bioRxiv Science⌕ Search

Biology subjects

Prospero, S.

Publications and source records attributed to Prospero, S..

8 recordsLinked to original sources

Worldwide spread of Hylurgus ligniperda (Coleoptera: Scolytinae), and the potential role of bridgehead invasions

Hylurgus ligniperda (F.) is a highly successful invader among bark beetles (Scolytinae) and forest insects in general. Native to the western Palearctic region, it has become established in every continent where its host plants (Pinus spp.) occur. Especially in southern hemisphere regions with large pine plantations, it is often highly abundant. As a repeat invader with a wealth of information on various aspects relevant for biological invasions, it is highly suitable as a model organism for studying the role of international trade, the planting of non-native trees, and the potential occurrence of bridgehead invasions (where abundant non-native populations precipitate further invasions). In the present study, our specific objectives were to reconstruct the worldwide invasions of H. ligniperda and the pathways involved by using a multi-pronged approach including population genetics, analysis of historic interception data generated from inspections of imports, and records of establishments in the literature. Our review of the native and non-native ranges of H. ligniperda and the chronology of establishments revealed at least 13 separate invasions of non-native regions, beginning with Madeira (Portugal) before 1850, and, most recently, eastern China in 2019. We compared the population genetics of 464 specimens from eight countries in the native range and eight countries in the non-native range. Sequencing of the mitochondrial COI gene revealed the presence of 29 haplotypes in six well-supported clades, based on a Bayesian analysis. Non-native populations had significantly lower haplotype diversity (mean h = 0.219) than populations in the native range (mean h = 0.691). Countries in the non-native range had an average of about two haplotypes compared with about four haplotypes in native countries. In the non-native range, only one or two haplotypes were dominant, and these differed among invaded regions except for haplotype HL-H3 which occurred in Australia, New Zealand and China as well as in four countries in southern Europe, and HL-H4 which was dominant in New Zealand, California, New York State, and eastern China as well as two countries in southern Europe. Analyses of interceptions of H. ligniperda with imports arriving in five countries revealed that between 74% and 99% of interceptions originated from other non-native regions while in the USA, most interceptions were linked to imports from the native range beginning in the 1970s. Based on the combined evidence of the chronology of invasions, interception data, and analysis of haplotype distribution, we conclude that the early invasions (before 1950) probably all originated from the native range, while several of the more recent invasions probably originated from parts of the non-native range (suggestive of a bridgehead effect). However, it cannot be determined with certainty what the original sources of each of the invading populations were.

ecology↗

Million years old recombination suppression and balancing selection in a region linked to the mating-type locus in the invasive chestnut blight fungal pathogen Cryphonectria parasitica

Recombination suppression can evolve in sex or mating-type chromosomes, or in autosomal supergenes, with different haplotypes being maintained by balancing selection. In the invasive chestnut blight fungus Cryphonectria parasitica, a genomic region was suggested to lack recombination and to be partially linked to the mating-type (MAT) locus based on segregation analyses. Using hundreds of available C. parasitica genomes and generating new high-quality genome assemblies, we show that a ca. 1.2 Mb genomic region proximal to the mating-type locus lacks recombination, with the segregation of two highly differentiated haplotypes in balanced proportions in invasive populations. High-quality genome assemblies further revealed an inversion in one of the haplotypes in the invaded range. The two haplotypes were estimated to have diverged 1.5 million years ago, and each harboured specific genes, some of which likely belonging to Starship elements, that are large mobile elements, mobilized by tyrosine recombinases, able to move accessory genes, and involved in adaptation in multiple fungi. The MAT-proximal region carried genes upregulated under virus infection or vegetative incompatibility reaction. In the native range, the MAT-proximal region also appeared to have a different evolutionary history than the rest of the genome. In all continents, the MAT-Proximal region was enriched in non-synonymous substitutions, in gene presence/absence polymorphism, in tyrosine recombinases and in transposable elements. This study thus sheds light on a case of a large non-recombining region partially linked to a mating compatibility locus, with likely balancing selection maintaining differentiated haplotypes, possibly involved in adaptation in a devastating tree pathogen.

evolutionary biology↗

Climate, host and geography shape insect and fungal communities of trees

Non-native pests, climate change, and their interactions are likely to alter relationships between trees and tree-associated organisms with consequences for forest health. To understand and predict such changes, factors structuring tree-associated communities need to be determined. Here, we analysed the data consisting of records of insects and fungi collected from dormant twigs from 155 tree species at 51 botanical gardens or arboreta in 32 countries. Generalized dissimilarity models revealed similar relative importance of studied climatic, host-related and geographic factors on differences in tree-associated communities. Mean annual temperature, phylogenetic distance between hosts and geographic distance between locations were the major drivers of dissimilarities. The increasing importance of high temperatures on differences in studied communities indicate that climate change could affect tree-associated organisms directly and indirectly through host range shifts. Insect and fungal communities were more similar between closely related vs. distant hosts suggesting that host range shifts may facilitate the emergence of new pests. Moreover, dissimilarities among tree-associated communities increased with geographic distance suggesting that human-mediated transport may facilitate the introductions of new pests. The results of this study highlight the need to limit the establishment of tree pests and increase the resilience of forest ecosystems to changes in climate.

ecology↗

Distribution of the invasive Anisandrus maiche (Coleoptera: Scolytinae) in Switzerland, first record in Europe of its ambrosia fungus Ambrosiella cleistominuta, and its new association with Xylosandrus crassiusculus

In 2022, two independent insect surveys in canton Ticino (southern Switzerland) revealed the widespread occurrence of the invasive ambrosia beetle Anisandrus maiche from southern to central-upper Ticino. This species is native to east Asia and has previously been found as a non-native invasive species in the United States, Canada, western Russia, Ukraine and, in 2021, in northern Italy. Here, we present the results of several trapping studies using different trap types (bottle traps, funnel traps and Polytrap intercept traps) and attractants and a map of the distribution of the species. In total, 685 specimens of A. maiche, all female, were trapped, and the identity of selected individuals was confirmed by morphological and molecular identification based on three mitochondrial and nuclear markers (COI, 28S and CAD). Traps checked from early April to early September 2022 in intervals of two to four weeks showed that flights of A. maiche occurred mainly from June to mid-August. Isolation of fungal associates of A. maiche from beetles trapped alive revealed the presence of four fungal species, including the ambrosia fungus Ambrosiella cleistominuta, the known mutualists of A. maiche. The identity of A. cleistominuta was confirmed by comparing DNA sequences of its nuclear, internal transcribed spacer (ITS) gene with reference sequences in NCBI and BOLDSYSTEMS. This represents the first record of A. cleistominuta in Europe. Ambrosiella cleistominuta was also found in association with another non-native invasive ambrosia beetle, Xylosandrus crassiusculus, at a botanic garden in central Ticino. As ambrosia beetles usually show a high degree of fidelity with only one mutualistic fungus (in the case of X. crassiusculus normally Ambrosiella roeperi), this association is highly unusual and probably the result of lateral transfer among these non-native invasive species. Of the other fungal associates isolated from A. maiche in Ticino, Fusarium lateritium is of note as there is a possibility that A. maiche could act as a vector of this plant pathogen. We highlight several research needs that should be addressed to gain insight into the potential impact of these non-native species and to overcome problems with heteroplasmy in COI sequences in studies of invasion and population genetics of ambrosia beetles.

ecology↗

Possible biological control of ash dieback using the parasitic Hymenoscyphus fraxineus mitovirus 2?

Invasive fungal diseases represent a major threat to forest ecosystems worldwide. As fungicides are often unfeasible and not a sustainable solution, only a few other control options are available, including biological control. In this context, the use of parasitic mycoviruses as biocontrol agents of fungal pathogens has recently gained particular attention. Since the 1990s, the Asian fungus Hymenoscyphus fraxineus has been causing lethal ash dieback across Europe. In the present study, we investigated the biocontrol potential of the mitovirus Hymenoscyphus fraxineus mitovirus 2 (HfMV2) previously identified in Japanese populations of the pathogen. HfMV2 could be successfully introduced via co-culturing into 16 out of 105 virus-free isolates. A virus infection had contrasting effects on fungal growth in vitro, from cryptic to detrimental or beneficial. Virus-infected H. fraxineus isolates whose growth was reduced by HfMV2 showed a lower virulence on ash (Fraxinus excelsior) saplings compared to their isogenic virus-free isolates. The results suggest that mycoviruses exist in the native populations of H. fraxineus in Asia that have the potential for biological control of ash dieback in Europe.

pathology↗

Comparative genomics analyses of lifestyle transitions at the origin of an invasive fungal pathogen in the genus Cryphonectria

Emerging fungal pathogens are a threat to forest and agroecosystems, as well as animal and human health. How pathogens evolve from non-pathogenic ancestors is still poorly understood making the prediction of future outbreaks challenging. Most pathogens have evolved lifestyle adaptations, which were enabled by specific changes in the gene content of the species. Hence, understanding transitions in the functions encoded by genomes gives valuable insight into the evolution of pathogenicity. Here, we studied lifestyle evolution in the genus Cryphonectria, including the prominent invasive pathogen C. parasitica, the causal agent of chestnut blight on Castanea species. We assembled and compared the genomes of pathogenic and putatively non-pathogenic Cryphonectria species, as well as sister group pathogens in the family Cryphonectriaceae (Diaporthales, Ascomycetes) to investigate the evolution of genome size and gene content. We found a striking loss of genes associated with carbohydrate metabolism (CAZymes) in C. parasitica compared to other Cryphonectriaceae. Despite substantial CAZyme gene loss, experimental data suggests that C. parasitica has retained wood colonization abilities shared with other Cryphonectria species. Putative effectors substantially varied in number, cysteine content and protein length among species. In contrast, secondary metabolite gene clusters show a high degree of conservation within the genus. Overall, our results underpin the recent lifestyle transition of C. parasitica towards a more pathogenic lifestyle. Our findings suggest that a CAZyme loss may have promoted pathogenicity of C. parasitica on chestnuts. Analyzing gene complements underlying key nutrition modes can facilitate the detection of species with the potential to emerge as pathogens.

microbiology↗

Testing the pathogenic potential of Cryphonectria parasitica and related species on three common European Fagaceae

Invasions by non-native pathogens represent a major threat to managed and natural ecosystems worldwide. Although necessary for adopting preventive strategies, the identification of invasive species before they are introduced is particularly difficult. Indeed, most pathogenic species that have become established in the last decades were first described only after they became invasive. To prevent further biological invasions, not only the early identification of potential new invasive plant pathogens is crucial, but also the assessment of their potential host range. In this study, we determined the pathogenicity and the saprotrophic ability of three Cryphonectria species towards three potential hosts in the family Fagaceae. For this, seedlings and dormant stems of European chestnut (Castanea sativa), pedunculate oak (Quercus robur) and European beech (Fagus sylvatica) were inoculated with different genotypes of C. parasitica (Asian species, invasive in Europe), C. naterciae (European species), and C. japonica (Asian species, not present in Europe). Lesion growth was measured and mortality assessed for four months. The highest damage was caused by C. parasitica on European chestnut, while C. japonica and C. naterciae induced significantly smaller lesions on this host species. All three Cryphonectria species did not grow saprophytically on F. sylvatica and Q. robur, but successfully colonized dormant stems of C. sativa. In the context of biological invasions, our study shows that the Asian C. japonica most likely represents a much less severe threat than C. parasitica for the tested European host species. Nonetheless, the ability of C. naterciae and C. japonica to saprotrophically colonize fresh chestnut wood may suggest that they could become established in chestnut forests and eventually infect weakened chestnut trees or other hosts not tested in this study.

pathology↗

Emergence and diversification of a highly invasive chestnut pathogen lineage across south-eastern Europe

Invasive microbial species constitute a major threat to biodiversity, agricultural production and human health. Invasions are often dominated by one or a small number of genotypes, yet the underlying factors driving invasions are poorly understood. The chestnut blight fungus Cryphonectria parasitica first decimated the American chestnut and a recent outbreak threatens European chestnut trees. To unravel the mechanisms underpinning the invasion of south-eastern Europe, we sequenced 188 genomes of predominantly European strains. Genotypes outside of the invasion zone showed high levels of diversity with evidence for frequent and ongoing recombination. The invasive lineage emerged from the highly diverse European genotype pool rather than a secondary introduction from Asia. The expansion across south-eastern Europe was mostly clonal and is dominated by a single mating type suggesting a fitness advantage of asexual reproduction. Our findings show how an intermediary, highly diverse bridgehead population gave rise to an invasive, largely clonally expanding pathogen. Data availabilityAll raw sequencing data is available on the NCBI Short Read Archive (BioProject PRJNA604575)

evolutionary biology↗