. We propose that dispersal leading to gene flow in C.megalophyllum, F.antipyretica and F.hypnoides takes place both along water via connecting streams and by animal vectors, such as waterfowl. Nevertheless, the slight genetic structuring pattern along the direction of water flow suggests that dispersal of shoots or their fragments along water is a means of dispersal in these mosses. The absence of sexual reproduction and spores may have caused the observed spatial genetic structure within populations, including aggregations of similar genotypes (clones or closely related genotypes) at short distances in populations otherwise showing an isolation by distance effect. Regardless of the results pointing to the dominance of vegetative propagation, it is impossible to completely rule out the potential role of rare long-distance spore dispersal from areas where the species are fertile.

Spatially mixed crops to control the stratified dispersal of airborne fungal diseases

Intraspecific crop diversification is thought to be a possible solution to the disease susceptibility of monocultured crops. We modelled the stratified dispersal of an airborne pathogen population in order to identify the spatial patterns of cultivar mixtures that could slow epidemic spread driven by dual dispersal mechanisms acting over both short and long distances. We developed a model to simulate the propagation of a fungal disease in a 2D field, including a reaction-diffusion model for short-distance disease dispersal, and a stochastic model for long-distance dispersal. The model was fitted to data for the spatio-temporal spread of faba bean rust (caused by Uromyces viciae- fabae) through a discontinuous field. The model was used to compare the effectiveness of eight different planting patterns of cultivar mixtures against a disease spread by short-distance and stratified dispersal. Our combined modelling approach provides a reasonably good fit with the observed data for the spread of faba bean rust. Similar predictive power could be expected for the management of resource-mediated invasions by other airborne fungi. If a disease spreads by short-distance dispersal, random mixtures can be used to slow the epidemic spread, since their spatial irregularity creates a natural barrier to the progression of a smooth epidemic wave. In the context of stratified dispersal, heterogeneous patterns should be used that include a minimum distance between susceptible units, which decreases the probability of infection by long-distance spore dispersal. We provide a simple framework for modelling the stratified dispersal of disease in a diversified crop. The model suggests that the spatial arrangement of components in cultivar mixtures has to accord with the dispersal characteristics of the pathogen in order to increase the efficiency of diversification strategies in agro-ecosystems and forestry. It can be applied in low input agriculture to manage pathogen invasion by intercropping and cultivar mixtures, and to design sustainable systems of land use.

Genetic population structure of the ectomycorrhizal fungus Pisolithus microcarpus suggests high gene flow in south-eastern Australia

Pisolithus are ectomycorrhizal fungi that associate with roots of numerous plant species in natural and plantation forests worldwide. Despite the fact that Pisolithus spp. are present in plantation forests in many countries, knowledge of the genetic population structure of Pisolithus spp. remains limited. In this study, we have tested the hypothesis that a propensity for long-distance spore dispersal in Pisolithus microcarpus, along with the widespread distribution of potential eucalypt and acacia plant hosts in south-eastern Australia facilitates gene flow that limits population differentiation. Five polymorphic simple sequence repeat markers were used to investigate the population structure of P. microcarpus. Isolates were grouped according to geographical origin and isolate genotypes were analysed among the geographical populations. Pairwise F (ST) estimates indicated limited genetic differentiation among the geographical populations. Analysis of molecular variance revealed that most of the genetic variation present was within geographical populations, with only 1.3% of the genetic variation among P. microcarpus geographical populations. This was particularly pronounced for four geographical populations within a ca 7,000 km(2) area New South Wales, which were each separated by < 100 km and appeared to be genetically homogeneous. The lack of population structure is suggested to be due to a high degree of gene flow, via basidiospores, between the New South Wales geographical populations.

Assessment of the genetic variation among &lt;i&gt;Suillus granulatus&lt;/i&gt; populations in Israel

Assessing genetic variation within populations, and genetic exchange between geographically separated populations, requires an understanding of the quantitative distribution of individual genotypes within the population. Studies of genetic variability isolates of Suillus granulatus by using randomly amplified polymorphic DNA (RAPD) markers revealed two groups of isolates in Israel. The differentiation of populations within groups (GST) was 0.732 for ISG-I and 0.495 for ISG-II. Conspicuous genetic differentiation between the two S. granulatus groups indicates that there was no extensive gene flow. The spread of alleles within or between populations might be by repeats of short-distance spore dispersal rather than by long-distance spore dispersal.

Monitoring longdistance spore dispersal by wind a review

Collection of meaningful data on long distance dispersal (LDD) of plant pathogens is very difficult because such events are very rare and the strength and locations of pathogen sources are often unknown This review of the different methods that have been deployed examines combinations of meteorological analyses and ground surveys including spore trapping devices collecting rainwater and identifying spores using realtime PCR The relevance of these techniques is discussed in the context of surveillance and monitoring transTasman dispersal of fungal spores

Patterns of variation of a common fern (Athyrium filix‐femina; Woodsiaceae): population structure along and between altitudinal gradients

Genetic variability of Athyrium filix-femina populations was evaluated with regard to phenotypic, allozyme, and RAPD variation in 20 Swiss populations along five altitudinal gradients at four different elevations in the northern Swiss Alps. Additionally, allozyme and phenotypic variations in one Italian and two Spanish populations were compared with the variation in the Swiss populations. We hypothesized that there will be statistically significant genetic differences among populations of different altitudes and sites. The results showed no substantial correlation between genetic variation and phenotypic variation among Swiss populations. These results imply that outbreeding and effective gene exchange (long-distance spore dispersal) are the keys to population structure in this fern species, and as a consequence, phenotypic plasticity is assumed to be favored. This contrasts with results found in similar studies of herbaceous flowering plants where genetic adaptation to gradients like altitude is common. However, when data from the more distant Italian and Spanish populations of A. filix-femina were included, significant variation was detected.

Preliminary phylogenetic analysis of the fern genus Lomariopsis (Lomariopsidaceae)

A preliminary phylogenetic analysis is presented forLomariopsis based on sequence data from the chloroplast intergenic spacertrnL-trnF. The analysis includes 27 (60%) of the approximately 45 species in the genus. A strict consensus of six most parsimonious trees supports two main clades—theSorbifolia-group and theJapurensis-group—previously proposed based on heteroblastic leaf development. TheSorbifolia-group is entirely neotropical and includes all the Antillean species. The species in this clade had either smooth or crested spores, but the tree was ambiguous whether these spore types define two separate clades. TheJapurensis-group consists of two clades, one primarily neotropical and the other entirely paleotropical. Within the neotropical clade nests a clade of two African species, which have long-spiny spores typical of the neotropical clade and unlike those found in the African-Madagascan clade. The occurrence of these two species in Africa is best explained by longdistance spore dispersal of their ancestral species from the neotropics to Africa. Within the paleotropical clade of theJapurensis-group, a clade of three African species is nested among seven species from Madagascar (all the species from that island). Within the genus as a whole, a derived character—the abortion of the rachis apex and its replacement by the distal lateral pinna assuming a terminal position—was found to have evolved separately in each of the four species with this kind of leaf apex. A scanning electron microcope study of the spores revealed five types, and a transformation series for these different types is proposed. Characters of spore morphology and heteroblastic leaf development agreed with many of the clades in the phylogenetic tree. This study represents the first phylogeny for the genus.

Bryophyte dispersal inferred from colonization of an introduced substratum on Whiteface Mountain, New York

A long-standing debate in bryophyte biogeography concerns the frequency of long-distance spore dispersal. The diversity of bryophytes on mortared rock walls along the Veterans Memorial Highway on Whiteface Mountain, New York, USA, was studied to document the recruitment of species over the 65 years since the highway was constructed. The highway is situated in the Adirondack Mountains, a relatively unpopulated region with a largely acidic flora. The introduction of mortar has increased the bryophyte diversity by 50% above that of native lithic substrata on the mountain. The composition of the native and mortar floras differed greatly, suggesting that the walls were not colonized by locally abundant ruderal species. Many of the species sampled on the walls are typically found only in lower elevation forested sites, distant (∼5 km or more) from the highway, and not on anthropogenic calcium carbonate. These results suggest that a bryophyte community consisting of common and uncommon species assembled from distant sites at the rate of at least one species per year in the last 65 years. These data provide the ecological context for experimental and phylogeographic studies and suggest that some bryophytes may be capable of routine dispersal over distances of at least 5 km.

Genetic structure of a population of the ectomycorrhizal fungus Russula vinosa in subtropical woodlands in southwest China.

The genetic structure of a population of the ectomycorrhizal fungus Russula vinosa was analyzed using random amplified polymorphic DNA markers. Of 121 bands, 114 (94.2%) were polymorphic and there was a high genetic diversity (H=34.98) in this population. Each sporocarp represented a different genet and the genet size was no larger than 1 m. Pairwise sporocarps closer than 10 m had significantly higher genetic similarity. Second-order analysis indicated clumps with a radius of about 20 m in the whole population as well as in three genetic groups, i.e. simple matching similarity coefficients (Sm) 0.5-0.6, 0.6-0.7, and 0.7-0.8, respectively. The high-genetic-similarity group tended to have small clumps with high density, whereas the low-genetic-similarity group tended to have large clumps with low density. The spatial pattern analysis showed that the population mainly spread by short-distance spore dispersal rather than vegetative growth of dicaryophytic mycelia or long-distance spore dispersal.