Publications by authors named "Danny Haelewaters"

38 Publications

gen. & comb. nov., the first yeast-like fungus in Leotiomycetes.

Int J Syst Evol Microbiol 2021 Jul;71(7)

Department of Botany and Plant Pathology, Purdue University, West Lafayette, Indiana 47907, USA.

is a pink yeast-like fungus that is not congeneric with other members of (Basidiomycota, Microbotryomycetes, Sporidiobolales). During our ongoing studies of pink yeasts we determined that was most closely related to (Ascomycota, Leotiomycetes, Thelebolales). A molecular phylogenetic analysis using sequences of the ITS region and the small and large subunit (SSU, LSU) rRNA genes, indicated that four isolates of , including three ex-type isolates, were placed in Thelebolales with maximum support. A new genus is proposed to accommodate , . This is the first pink yeast reported in Leotiomycetes.
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http://dx.doi.org/10.1099/ijsem.0.004862DOI Listing
July 2021

Isolation and Molecular Characterization of the Romaine Lettuce Phylloplane Mycobiome.

J Fungi (Basel) 2021 Apr 7;7(4). Epub 2021 Apr 7.

Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907, USA.

Romaine lettuce () is an important staple of American agriculture. Unlike many vegetables, romaine lettuce is typically consumed raw. Phylloplane microbes occur naturally on plant leaves; consumption of uncooked leaves includes consumption of phylloplane microbes. Despite this fact, the microbes that naturally occur on produce such as romaine lettuce are for the most part uncharacterized. In this study, we conducted culture-based studies of the fungal romaine lettuce phylloplane community from organic and conventionally grown samples. In addition to an enumeration of all such microbes, we define and provide a discussion of the genera that form the "core" romaine lettuce mycobiome, which represent 85.5% of all obtained isolates: , , , , , , , , , and . We highlight the need for additional mycological expertise in that 23% of species in these core genera appear to be new to science and resolve some taxonomic issues we encountered during our work with new combinations for and . Finally, our work lays the ground for future studies that seek to understand the effect these communities may have on preventing or facilitating establishment of exogenous microbes, such as food spoilage microbes and plant or human pathogens.
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http://dx.doi.org/10.3390/jof7040277DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8067711PMC
April 2021

sp. nov., a New Ectomycorrhizal Fungus from Mediterranean Croatia Revealed by Morphology and Multilocus Phylogenetic Analysis.

J Fungi (Basel) 2021 Mar 10;7(3). Epub 2021 Mar 10.

Laboratory for Biological Diversity, Ruđer Bošković Institute, Bijenička cesta 54, HR-10000 Zagreb, Croatia.

A new ectomycorrhizal species was discovered during the first survey of fungal diversity at Brijuni National Park (Croatia), which consists of 14 islands and islets. The National Park is located in the Mediterranean Biogeographical Region, a prominent climate change hot-spot. sp. nov., from sect. (Agaricales, Inocybaceae), is described based on morphology and multilocus phylogenetic data. The holotype collection was found at the edge between grassland and forest with a few planted trees, on Veli Brijun Island, the largest island of the archipelago. It is easily recognized by a conspicuous orange to orange-red-brown membranaceous surface layer located at or just above the basal part of the stipe. Other distinctive features of are the medium brown, radially fibrillose to rimose pileus; pale to medium brown stipe with fugacious cortina; relatively small, amygdaliform to phaseoliform, and smooth basidiospores, measuring ca. 6.5-9 × 4-5.5 µm; thick-walled, utriform, lageniform or fusiform pleurocystidia (lamprocystidia) with crystals and mostly not yellowing in alkaline solutions; cheilocystidia of two types (lamprocystidia and leptocystidia); and the presence of abundant caulocystidia only in the upper 2-3 mm of the stipe. Phylogenetic reconstruction of a concatenated dataset of the internal transcribed spacer region (ITS), the nuclear 28S rRNA gene (nrLSU), and the second largest subunit of RNA polymerase II () resolved and as sister species.
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http://dx.doi.org/10.3390/jof7030199DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8000951PMC
March 2021

Multigene phylogeny and taxonomic revision of Atheliales s.l.: Reinstatement of three families and one new family, Lobuliciaceae fam. nov.

Fungal Biol 2021 03 27;125(3):239-255. Epub 2020 Nov 27.

Department of Organismal Biology, Uppsala University, Norbyvägen 18D, 752 36, Uppsala, Sweden. Electronic address:

Atheliales (Agaricomycetes, Basidiomycota) is an order mostly composed of corticioid fungi, containing roughly 100 described species in 20 genera. Members exhibit remarkable ecological diversity, including saprotrophs, ectomycorrhizal symbionts, facultative parasites of plants or lichens, and symbionts of termites. Ectomycorrhizal members are well known because they often form a major part of boreal and temperate fungal communities. However, Atheliales is generally understudied, and molecular data are scarce. Furthermore, the order is riddled with many taxonomic problems; some genera are non-monophyletic and several species have been shown to be more closely related to other orders. We investigated the phylogenetic position of genera that are currently listed in Atheliales sensu lato by employing an Agaricomycetes-wide dataset with emphasis on Atheliales including the type species of genera therein. A phylogenetic analysis based on 5.8S, LSU, rpb2, and tef1 (excluding third codon) retrieved Atheliales in subclass Agaricomycetidae, as sister to Lepidostromatales. In addition, a number of Atheliales genera were retrieved in other orders with strong support: Byssoporia in Russulales, Digitatispora in Agaricales, Hypochnella in Polyporales, Lyoathelia in Hymenochaetales, and Pteridomyces in Trechisporales. Based on this result, we assembled another dataset focusing on the clade with Atheliales sensu stricto and representatives from Lepidostromatales and Boletales as outgroups, based on ITS (ITS1-5.8S-ITS2), LSU, rpb2, and tef1. The reconstructed phylogeny of Atheliales returned five distinct lineages, which we propose here as families. Lobulicium, a monotypic genus with a distinct morphology of seven-lobed basidiospores, was placed as sister to the rest of Atheliales. A new family is proposed to accommodate this genus, Lobuliciaceae fam. nov. The remaining four lineages can be named following the family-level classification by Jülich (1982), and thus we opted to use the names Atheliaceae, Byssocorticiaceae, Pilodermataceae, and Tylosporaceae, albeit with amended circumscriptions.
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http://dx.doi.org/10.1016/j.funbio.2020.11.007DOI Listing
March 2021

A parasitic coevolution since the Miocene revealed by phase-contrast synchrotron X-ray microtomography and the study of natural history collections.

Sci Rep 2021 Jan 29;11(1):2672. Epub 2021 Jan 29.

European Synchrotron Radiation Facility, Grenoble, France.

The discovery of a new fossil species of the Caribbeo-Mexican genus Proptomaphaginus (Coleoptera, Leiodidae, Cholevinae) from Dominican amber, associated with a new fossil parasitic fungus in the genus Columnomyces (Ascomycota, Laboulbeniales), triggered an investigation of extant species of Proptomaphaginus and revealed the long-enduring parasitic association between these two genera. This effort resulted in the description of the fossil species †Proptomaphaginus alleni sp. nov., and one fossil and two extant species of Columnomyces, selectively associated with species of Proptomaphaginus: †Columnomyces electri sp. nov. associated with the fossil †Proptomaphaginus alleni in Dominican amber, Columnomyces hispaniolensis sp. nov. with the extant Proptomaphaginus hispaniolensis (endemic of Hispaniola), and Columnomyces peckii sp. nov. with the extant Proptomaphaginus puertoricensis (endemic of Puerto Rico). Based on biogeography, our current understanding is that the Caribbean species of Proptomaphaginus and their parasitic species of Columnomyces have coevolved since the Miocene. This is the first occurrence of such a coevolution between a genus of parasitic fungus and a genus of Coleoptera. The phylogenetic relations among Proptomaphaginus species are also addressed based on a parsimony analysis. Fossil specimens were observed by propagation phase-contrast synchrotron X-ray microtomography (PPC-SRμCT) and extant specimens were obtained through the study of preserved dried, pinned insects, attesting for the importance of (i) technological advancement and (ii) natural history collections in the study of microparasitic relationships.
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http://dx.doi.org/10.1038/s41598-020-79481-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7846571PMC
January 2021

On the Fly: Tritrophic Associations of Bats, Bat Flies, and Fungi.

J Fungi (Basel) 2020 Dec 12;6(4). Epub 2020 Dec 12.

Research Group Mycology, Department of Biology, Ghent University, K.L. Ledeganckstraat 35, 9000 Ghent, Belgium.

Parasitism is one of the most diverse and abundant modes of life, and of great ecological and evolutionary importance. Notwithstanding, large groups of parasites remain relatively understudied. One particularly unique form of parasitism is hyperparasitism, where a parasite is parasitized itself. Bats (Chiroptera) may be parasitized by bat flies (Diptera: Hippoboscoidea), obligate blood-sucking parasites, which in turn may be parasitized by hyperparasitic fungi, Laboulbeniales (Ascomycota: Laboulbeniomycetes). In this study, we present the global tritrophic associations among species within these groups and analyze their host specificity patterns. Bats, bat flies, and Laboulbeniales fungi are shown to form complex networks, and sixteen new associations are revealed. Bat flies are highly host-specific compared to Laboulbeniales. We discuss possible future avenues of study with regard to the dispersal of the fungi, abiotic factors influencing the parasite prevalence, and ecomorphology of the bat fly parasites.
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http://dx.doi.org/10.3390/jof6040361DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7770572PMC
December 2020

Animal-associated fungi: Editorial.

Mycologia 2020 Nov-Dec;112(6):1045-1047

Division of Plant and Soil Sciences, West Virginia University , Morgantown, West Virginia 26506.

Of 1882 fungal species described in 2019, only 3.5% were animal-associated. This percentage is representative of the poor understanding we have of this group of fungi, which are ephemeral, sometimes inconspicuous, and difficult to access, while often requiring specialized methods for their study. Following a two-session symposium on animal-associated fungi during the 2019 Annual Meeting of the Mycological Society of America, this special issue presents the work of 61 researchers in 16 countries. Twelve articles cover animal-associated fungi among Ascomycota, Basidiomycota, and Neocallimastigomycota-describing 29 new species, presenting new evolutionary hypotheses, and unearthing new ecological data.
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http://dx.doi.org/10.1080/00275514.2020.1841469DOI Listing
December 2020

Mortality of native and invasive ladybirds co-infected by ectoparasitic and entomopathogenic fungi.

PeerJ 2020 4;8:e10110. Epub 2020 Nov 4.

Agricultural Research Service, Southeastern Fruit and Tree Nut Research Laboratory, United States Department of Agriculture, Byron, GA, United States of America.

is an invasive alien ladybird in North America and Europe. Studies show that multiple natural enemies are using as a new host. However, thus far, no research has been undertaken to study the effects of simultaneous infection by multiple natural enemies on . We hypothesized that high thallus densities of the ectoparasitic fungus on a ladybird weaken the host's defenses, thereby making it more susceptible to infection by other natural enemies. We examined mortality of the North American-native and co-infected with and an entomopathogenic fungus-either or . Laboratory assays revealed that -infected individuals are more susceptible to entomopathogenic fungi, but does not suffer the same effects. This is in line with the enemy release hypothesis, which predicts that invasive alien species in new geographic areas experience reduced regulatory effects from natural enemies compared to native species. Considering our results, we can ask how affects survival when confronted by other pathogens that previously had little impact on .
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http://dx.doi.org/10.7717/peerj.10110DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7648450PMC
November 2020

Laboulbeniomycetes: Intimate Fungal Associates of Arthropods.

Annu Rev Entomol 2021 01 31;66:257-276. Epub 2020 Aug 31.

Farlow Reference Library and Herbarium of Cryptogamic Botany, Harvard University, Cambridge, Massachusetts 02138, USA; email:

Arthropod-fungus interactions involving the Laboulbeniomycetes have been pondered for several hundred years. Early studies of Laboulbeniomycetes faced several uncertainties. Were they parasitic worms, red algal relatives, or fungi? If they were fungi, to which group did they belong? What was the nature of their interactions with their arthropod hosts? The historical misperceptions resulted from the extraordinary morphological features of these oddly constructed ectoparasitic fungi. More recently, molecular phylogenetic studies, in combination with a better understanding of life histories, have clearly placed these fungi among filamentous Ascomycota (subphylum Pezizomycotina). Species discovery and research on the classification of the group continue today as arthropods, and especially insects, are routinely collected and examined for the presence of Laboulbeniomycetes. Newly armed with molecular methods, mycologists are poisedto use Laboulbeniomycetes-insect associations as models for the study of a variety of basic evolutionary and ecological questions involving host-parasite relationships, modes of nutrient intake, population biology, host specificity, biological control, and invasion biology. Collaboration between mycologists and entomologists is essential to successfully advance knowledge of Laboulbeniomycetes and their intimate association with their hosts.
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http://dx.doi.org/10.1146/annurev-ento-013020-013553DOI Listing
January 2021

Checklist of thallus-forming Laboulbeniomycetes from Belgium and the Netherlands, including and spp. nov.

MycoKeys 2020 30;71:23-86. Epub 2020 Jul 30.

Meise Botanic Garden, Meise, Belgium Meise Botanic Garden Meise Belgium.

In this paper we present an updated checklist of thallus-forming Laboulbeniomycetes (Ascomycota, Pezizomycotina), that is, the orders Herpomycetales and Laboulbeniales, from Belgium and the Netherlands. Two species are newly described based on morphology, molecular data (ITS, LSU ribosomal DNA) and ecology (host association). These are on (Coleoptera, Coccinellidae) from both countries and on (Coleoptera, Carabidae) from Belgium. In addition, nine new country records are presented. For Belgium: on (Coleoptera, Carabidae) and on (Coleoptera, Carabidae). For the Netherlands: on (Coleoptera, Dytiscidae), on (Coleoptera, Leiodidae), on (Coleoptera, Carabidae), on and (Coleoptera, Carabidae), on (Coleoptera, Carabidae), on (Coleoptera, Carabidae), and on (Diptera, Ephydridae). Finally, an identification key to 140 species of thallus-forming Laboulbeniomycetes in Belgium and the Netherlands is provided. Based on the combined data, we are able to identify mutual gaps that need to be filled as well as weigh the impact of chosen strategies (fieldwork, museum collections) and techniques in these neighboring countries. The aim of this work is to serve as a reference for studying Laboulbeniomycetes fungi in Europe.
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http://dx.doi.org/10.3897/mycokeys.71.53421DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7410850PMC
July 2020

New species of (Agaricales, Inocybaceae) from Pakistan revealed by morphology and multi-locus phylogenetic reconstruction.

MycoKeys 2020 10;69:1-31. Epub 2020 Jul 10.

Department of Botany, University of the Punjab, Lahore, Pakistan University of the Punjab Lahore Pakistan.

During fungal surveys between 2012 and 2014 in pine-dominated forests of the western Himalayas in Pakistan, several collections of (Agaricales, Inocybaceae) were made. These were documented, based on morphological and molecular data. During this work, three new species came to light, which are here formally described as , and . These species belong in the genus Matheny et al. (2019) = Pseudosperma clade Matheny (2005) = sect. Rimosae s.s. fideLarsson et al. (2009). Macro- and micro-morphological descriptions, illustrations and molecular phylogenetic reconstructions of the studied taxa are provided. The new species are differentiated from their close relatives by basidiospore size and colouration of basidiomata. Molecular phylogenetic relationships are inferred using ITS (ITS1-5.8S-ITS2), nrLSU and mtSSU sequence data. All three newly-described taxa likely share an ectomycorrhizal association with trees in the genus . In addition, five names are recombined in , and . These are , , , and .
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http://dx.doi.org/10.3897/mycokeys.69.33563DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7367896PMC
July 2020

A new species of from Ecuador and Panama revealed by morphology and phylogenetic reconstruction, with a discussion of secondary barcodes in Laboulbeniomycetes taxonomy.

Mycologia 2020 Nov-Dec;112(6):1192-1202. Epub 2020 Jul 27.

Department of Botany and Plant Pathology, Purdue University , West Lafayette, Indiana 47907.

This paper describes and illustrates a new species of Laboulbeniales (Ascomycota, Laboulbeniomycetes) recovered from bat flies (Diptera, Streblidae) in Ecuador and Panama. Bat fly-associated Laboulbeniales are still unexplored in the Neotropics, with only four described species of and one species of known. Morphological characteristics and phylogenetic analyses support placement of the new taxon in and its recognition as an undescribed species. sp. nov. is easily recognized by 2-3 longitudinal rows of undulations at its perithecial venter. Phylogenetic reconstructions of the large subunit (LSU) ribosomal DNA and the translation elongation factor 1α () both resolve and as sister species. We discuss the utility of LSU and as secondary barcodes in Laboulbeniomycetes taxonomy.
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http://dx.doi.org/10.1080/00275514.2020.1781496DOI Listing
July 2020

A multigene phylogeny toward a new phylogenetic classification of .

IMA Fungus 2019 7;10. Epub 2019 Jun 7.

Department of Biostatistics, Yale University, 135 College St, New Haven, CT 06510 USA.

Fungi in the class are ecologically diverse, including mycorrhizas, endophytes of roots and leaves, plant pathogens, aquatic and aero-aquatic hyphomycetes, mammalian pathogens, and saprobes. These fungi are commonly detected in cultures from diseased tissue and from environmental DNA extracts. The identification of specimens from such character-poor samples increasingly relies on DNA sequencing. However, the current classification of is still largely based on morphologically defined taxa, especially at higher taxonomic levels. Consequently, the formal classification is frequently poorly congruent with the relationships suggested by DNA sequencing studies. Previous class-wide phylogenies of have been based on ribosomal DNA markers, with most of the published multi-gene studies being focussed on particular genera or families. In this paper we collate data available from specimens representing both sexual and asexual morphs from across the genetic breadth of the class, with a focus on generic type species, to present a phylogeny based on up to 15 concatenated genes across 279 specimens. Included in the dataset are genes that were extracted from 72 of the genomes available for the class, including 10 new genomes released with this study. To test the statistical support for the deepest branches in the phylogeny, an additional phylogeny based on 3156 genes from 51 selected genomes is also presented. To fill some of the taxonomic gaps in the 15-gene phylogeny, we further present an ITS gene tree, particularly targeting ex-type specimens of generic type species. A small number of novel taxa are proposed: ord. nov., and and fams. nov. The formal taxonomic changes are limited in part because of the ad hoc nature of taxon and specimen selection, based purely on the availability of data. The phylogeny constitutes a framework for enabling future taxonomically targeted studies using deliberate specimen selection. Such studies will ideally include designation of epitypes for the type species of those genera for which DNA is not able to be extracted from the original type specimen, and consideration of morphological characters whenever genetically defined clades are recognized as formal taxa within a classification.
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http://dx.doi.org/10.1186/s43008-019-0002-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7325659PMC
June 2019

Additions to the genus (Boletales, Gomphidiaceae) from Pakistan.

MycoKeys 2020 30;66:23-38. Epub 2020 Mar 30.

Department of Botany, University of the Punjab, Quaid-e-Azam Campus, Lahore, 54590, Pakistan.

With only three published reports, the genus (Boletales, Gomphidiaceae) is poorly studied in Pakistan. During recent sampling events in Khyber Pakhtunkhawa province, Pakistan, several collections of were made, representing undescribed taxa. Based on morphological and molecular data, two new species are described: and . We present a description and illustrations for both taxa. A molecular phylogenetic reconstruction, based on the internal transcribed spacer (ITS1-5.8S-ITS2) barcode region, shows that and are placed in two different subgenera of Chroogomphus (subg. Chroogomphus and subg. Siccigomphus, respectively).
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http://dx.doi.org/10.3897/mycokeys.66.38659DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7136303PMC
March 2020

Laboulbeniomycetes: Evolution, natural history, and Thaxter's final word.

Mycologia 2020 Nov-Dec;112(6):1048-1059. Epub 2020 Mar 17.

Department of Organismic and Evolutionary Biology and Farlow Reference Library and Herbarium of Cryptogamic Botany, Harvard University , Cambridge, Massachusetts 02138.

Historically, thallus-forming Laboulbeniomycetes, including the orders Laboulbeniales and Herpomycetales, were set apart because of their distinctive morphology and ecology. Although some biologists correctly interpreted these arthropod ectoparasites as fungi, even ascomycetes, others thought they were worms, red algae, or members of taxa described especially for them. Speculation on the evolution of the group involving red algae, the morphology-based Floridean Hypothesis, persisted deep into the 20th century, in part because valid alternatives were not presented. Although the distinctive features of Laboulbeniales clearly set them apart from other fungi, the difficulty was in the absence of characters grouping them among the fungi. Thaxter considered the Laboulbeniales to be ascomycetes, but he avoided phylogenetic discussions involved in the Floridean Hypothesis all of his life. Eventually, developmental studies of the life history of species, hyphal perithecial ascomycetes with 2-celled ascospores, revealed characters connecting Laboulbeniales to other ascomycetes. The distinctive morphological features of Laboulbeniales (absence of mycelium, a thallus developed from 2-celled ascospores by cell divisions in several planes, arthropod parasitism) can be best understood by comparison with . The development of a 3-dimensional thallus composed of true parenchyma occurs not only in Laboulbeniales, but also in species. The life history of arthropod ectoparasitism of Laboulbeniales as well as mycoparasitism and phoretic dispersal by arthropods of species can be explained by Tranzschel's Law, originally applied to rust fungi. Molecular analyses including other arthropod-associated fungi have contributed to a better understanding of an enlarged class, Laboulbeniomycetes, which now includes a clade comprising , and . A two-locus phylogenetic tree highlights evolutionary and life history questions with regard to the placement of Herpomycetales as the first diverging lineage of the Laboulbeniomycetes. The sister group for all the Laboulbeniomycetes remains to be discovered.
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http://dx.doi.org/10.1080/00275514.2020.1718442DOI Listing
March 2020

Draft Genome Sequence of the Globally Distributed Cockroach-Infecting Fungus Herpomyces periplanetae Strain D. Haelew. 1187d.

Microbiol Resour Announc 2020 Feb 6;9(6). Epub 2020 Feb 6.

Farlow Reference Library and Herbarium of Cryptogamic Botany, Harvard University, Cambridge, Massachusetts, USA.

is an obligate biotroph of , the American cockroach. Its nearly cosmopolitan distribution is shaped by its globally invasive host and the international pet trade. Here, we report the draft genome sequence of , based on a thallus from collected in Cambridge, Massachusetts.
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http://dx.doi.org/10.1128/MRA.01458-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7005119PMC
February 2020

Fungal Systematics and Evolution: FUSE 5.

Sydowia 2019 Dec 23;71:141-245. Epub 2019 Dec 23.

Agroscope, Competence Division for Plants and Plant Products, Ecotoxicology, Müller-Thurgau-Strasse 29, CH-8820 Wädenswil, Switzerland.

Thirteen new species are formally described: from Pakistan, from India, on from Iran, from China, on species of , , and (Coleoptera, Carabidae) from Nicaragua and Panama, on (Hemiptera, Veliidae) from Brazil, on (Blattodea, Termitidae) from the DR Congo, from Slovenia, from Peru, from China, on from Italy, from , on subsp. from Pakistan. The following new records are reported: on from India; on apple and quince fruits from Iran; from Turkey; and on from Italy; causing tip blight of '' from India; from Madeira, Portugal, new for Macaronesia and Africa; , , and from Russia; on from India; on from Italy; on from Austria; from Turkey; from Wisconsin, USA; and from Turkey. Multi-locus analysis of ITS, LSU, , sequences revealed that , commonly classified within Gnomoniaceae (Diaporthales) or as Sordariomycetes , belongs to Magnaporthaceae (Magnaporthales). Analysis of a six-locus Ascomycota-wide dataset including SSU and LSU sequences of revealed that this species, currently in Ascomycota , belongs to Pyronemataceae (Pezizomycetes, Pezizales).
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http://dx.doi.org/10.12905/0380.sydowia71-2019-0141DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6978154PMC
December 2019

Peramorphosis, an evolutionary developmental mechanism in neotropical bat skull diversity.

Dev Dyn 2019 11 6;248(11):1129-1143. Epub 2019 Aug 6.

Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts.

Background: The neotropical leaf-nosed bats (Chiroptera, Phyllostomidae) are an ecologically diverse group of mammals with distinctive morphological adaptations associated with specialized modes of feeding. The dramatic skull shape changes between related species result from changes in the craniofacial development process, which brings into focus the nature of the underlying evolutionary developmental processes.

Results: In this study, we use three-dimensional geometric morphometrics to describe, quantify, and compare morphological modifications unfolding during evolution and development of phyllostomid bats. We examine how changes in development of the cranium may contribute to the evolution of the bat craniofacial skeleton. Comparisons of ontogenetic trajectories to evolutionary trajectories reveal two separate evolutionary developmental growth processes contributing to modifications in skull morphogenesis: acceleration and hypermorphosis.

Conclusion: These findings are consistent with a role for peramorphosis, a form of heterochrony, in the evolution of bat dietary specialists.
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http://dx.doi.org/10.1002/dvdy.90DOI Listing
November 2019

A case of silent invasion: Citizen science confirms the presence of Harmonia axyridis (Coleoptera, Coccinellidae) in Central America.

PLoS One 2019 18;14(7):e0220082. Epub 2019 Jul 18.

Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, United States of America.

Harmonia axyridis (Coleoptera, Coccinellidae) is a globally invasive ladybird. It has been intentionally introduced in many countries as a biological control agent, whereas it has been unintentionally released in many others. Climatic factors are important in limiting the spread of H. axyridis. For example, very few records are known from tropical or desert regions. Currently, no published reports are known from Central America. Here, we report H. axyridis from Costa Rica, Guatemala, Honduras, Panama, and Puerto Rico. Specimens were either observed by the authors, discovered in dried insect collections, or retrieved from searching through online photographs available from the citizen science project iNaturalist and the photo-sharing website Flickr. These new records and the wide distribution of H. axyridis in Latin America suggest several invasion events, which have gone unnoticed until now. We stress the need for further, large-scale monitoring and show the advantage of citizen science to assess the presence of invasive alien species.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0220082PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6638987PMC
March 2020

Studies of Laboulbeniales on Myrmica ants (IV): host-related diversity and thallus distribution patterns of Rickia wasmannii.

Parasite 2019 20;26:29. Epub 2019 May 20.

Faculty of Science, University of South Bohemia, Branišovská 31, 37005 České Budějovice, Czech Republic.

Fungal species identities are often based on morphological features, but current molecular phylogenetic and other approaches almost always lead to the discovery of multiple species in single morpho-species. According to the morphological species concept, the ant-parasitic fungus Rickia wasmannii (Ascomycota, Laboulbeniales) is a single species with pan-European distribution and a wide host range. Since its description, it has been reported from ten species of Myrmica (Hymenoptera, Formicidae), of which two belong to the rubra-group and the other eight to the phylogenetically distinct scabrinodis-group. We found evidence for R. wasmannii being a single phylogenetic species using sequence data from two loci. Apparently, the original morphological description (dating back to 1899) represents a single phylogenetic species. Furthermore, the biology and host-parasite interactions of R. wasmannii are not likely to be affected by genetic divergence among different populations of the fungus, implying comparability among studies conducted on members of different ant populations. We found no differences in total thallus number on workers between Myrmica species, but we did observe differences in the pattern of thallus distribution over the body. The locus of infection is the frontal side of the head in Myrmica rubra and M. sabuleti whereas in M. scabrinodis the locus of infection differs between worker ants from Hungary (gaster tergites) and the Netherlands (frontal head). Possible explanations for these observations are differences among host species and among populations of the same species in (i) how ant workers come into contact with the fungus, (ii) grooming efficacy, and (iii) cuticle surface characteristics.
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http://dx.doi.org/10.1051/parasite/2019028DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6526729PMC
August 2019

Birth of an order: Comprehensive molecular phylogenetic study excludes Herpomyces (Fungi, Laboulbeniomycetes) from Laboulbeniales.

Mol Phylogenet Evol 2019 04 6;133:286-301. Epub 2019 Jan 6.

Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA.

The class Laboulbeniomycetes comprises biotrophic parasites associated with arthropods and fungi. Two orders are currently recognized, Pyxidiophorales and Laboulbeniales. Herpomyces is an isolated genus of Laboulbeniales, with species that exclusively parasitize cockroaches (Blattodea). Here, we evaluate 39 taxa of Laboulbeniomycetes with a three-locus phylogeny (nrSSU, ITS, nrLSU) and propose a new order in this class. Herpomycetales accommodates a single genus, Herpomyces, with currently 26 species, one of which is described here based on morphological and molecular data. Herpomyces shelfordellae is found on Shelfordella lateralis cockroaches from Hungary, Poland, and the USA. We also build on the six-locus dataset from the Ascomycota Tree of Life paper (Schoch and colleagues, 2009) to confirm that Laboulbeniomycetes and Sordariomycetes are sister classes, and we apply laboulbeniomyceta as a rankless taxon for the now well-resolved node that describes the most recent common ancestor of both classes.
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http://dx.doi.org/10.1016/j.ympev.2019.01.007DOI Listing
April 2019

Studies in the Stypella vermiformis group (Auriculariales, Basidiomycota).

Antonie Van Leeuwenhoek 2019 May 8;112(5):753-764. Epub 2018 Dec 8.

Natural History Museum, University of Oslo, P.O. Box 1172, Blindern, 0318, Oslo, Norway.

Stypella vermiformis is a heterobasidiomycete producing minute gelatinous basidiocarps on rotten wood of conifers in the Northern Hemisphere. In the current literature, Stypella papillata, the genus type of Stypella (described from Brazil), is treated as a taxonomic synonym of S. vermiformis. In the present paper, we revise the type material of S. papillata and a number of specimens addressed to S. vermiformis. As a result, the presumed synonymy of S. papillata and S. vermiformis is rejected and the genus Stypella is restricted to the single species S. papillata. Morphological and molecular phylogenetic studies of specimens from the Northern Hemisphere corresponding to the current concept of S. vermiformis uncovered three species from two newly described genera. S. vermiformis s.str. is distributed in temperate Europe and has small-sized basidia and basidiospores, and it is placed in a new genus, Mycostilla. Another genus, Stypellopsis, is created for two other species, the North American Stypellopsis farlowii, comb. nov., and the North European Stypellopsis hyperborea, sp. nov. Basidia and basidiospores of Stypellopsis spp. are larger than in Mycostilla vermiformis but other morphological characters are very similar. In addition, Spiculogloea minuta (Spiculogloeomycetes, Pucciniomycotina) is reported as new to Norway, parasitising basidiocarps of M. vermiformis and Tulasnella spp.
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http://dx.doi.org/10.1007/s10482-018-01209-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6456474PMC
May 2019

Integrative taxonomy reveals hidden species within a common fungal parasite of ladybirds.

Sci Rep 2018 10 29;8(1):15966. Epub 2018 Oct 29.

Department of Organismic and Evolutionary Biology, Harvard University, 22 Divinity Avenue, Cambridge, Massachusetts, 02138, USA.

Our understanding of fungal diversity is far from complete. Species descriptions generally focus on morphological features, but this approach may underestimate true diversity. Using the morphological species concept, Hesperomyces virescens (Ascomycota, Laboulbeniales) is a single species with global distribution and wide host range. Since its description 120 years ago, this fungal parasite has been reported from 30 species of ladybird hosts on all continents except Antarctica. These host usage patterns suggest that H. virescens could be made up of many different species, each adapted to individual host species. Using sequence data from three gene regions, we found evidence for distinct clades within Hesperomyces virescens, each clade corresponding to isolates from a single host species. We propose that these lineages represent separate species, driven by adaptation to different ladybird hosts. Our combined morphometric, molecular phylogenetic and ecological data provide support for a unified species concept and an integrative taxonomy approach.
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http://dx.doi.org/10.1038/s41598-018-34319-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6206035PMC
October 2018

Laboulbeniales hyperparasites (Fungi, Ascomycota) of bat flies: Independent origins and host associations.

Ecol Evol 2018 Aug 24;8(16):8396-8418. Epub 2018 Jul 24.

Department of Organismic and Evolutionary Biology Farlow Reference Library and Herbarium of Cryptogramic Botany Harvard University Cambridge Massachusetts.

The aim of this study was to explore the diversity of ectoparasitic fungi (Ascomycota, Laboulbeniales) that use bat flies (Diptera, Hippoboscoidea) as hosts. Bat flies themselves live as ectoparasites on the fur and wing membranes of bats (Mammalia, Chiroptera); hence this is a tripartite parasite system. Here, we collected bats, bat flies, and Laboulbeniales, and conducted phylogenetic analyses of Laboulbeniales to contrast morphology with ribosomal sequence data. Parasitism of bat flies by Laboulbeniales arose at least three times independently, once in the Eastern Hemisphere () and twice in the Western Hemisphere (, ). We hypothesize that the genera and evolved independently from lineages of ectoparasites of true bugs (Hemiptera). We assessed phylogenetic diversity of the genus by considering the LSU rDNA region. Phenotypic plasticity and position-induced morphological adaptations go hand in hand. Different morphotypes belong to the same phylogenetic species. Two species, and , show divergence by host utilization. In our assessment of coevolution, we only observe congruence between the Old World clades of bat flies and Laboulbeniales. The other associations are the result of the roosting ecology of the bat hosts. This study has considerably increased our knowledge about bats and their associated ectoparasites and shown the necessity of including molecular data in Laboulbeniales taxonomy.
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http://dx.doi.org/10.1002/ece3.4359DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6145224PMC
August 2018

Bats, Bat Flies, and Fungi: A Case of Hyperparasitism.

Trends Parasitol 2018 09;34(9):784-799

Department of Biology, Western Kentucky University, Bowling Green, KY, USA; Integrative Research Center, Field Museum of Natural History, Chicago, IL, USA.

Bats are parasitized by numerous lineages of arthropods, of which bat flies (Diptera, Nycteribiidae and Streblidae) are the most conspicuous. Bat flies themselves can be parasitized by Laboulbeniales, fungal biotrophs of arthropods. This is known as hyperparasitism, a severely understudied phenomenon. Three genera of Laboulbeniales occur on bat flies: Arthrorhynchus on Nycteribiidae, Gloeandromyces and Nycteromyces on Streblidae. In this review we introduce the parasitic partners in this tripartite system and discuss their diversity, ecology, and specificity patterns, alongside some important life history traits. Furthermore, we cover recent advances in the study of the associations between bat flies and Laboulbeniales, which were neglected for decades. Among the most immediate needs for further studies are detailed tripartite field surveys. The vermin only teaze and pinch Their foes superior by an inch So, naturalists observe, a flea Has smaller fleas that on him prey; And these have smaller still to bite 'em, And so proceed ad infinitum. Jonathan Swift (On Poetry: A Rhapsody, 1733).
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http://dx.doi.org/10.1016/j.pt.2018.06.006DOI Listing
September 2018

Laboulbeniales (Fungi: Ascomycota) infection of bat flies (Diptera: Nycteribiidae) from Miniopterus schreibersii across Europe.

Parasit Vectors 2018 Jul 5;11(1):395. Epub 2018 Jul 5.

Museum of Zoology, Palais de Rumine, Place de la Riponne 6, CH-1014, Lausanne, Switzerland.

Background: Bat flies (Diptera: Nycteribiidae and Streblidae) are obligate, blood-sucking ectoparasites of bats with specialized morphology, life-cycle and ecology. Bat flies are occasionally infected by different species of Laboulbeniales (Fungi: Ascomycota), microscopic fungal ectoparasites belonging to three genera: Arthrorynchus spp. are restricted to the Eastern Hemisphere, while species of Gloeandromyces and Nycteromyces occur on Neotropical bat flies. Little is known about the distribution and host specificity of Arthrorynchus spp. on bat flies. In this study, we focused on sampling bat flies from the cave-dwelling bat species Miniopterus schreibersii. Bat and ectoparasite collection took place in Albania, Croatia, Hungary, Italy, Portugal, Slovakia, Spain and Switzerland. Flies were inspected for Laboulbeniales infections.

Results: Six hundred sixty seven bat flies of five species were collected: Nycteribia latreillii, N. pedicularia, N. schmidlii, Penicillidia conspicua, and P. dufourii. Laboulbeniales infection was observed on 60 specimens (prevalence = 9%). Two Laboulbeniales species, Arthrorhynchus eucampsipodae and A. nycteribiae, were present on three bat fly species. All observations of A. eucampsipodae were on N. schmidlii, and A. nycteribiae was present on P. conspicua and P dufourii. Arthrorhynchus eucampsipodae is, for the first time, reported from Slovakia and Spain. Arthrorhynchus nycteribiae represents a new country record for Portugal and Slovakia. There were no significant differences among infection rates in different countries. Females of N. schmidlii showed a higher infection rate than males with an observable trend (P = 0.0502). No sex differences in infection rate for P. conspicua and P. dufourii were detected. Finally, thallus density was significantly lower in N. schmidlii compared to P. conspicua and P. dufourii.

Conclusions: With this study, we contribute to the knowledge of the geographical distribution and host specificity of Laboulbeniales fungi associated with ectoparasitic bat flies within Europe. We discuss parasite prevalence and host specificity in the light of our findings and the available literature. Penicillidia conspicua is unambiguously the main host species for A. nycteribiae based on our and previous findings. Differences in parasite intensity and sex-biased infections of the fungi are possible depending on the species.
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http://dx.doi.org/10.1186/s13071-018-2921-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6034341PMC
July 2018

Influence of Elytral Color Pattern, Size, and Sex of Harmonia axyridis (Coleoptera, Coccinellidae) on Parasite Prevalence and Intensity of Hesperomyces virescens (Ascomycota, Laboulbeniales).

Insects 2018 Jun 15;9(2). Epub 2018 Jun 15.

Department of Organismic and Evolutionary Biology, Faculty of Arts and Sciences, Harvard University, Cambridge, MA 02138, USA.

is an invasive ladybird (Coleoptera, Coccinellidae) with the potential to outcompete native ladybird species in its invasive distribution area. It was introduced as a biological control agent in many countries but has also spread unintentionally in many others. (Ascomycota, Laboulbeniales) is a minute (200⁻400 µm in size) biotrophic fungus that infects over 30 species of ladybirds. The aim of this study was to evaluate whether the elytral color pattern, size, and sex of affect infection by . Coloration in has been linked to the presence of an antimicrobial alkaloid (harmonine). In fall 2016, we collected 763 individuals in Cambridge, Massaschusetts, of which 119 (16%) bore fruiting bodies. We analyzed 160 individuals (80 infected, 80 uninfected) concerning the intensity of infection by . Elytral sizes and coloration patterns were quantified using digital photography and analytical methods. Smaller ladybirds had a higher prevalence and higher intensity of parasitism. Additionally, male ladybirds bore more thalli compared to female ladybirds. Elytral color patterns had an effect on neither prevalence nor intensity of infection by Laboulbeniales in our dataset, although we found a slight trend to higher intensity of parasitism in more melanic males. This suggests that the development of Laboulbeniales might be affected by certain insect alkaloids.
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http://dx.doi.org/10.3390/insects9020067DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6023472PMC
June 2018

Herpomyces ectoparasitic fungi (Ascomycota, Laboulbeniales) are globally distributed by their invasive cockroach hosts and through the pet trade industry.

Mycologia 2018 Jan-Feb;110(1):39-46

d Department of Organismic and Evolutionary Biology , Harvard University , Cambridge , Massachusetts 02138.

The introduction of non-native animals occasionally results in the co-introduction of their microbial symbionts or parasites. The trade of exotic pets and zoo animals has inadvertently introduced several parasitic species to countries where they are non-native. Both the presence of suitable native hosts and opportunity for dispersal determine whether these non-native species become naturalized. During our studies dealing with species of Herpomyces (Ascomycota, Laboulbeniomycetes), fungi that are exclusively ectoparasitic on cockroaches (Hexapoda, Blattodea), we make use of artificial colonies. Most of our specimens originate from pet stores and laboratory populations. Although they were originally intended for transmission studies, we discovered that some cockroaches from artificial colonies carried fruiting bodies of Herpomyces. We screened a total 292 cockroaches from 11 populations that we maintained after purchase. Sources were different pet stores, a toxicological laboratory, and a biological supply company. In eight populations, we found at least some Herpomyces-infected cockroaches. Parasite prevalence varied between 8.77% and 86.33%. Host associations were Blatta orientalis with Herpomyces stylopygae, Blattella germanica with H. ectobiae, Periplaneta americana with H. periplanetae, Phoetalia pallida with H. leurolestis, and Shelfordella lateralis with an undescribed species of Herpomyces. Apart from the new reports, host associations, and consequences for taxonomy (a new species based on morphological and molecular characters), we started to think about the geographic distributions of these fungi and how we, humans, shape them through spreading hosts and through international pet trade. We reviewed the currently known records of Herpomyces-associated cockroaches and host-parasite relationships. Based on the available data, on a global scale, at least half of the currently known species of Herpomyces are spread by globally invasive host species and through international pet trade. This indicates that the distribution and host range of these obscure and often unnoticed fungi are affected by human activities.
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http://dx.doi.org/10.1080/00275514.2017.1418567DOI Listing
December 2018

A new species of (Leotiomycetes, Helotiales) from Western Siberia.

MycoKeys 2018 20(32):49-63. Epub 2018 Mar 20.

Blaihofstraße 42, 72074 Tübingen, Germany.

A new species of is described based on morphology and molecular data from a collection made in West Siberia. is differentiated by lanceolate, strongly protruding paraphyses and comparatively narrow, fusoid-clavate ascospores. The apothecia are urn-shaped due to a prominent and even collar as in . The species grows on fallen side branches of , a rarely recorded host for . The authors formally describe the new species and provide colour illustrations. In addition, the literature is reviewed on previously described species of . Phylogenetic reconstruction of the lineage, based on the ITS ribosomal DNA, strongly supports the three currently recognised species: , and .
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http://dx.doi.org/10.3897/mycokeys.32.23277DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5904377PMC
March 2018

A tripartite survey of hyperparasitic fungi associated with ectoparasitic flies on bats (Mammalia: Chiroptera) in a neotropical cloud forest in Panama.

Parasite 2018 10;25:19. Epub 2018 Apr 10.

Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, Massachusetts 02138, USA - Smithsonian Tropical Research Institute, Apartado Postal 0843-03092, Balboa, Panama - Herbario UCH, Universidad Autónoma de Chiriquí, Apartado Postal 0427, David, Panama.

The Darién province in eastern Panama is one of the most unexplored and biodiverse regions in the world. The Chucantí Nature Reserve, in Serranía de Majé, consists of a diverse tropical cloud forest ecosystem. The aim of this research was to explore and study host associations of a tripartite system of bats, ectoparasitic flies on bats (Diptera, Streblidae), and ectoparasitic fungi (Ascomycota, Laboulbeniales) that use bat flies as hosts. We captured bats at Chucantí, screened each bat for presence of bat flies, and screened collected bat flies for presence of Laboulbeniales. We mistnetted for 68 mistnet hours and captured 227 bats representing 17 species. We captured Micronycteris schmidtorum, a species previously unreported in Darién. In addition, we encountered the rarely collected Platyrrhinus dorsalis, representing the westernmost report for this species. Of all captured bats, 148 carried bat flies (65%). The number of sampled bat flies was 437, representing 16 species. One species represents a new country record (Trichobius anducei) and five species represent first reports for Darién (Basilia anceps, Anatrichobius scorzai, Nycterophilia parnelli, T. johnsonae, T. parasiticus). All 74 bat fly species currently reported in Panama are presented in tabulated form. Of all screened bat flies, 30 bore Laboulbeniales fungi (7%). Based on both morphology and large ribosomal subunit (LSU) sequence data, we delimited 7 species of Laboulbeniales: Gloeandromyces nycteribiidarum (newly reported for Panama), G. pageanus, G. streblae, Nycteromyces streblidinus, and 3 undescribed species. Of the 30 infected flies, 21 were Trichobius joblingi. This species was the only host on which we observed double infections of Laboulbeniales.
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http://dx.doi.org/10.1051/parasite/2018017DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5892177PMC
October 2018
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