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. 2018 Oct 29;8(1):15966.
doi: 10.1038/s41598-018-34319-5.

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

Danny Haelewaters  1   2 , André De Kesel  3 , Donald H Pfister  4
Affiliations

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

Danny Haelewaters et al. Sci Rep. .

Abstract

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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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Hesperomyces virescens parasitizing Harmonia axyridis. A group of thalli of Hesperomyces virescens attached to the elytral tips of a specimen of Harmonia axyridis (from Watermaal-Bosvoorde, Belgium). Image provided by Gilles San Martin. Inserted is a drawing of a single adult thallus (D. Haelew. 601c, FH 00313615, Byron, Georgia, USA), with the following structures annotated: haustorium; cells I, II, and III of the receptacle; the appendage (app.) with antheridia (anth.); and the perithecium (perith.) with its terminal projections (proj.). Drawing by André De Kesel.
Figure 2
Figure 2
Adult thallus of Hesperomyces virescens. Thallus was removed from a specimen of Psyllobora vigintiduopunctata (ADK763b, Zwin Nature Park, Belgium). Letters a through z refer to begin and end points (landmarks) for measurements taken of 22 parameters. Details in text.
Figure 3
Figure 3
Results of Principal Component Analysis. (a) Morphospace formed by the first two PCs of the PCA showing the importance of ratios. (b,c) Contributions of included ratios to PC1 (b) and PC2 (c) separately. The dashed line is a reference corresponding to the expected value if the contributions were uniform. Contributions above the reference line are considered as important.
Figure 4
Figure 4
PCA using morphometric variables showing variation in thallus shape. Each symbol represents an individual thallus in the two-dimensional morphospace formed by the first two PCs. Thalli are colored by host species (yellow circles Cheilomenes propinqua, green triangles Harmonia axyridis, purple squares Olla v-nigrum).
Figure 5
Figure 5
Phylogenetic reconstruction of Hesperomyces virescens sensu lato. (a) Phylogram reconstructed from the ITS dataset. (b) Phylogram reconstructed from the LSU dataset. Topologies are the result of maximum likelihood inference. For each node, the ML bootstraps (if >70) are presented above the branch leading to that node. The arrowhead in both reconstructions points at the node leading to the Hesperomyces clade. Monophyletic clades are color-coded by host species. All host species included in the analysis are pictured left and right of the phylogenies. Photo credits: Adalia bipunctata, A. decempunctata, Halyzia sedecimguttata, Harmonia axyridis, Gilles San Martin (Flickr); Azya orbigera, Pavel Kirillov (Wikimedia Commons); Cheilomenes propinqua, Sally Adam (iNaturalist); Cycloneda sanguinea, Damon Tighe (iNaturalist); Olla v-nigrum, Roberto Güller (Flickr); Psyllobora vigintimaculata, Katja Schulz (iNaturalist).
Figure 6
Figure 6
Three-gene phylogeny showing results of sequence-based species delimitation methods. Maximum clade credibility tree of the Hesperomyces virescens complex, reconstructed from the concatenated SSU+ITS+LSU dataset. The tree is the result of a Bayesian analysis performed in BEAST. For each node, the ML bootstraps (if >70) and posterior probabilities (if >0.70) are presented above/below the branch leading to that node. Monophyletic clades are color-coded by host species. To the left of the phylogeny, all host species included in the analysis are pictured. Photo credits: Adalia bipunctata, A. decempunctata, Halyzia sedecimguttata, Harmonia axyridis, Gilles San Martin (Flickr); Azya orbigera, Pavel Kirillov (Wikimedia Commons); Cheilomenes propinqua, Sally Adam (iNaturalist); Cycloneda sanguinea, Damon Tighe (iNaturalist); Olla v-nigrum, Roberto Güller (Flickr); Psyllobora vigintimaculata, Katja Schulz (iNaturalist). To the right of the phylogeny, the results of species delimitation analyses are summarized, from left to right: ABGD analysis of the SSU+ITS+LSU alignment; bPTP analysis of the ITS topology; bPTP analysis of the LSU topology; and GMYC analysis of the ITS, LSU and SSU+ITS+LSU ultrametric trees (without outgroups) generated in BEAST. Hatching implies lack of support, whereas no coloration means that clade was absent in that analysis.
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References

    1. Simpson, G. G. Principles of animal taxonomy (Columbia University Press, 1961). - PubMed
    1. 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).
    1. de Queiroz K. Species concepts and species delimitation. Syst. Biol. 2007;56:879–886. doi: 10.1080/10635150701701083. - DOI - PubMed
    1. Blackwell M. The Fungi: 1, 2, 3 … 5.1 million species? Am. J. Bot. 2011;98:426–438. doi: 10.3732/ajb.1000298. - DOI - PubMed
    1. Hibbett D, et al. Sequence-based classification and identification of Fungi. Mycologia. 2016;108:1049–1068. - PubMed

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