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

. 2018 Oct 29 ; 8 (1) : 15966. [epub] 20181029

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid30374135

Odkazy
PubMed 30374135
PubMed Central PMC6206035
DOI 10.1038/s41598-018-34319-5
PII: 10.1038/s41598-018-34319-5
Knihovny.cz E-zdroje

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.

Zobrazit více v PubMed

PubMed

de Queiroz, K. The general lineage concept of species, species criteria, and the process of speciation: A conceptual unification and terminological recommendations in Endless forms. Species and speciation (eds Howard, D. J. & Berlocher, S. H.) 57–75 (Oxford University Press, 1998).

PubMed DOI

PubMed DOI

PubMed

Hawksworth DL. The fungal dimension of biodiversity: magnitude, significance, and conservation. Mycol. Res. 1991;95:641–655. doi: 10.1016/S0953-7562(09)80810-1. DOI

PubMed DOI PMC

Taylor DL, et al. A first comprehensive census of fungi in soil reveals both hyperdiversity and fine‐scale niche partitioning. Ecol. Monogr. 2014;84:3–20. doi: 10.1890/12-1693.1. DOI

PubMed DOI

PubMed DOI PMC

PubMed DOI PMC

PubMed DOI

Schluter, D. The ecology of adaptive radiation (Oxford University Press, 2015).

Rundle HD, Nosil P. Ecological speciation. Ecol. Lett. 2005;8:336–352. doi: 10.1111/j.1461-0248.2004.00715.x. DOI

Dobzhansky T. Complete reproductive isolation between two morphologically similar species of Drosophila. Ecology. 1946;27:205–211. doi: 10.2307/1932895. DOI

PubMed DOI

Araújo JPM, Evans HC, Geiser DM, Mackay WP, Hughes DP. Unravelling the diversity behind the Ophiocordyceps unilateralis (Ophiocordycipitaceae) complex: Three new species of zombie-ant fungi from the Brazilian Amazon. Phytotaxa. 2015;220:224–238. doi: 10.11646/phytotaxa.220.3.2. DOI

Weir A, Hammond PM. Laboulbeniales on beetles: host utilization patterns and species richness of the parasites. Biodivers. Conserv. 1997;6:701–719. doi: 10.1023/A:1018318320019. DOI

Weir, A. & Blackwell, M. Fungal biotrophic parasites of insects and other arthropods in Insect-fungal associations: Ecology and evolution (eds Vega, F. E. & Blackwell, M.) 119–145 (Oxford University Press, 2005).

Santamaria S, et al. First Laboulbeniales from harvestmen: the new genus. Opilionomyces. Phytotaxa. 2017;305:285–292. doi: 10.11646/phytotaxa.305.4.4. DOI

Haelewaters D, De Kesel A. De schimmel Hesperomyces virescens, een natuurlijke vijand van lieveheersbeestjes. Entomol. Ber. 2017;77:106–118.

Haelewaters D, et al. Parasites of Harmonia axyridis: current research and perspectives. BioControl. 2017;62:355–371. doi: 10.1007/s10526-016-9766-8. DOI

Cottrell TE, Riddick EW. Limited transmission of the ectoparasitic fungus Hesperomyces virescens between ladybirds. Psyche. 2012;2012:814378. doi: 10.1155/2012/814378. DOI

Majerus, M. E. N. Ladybirds. (Harper Collins, 1994).

Ireland H, Kearns PWE, Majerus MEN. Interspecific hybridisation in the coccinellids: some observations on an old controversy. Entomol. Rec. J. Var. 1986;98:181–185.

Majerus MEN. Interspecific hybridisation in the Coccinellidae. Entomol. Rec. J. Var. 1997;109:11–23.

PubMed DOI

PubMed DOI PMC

PubMed DOI

PubMed DOI PMC

Dayrat B. Towards integrative taxonomy. Biol. J. Linn. Soc. 2005;85:407–415. doi: 10.1111/j.1095-8312.2005.00503.x. DOI

PubMed DOI PMC

PubMed DOI PMC

Leavitt, S. D., Moreau, S. D. & Lumbsch, H. T. The dynamic discipline of species delimitation: progress toward effectively recognizing species boundaries in natural populations in Recent advances in lichenology (eds Upreti, D. K., Divakar, P. K., Shukla, V. & Bajapi, R.) 11–44 (Springer, 2015b).

PubMed DOI PMC

PubMed DOI PMC

PubMed DOI

PubMed DOI PMC

PubMed DOI

PubMed DOI PMC

PubMed DOI PMC

PubMed DOI

PubMed DOI

Kovács GM, Jankovics T, Kiss L. Variation in the nrDNA ITS sequences of some powdery mildew species: do routine molecular identification procedures hide valuable information? Eur. J. Plant Pathol. 2011;131:135. doi: 10.1007/s10658-011-9793-3. DOI

PubMed DOI PMC

PubMed DOI

PubMed DOI PMC

PubMed DOI PMC

Miadlikowska J, Lutzoni F. Phylogenetic revision of the genus Peltigera (lichen-forming Ascomycota) based on morphological, chemical, and large subunit nuclear ribosomal DNA data. Int. J. Plant Sci. 2000;161:925–958. doi: 10.1086/317568. DOI

PubMed DOI

Hawksworth DL. Fungal diversity and its implications for genetic resource collections. Stud. Mycol. 2004;50:9–18.

PubMed DOI

PubMed DOI

Olariaga I, Laskibar X, Holec J. Molecular data reveal cryptic speciation within Tricholomopsis rutilans: description of T. pteridicola sp. nov. associated with Pteridium aquilinum. Mycol. Progress. 2015;14:21. doi: 10.1007/s11557-015-1040-4. DOI

PubMed DOI

PubMed DOI

Adamcik S, et al. A molecular analysis reveals hidden species diversity within the current concept of Russula maculata (Russulaceae, Basidiomycota) Phytotaxa. 2016;270:71–88. doi: 10.11646/phytotaxa.270.2.1. DOI

PubMed DOI PMC

Zelditsch, M. L., Swiderski, D. L. & Sheets H. D. Geometric morphometrics for biologists: a primer (Academic Press, 2012).

De Kesel A, den Neucker V. T. Morphological variation in Laboulbenia flagellata (Ascomycetes, Laboulbeniales) Belg. J. Bot. 2006;138:165–172.

PubMed DOI

PubMed DOI

De Kesel A. Hesperomyces (Laboulbeniales) and coccinellid hosts. Sterbeeckia. 2011;30:32–37.

Thaxter R. Supplementary note on North American Laboulbeniaceae. Proc. Am. Acad. Arts Sci. 1891;25:261–270. doi: 10.2307/20020441. DOI

Maddison WP. Gene trees in species trees. Syst. Biol. 1997;46:523–536. doi: 10.1093/sysbio/46.3.523. DOI

Riddick EW, Cottrell TE. Is the prevalence and intensity of the ectoparasitic fungus Hesperomyces virescens related to the abundance of entomophagous coccinellids. Bull. Insectol. 2010;63:71–78.

Benjamin RK. Introduction and supplement to Roland Thaxter’s contribution towards a monograph of the Laboulbeniaceae. Bibl. Mycol. 1971;80:1–155.

Thaxter R. Contribution towards a monograph of the Laboulbeniaceae. Mem. Am. Acad. Arts Sci. 1896;12:187–429.

Santamaría SL., II Acompsomyces–Ilyomyces. Flora Mycol. Iberica. 2003;5:1–344.

Bates D, Maechler. M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 2015;67:1–48. doi: 10.18637/jss.v067.i01. DOI

Akaike H. New look at statistical-model identification. IEEE Trans. Autom. Control. 1974;19:716–723. doi: 10.1109/TAC.1974.1100705. DOI

Kassambara, A. factoextra: Visualization of the outputs of a multivariate analysis. R package version 1.0.1 https://cran.r-project.org/web/packages/factoextra/index.html (2015).

PubMed DOI PMC

Haelewaters, D. Studies of the Laboulbeniomycetes: Diversity, evolution, and speciation. Ph.D. dissertation thesis, Harvard University (2018).

White, T. J., Bruns, T. D., Lee, S. B. & Taylor, J. W. Analysis of phylogenetic relationships by amplification and direct sequencing of ribosomal RNA genes in PCR Protocols: a guide to methods and applications (eds Innis, M. A., Gelfand, D. H., Sninsky, J. J., White, T. J.) 315–322 (Academic Press, 1990).

Landvik S, Egger KN, Schumacher T. Towards a subordinal classification of the Pezizales. Nord. J. Bot. 1997;17:403–418. doi: 10.1111/j.1756-1051.1997.tb00337.x. DOI

PubMed DOI

PubMed DOI

PubMed DOI PMC

PubMed DOI PMC

Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proc. Gateway Comp. Environ. Workshop. 2010;14 Nov. 2010:1–8.

PubMed DOI PMC

PubMed DOI PMC

Swofford, D. L. PAUP: Phylogenetic Analysis Using Parsimony, Version 3.1 (1991).

PubMed DOI PMC

PubMed DOI PMC

PubMed DOI PMC

PubMed DOI PMC

PubMed DOI PMC

PubMed DOI

Rambaut, A., Suchard, M. A., Xie, D. & Drummond, A. J. Tracer v1.6. http://tree.bio.ed.ac.uk/software/tracer/ (2014).

PubMed DOI

PubMed DOI

Michonneau, F., Bolker, B., Holder, M., Lewis, P. & O’Meara, B. rncl: an interface to the nexus class library. R package version 0.6.0 http://CRAN.R-project.org/package = rncl (2015).

Ezard, T., Fujisawa, T. & Barraclough, T. G. splits: SPecies’ LImits by Threshold Statistics. R package version 1.0-14/r31 http://R-Forge.R-project.org/projects/splits/ (2009).

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

New insights into the DNA extraction and PCR amplification of minute ascomycetes in the genus Laboulbenia (Pezizomycotina, Laboulbeniales)

. 2024 Jun 11 ; 15 (1) : 14. [epub] 20240611

Singleton-based species names and fungal rarity: Does the number really matter?

. 2024 Mar 20 ; 15 (1) : 7. [epub] 20240320

Fungal ectoparasites increase winter mortality of ladybird hosts despite limited effects on their immune system

. 2022 Mar 30 ; 289 (1971) : 20212538. [epub] 20220323

The haustorium as a driving force for speciation in thallus-forming Laboulbeniomycetes

. 2022 Jan 31 ; 13 (1) : 1. [epub] 20220131

Hesperomyces (Fungi, Ascomycota) associated with Hyperaspis ladybirds (Coleoptera, Coccinellidae): Rethinking host specificity

. 2022 ; 3 () : 1040102. [epub] 20230109

Fungal Planet description sheets: 1284-1382

. 2021 Dec ; 47 () : 178-374. [epub] 20211224

Fungal Planet description sheets: 1284-1382

. 2021 Aug ; 47 () : 178-374. [epub] 20211224

Notes on Trochila (Ascomycota, Leotiomycetes), with new species and combinations

. 2021 ; 78 () : 21-47. [epub] 20210211

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

. 2021 Jan 29 ; 11 (1) : 2672. [epub] 20210129

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

. 2020 ; 8 () : e10110. [epub] 20201104

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

. 2020 ; 71 () : 23-86. [epub] 20200730

Fungal Systematics and Evolution: FUSE 5

. 2019 Dec ; 71 () : 141-245. [epub] 20191223

Fifty Shades of the Harlequin Ladybird and a Sexually Transmitted Fungus

. 2019 Nov 01 ; 19 (6) : .

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

. 2019 ; 14 (7) : e0220082. [epub] 20190718

Octosporaconidiophora (Pyronemataceae) - a new species from South Africa and the first report of anamorph in bryophilous Pezizales

. 2019 ; 54 () : 49-76. [epub] 20190610

Morphological species of Gloeandromyces (Ascomycota, Laboulbeniales) evaluated using single-locus species delimitation methods

. 2019 Jun ; 3 () : 19-33. [epub] 20190111

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

. 2019 ; 26 () : 29. [epub] 20190520

Najít záznam

Citační ukazatele

Nahrávání dat...

Možnosti archivace

Nahrávání dat...