Hygrophorus sect. Olivaceoumbrini: new boundaries, extended biogeography and unexpected diversity unravelled by transatlantic studies

Abstract

As currently delineated, Hygrophorus sect. Olivaceoumbrini is a polyphyletic assembly within subg. Colorati, encompassing glutinous and pigmented taxa. According to available literature, between a dozen and twenty species may belong in the section, mostly represented in continental and boreal forests of Europe and North America. However, the limited phylogenetic and biogeographic coverage of the genus does not presently allow for a reliable assessment of its taxonomic boundaries, nor does it provide a complete picture of species diversity within sect. Olivaceoumbrini. In an ongoing effort to confer an evolutionary backbone to Hygrophorus systematics, we assembled and analysed a dataset comprising 268 intercontinental sequences, including holotypes of 7 taxa previously not positioned phylogenetically, and enriched with collections from largely unexplored Mediterranean and Anatolian ecosystems. Overall, 30 clades are identified within 5 distinct lineages, including 11 species putatively new to science. Seven of these are formally described here as H. agathosmoides, H. albofloccosus, H. canadensis, H. limosus, H. marcocontui, H. pinophilus and H. pustulatoides spp. nov. This enriched coverage of section Olivaceoumbrini s.lat. calls for a re-evaluation of its natural boundaries into a core monophyletic clade, including H. olivaceoalbus and five closely related lookalikes, as well as the assignment of the section rank to the four remaining lineages: sect. Fuscocinerei sect. nov., sect. Limacini sect. nov., sect. Nudolidi sect. nov. and sect. Tephroleuci, respectively. We also stabilize the usage of six historical names, H. glutinifer, H. hyacinthinus, H. mesotephrus, H. olivaceoalbus, H. pustulatus and H. tephroleucus, through designation of two neotypes, three lectotypes and four epitypes. Citation: Bellanger J-M, Lebeuf R, Sesli E, et al. 2021. Hygrophorus sect. Olivaceoumbrini: new boundaries, extended biogeography and unexpected diversity unravelled by transatlantic studies. Persoonia 46: 272-312. https://doi.org/10.3767/persoonia.2021.46.10.

Keywords: Hygrophorus latitabundus; Hygrophorus olivaceoalbus; Hygrophorus persoonii; phylogeny; taxonomy; waxcap.

Fig. 1

ITS phylogeny of Hygrophorus subg. Colorati. Phylogenetic trees inferred from the combined Bayesian and Maximum likelihood analysis of 267 ITS sequences falling in sect. Olivaceoumbrini s.lat. plus, for rooting purposes, 8 sequences in sect. Aurei, Pudorini and Hygrophorus. Branches with strong statistical support (SH-aLRT > 0.8 and BPP ≥ 95 %) are highlighted as thick lines. a. Condensed phylogeny with sequences in sect. Tephroleuci, Limacini and Olivaceoumbrini s.str. collapsed; b. expanded sect. Olivaceoumbrini s.str.; c. expanded sect. Tephroleuci; d. expanded sect. Limacini. The short sequences (ITS2 only) of the isotype of H. bakerensis TENN014219, of the isotype of H. agathosmus f. albus LUG8454 and of collection ADP051014-1 fall, respectively, within the /H. bakerensis, /H. agathosmoides and /H. agathosmus clades. Sequences from type material are highlighted in bold in panels b–d. Grey boxes highlight sect. Olivaceoumbrini s.lat. (Lodge et al. 2014) in panel a and the seven novel species described in the manuscript in panels b–d.

Fig. 1

ITS phylogeny of Hygrophorus subg. Colorati. Phylogenetic trees inferred from the combined Bayesian and Maximum likelihood analysis of 267 ITS sequences falling in sect. Olivaceoumbrini s.lat. plus, for rooting purposes, 8 sequences in sect. Aurei, Pudorini and Hygrophorus. Branches with strong statistical support (SH-aLRT > 0.8 and BPP ≥ 95 %) are highlighted as thick lines. a. Condensed phylogeny with sequences in sect. Tephroleuci, Limacini and Olivaceoumbrini s.str. collapsed; b. expanded sect. Olivaceoumbrini s.str.; c. expanded sect. Tephroleuci; d. expanded sect. Limacini. The short sequences (ITS2 only) of the isotype of H. bakerensis TENN014219, of the isotype of H. agathosmus f. albus LUG8454 and of collection ADP051014-1 fall, respectively, within the /H. bakerensis, /H. agathosmoides and /H. agathosmus clades. Sequences from type material are highlighted in bold in panels b–d. Grey boxes highlight sect. Olivaceoumbrini s.lat. (Lodge et al. 2014) in panel a and the seven novel species described in the manuscript in panels b–d.

Fig. 1

ITS phylogeny of Hygrophorus subg. Colorati. Phylogenetic trees inferred from the combined Bayesian and Maximum likelihood analysis of 267 ITS sequences falling in sect. Olivaceoumbrini s.lat. plus, for rooting purposes, 8 sequences in sect. Aurei, Pudorini and Hygrophorus. Branches with strong statistical support (SH-aLRT > 0.8 and BPP ≥ 95 %) are highlighted as thick lines. a. Condensed phylogeny with sequences in sect. Tephroleuci, Limacini and Olivaceoumbrini s.str. collapsed; b. expanded sect. Olivaceoumbrini s.str.; c. expanded sect. Tephroleuci; d. expanded sect. Limacini. The short sequences (ITS2 only) of the isotype of H. bakerensis TENN014219, of the isotype of H. agathosmus f. albus LUG8454 and of collection ADP051014-1 fall, respectively, within the /H. bakerensis, /H. agathosmoides and /H. agathosmus clades. Sequences from type material are highlighted in bold in panels b–d. Grey boxes highlight sect. Olivaceoumbrini s.lat. (Lodge et al. 2014) in panel a and the seven novel species described in the manuscript in panels b–d.

Fig. 1

ITS phylogeny of Hygrophorus subg. Colorati. Phylogenetic trees inferred from the combined Bayesian and Maximum likelihood analysis of 267 ITS sequences falling in sect. Olivaceoumbrini s.lat. plus, for rooting purposes, 8 sequences in sect. Aurei, Pudorini and Hygrophorus. Branches with strong statistical support (SH-aLRT > 0.8 and BPP ≥ 95 %) are highlighted as thick lines. a. Condensed phylogeny with sequences in sect. Tephroleuci, Limacini and Olivaceoumbrini s.str. collapsed; b. expanded sect. Olivaceoumbrini s.str.; c. expanded sect. Tephroleuci; d. expanded sect. Limacini. The short sequences (ITS2 only) of the isotype of H. bakerensis TENN014219, of the isotype of H. agathosmus f. albus LUG8454 and of collection ADP051014-1 fall, respectively, within the /H. bakerensis, /H. agathosmoides and /H. agathosmus clades. Sequences from type material are highlighted in bold in panels b–d. Grey boxes highlight sect. Olivaceoumbrini s.lat. (Lodge et al. 2014) in panel a and the seven novel species described in the manuscript in panels b–d.

Fig. 1

ITS phylogeny of Hygrophorus subg. Colorati. Phylogenetic trees inferred from the combined Bayesian and Maximum likelihood analysis of 267 ITS sequences falling in sect. Olivaceoumbrini s.lat. plus, for rooting purposes, 8 sequences in sect. Aurei, Pudorini and Hygrophorus. Branches with strong statistical support (SH-aLRT > 0.8 and BPP ≥ 95 %) are highlighted as thick lines. a. Condensed phylogeny with sequences in sect. Tephroleuci, Limacini and Olivaceoumbrini s.str. collapsed; b. expanded sect. Olivaceoumbrini s.str.; c. expanded sect. Tephroleuci; d. expanded sect. Limacini. The short sequences (ITS2 only) of the isotype of H. bakerensis TENN014219, of the isotype of H. agathosmus f. albus LUG8454 and of collection ADP051014-1 fall, respectively, within the /H. bakerensis, /H. agathosmoides and /H. agathosmus clades. Sequences from type material are highlighted in bold in panels b–d. Grey boxes highlight sect. Olivaceoumbrini s.lat. (Lodge et al. 2014) in panel a and the seven novel species described in the manuscript in panels b–d.

Fig. 2

Fixed ITS polymorphisms within the H. agathosmus and H. pustulatus complexes. Nature and position of fixed single nucleotide polymorphisms and indels between: a. H. agathosmoides and H. agathosmus; and b. H. pustulatoides and H. pustulatus. Inserted nucleotide(s) are indicated in triangles above or below the ITS locus, according to the relevant species in the pair. See Supplementary Table 1 and 2 for a more detailed distribution of polymorphisms within these two complexes.

Fig. 3

Typification of Hygrophorus glutinifer and Hygrophorus hyacinthinus. a. Lectotype of H. glutinifer P. Bulliard (1786); b. epitype of H. glutinifer P.-A. Moreau 00102303/LIP0401690; c. neotype of H. hyacinthinus J.-M. Moingeon 10092801/LIP0401691. — Photos by: b. P.-A. Moreau; c. J.-M. Moingeon.

Fig. 4

Typification of Hygrophorus mesotephrus. a–b. Isolectotypes Berkeley K(M)92925 (1853, A) & Broome K(M)92927 (1853, B); c. epitype L. Goodwin K(M)227410. — Photo by: c. L. Goodwin.

Fig. 5

Typification of Hygrophorus olivaceoalbus. a. Lectotype J.C. Schaeffer (1774); b. epitype E. Larsson 196-10/GB0183666!. — Photo by: b. E. Larsson.

Fig. 6

Typification of Hygrophorus pustulatus and Hygrophorus tephroleucus. a. Neotype of H. pustulatus E. Larsson 185-14/GB0183665!; b. lectotype of H. tephroleucus A.J.G.K. Batsch (1789); c. epitype of H. tephroleucus E. Larsson 223-08/GB0207586. — Photos by: a, c. E. Larsson.

Fig. 7

Overview of sect. Olivaceoumbrini. a. H. olivaceoalbus PAM16082601; b. H. canadensis HRL2344/DAOM984766 (holotype); c. H. fuscoalboides HRL2345; d. H. korhonenii EL390-13/GB0183574; e. H. marcocontui KATO Fungi 3554; f. H. whitei JO-01/HRL2892. — Photos by: a. P.-A. Moreau; b–c. R. Lebeuf; d. E. Larsson; e. E. Sesli; f. J. Olson.

Fig. 8

Hygrophorus canadensis sp. nov. a. Collection HRL1601 in situ; b. spores; c. basidia; d–e. pileipellis, radial section; f. lamellar trama hyphae; g. stipitipellis hyphae; h. details of stipitipellis showing hyphae surrounded by a gelatinous cuff covered with small specks of refractive material. — Scale bars: b–c, e–f, h = 10 μm; d, g = 50 μm. — Photo by: a. R. Lebeuf.

Fig. 9

Hygrophorus marcocontui sp. nov. a–b. Collections KATO Fungi 2976 (holotype) & KATO Fungi 3600 in situ; c. spores; d. hymenium with basidia and basidioles; e–f. cystidioid elements found on the lamella surface of some collections; g. pileipellis hyphae; h. stipitipellis hyphae. — Scale bars: c, e–g = 10 μm; d, h = 20 μm. — Photos by: a–b. E. Sesli.

Fig. 10

Overview of sect. Tephroleuci. a. H. agathosmus DB051013; b. H. agathosmoides f. albus AMNH-185145/GB0183713 (holotype); c. H. albofloccosus INAT37760508 (not sequenced but same mycelium as INAT38259606); d. H. exiguus HRL3114; e. H. pinophilus AB09-10-362; f. H. pustulatoides NS3599/HRL2890; g. H. pustulatus CMMF005053; h. H. hyacinthinus EL326-10; i. H. odoratus HRL3088; j. H. suaveolens Kleine 07110801. — Photos by: a. D. Borgarino; b. G.G. Eyjólfsdóttir; c. C. Schwarz; d, i. R. Lebeuf; e. A. Bidaud; f. N. Siegel; g. R. Boyer; h. E. Larsson; j. J. Kleine.

Fig. 11

Hygrophorus agathosmoides sp. nov. a. Collection HRL2823/DAOM984765 in situ (holotype); b. collection EL294-13 in situ; c. spores; d. hymenium; e. cystidioid elements found in the hymenium of some western North American collections; f. pileipellis, radial section; g–h. floccules on stipe; i–j. H. agathosmoides f. trabzonensis, in situ (i, collection KATO Fungi 3264) and cystidioid elements on lamellar faces (j, collection KATO Fungi 3604, holotype). — Scale bars: c–e, g, j = 10 μm; f = 50 μm; h = 25 μm. — Photos by: a. R. Lebeuf; b. E. Larsson; i. E. Sesli.

Fig. 12

Hygrophorus albofloccosus sp. nov. a. Collection UCSC-F-2171 in situ (holotype); b. spores; c. hymenium; d. lamella, radial section; e. pileipellis, radial section; f. stipitipellis; g. stipitipellis hyphae covered with refractive material; h. stipitipellis terminal hyphae. — Scale bars: b–c, g–h = 10 μm; d–f = 50 μm. — Photo by: a. C. Schwarz.

Fig. 13

Hygrophorus pinophilus sp. nov. a. Collection EL289-11 in situ (holotype); b. collection ML411162HA in situ; c. spores; d. hymenium; e. floccule at stipe apex; f. subcuticular hyphae; g. inflated hyphae in lamella trama; h. pileipellis, cluster of parallel hyphae. — Scale bars: c–d, f, h = 10 μm; e, g = 25 μm. — Photos by: a. E. Larsson; b. M. Loizides.

Fig. 14

Hygrophorus pustulatoides sp. nov. a. Collection HRL2832/DAOM984764 in situ (holotype); b. details of stipe; c. spores; d. hymenium; e–f. pileipellis, radial section; g–h. floccules on stipe. — Scale bars: c–d, f, h = 10 μm; e, g = 25 μm. — Photos by: a–b. R. Lebeuf.

Fig. 15

Overview of sect. Limacini. a. H. limacinus EL452-17 (not sequenced); b. H. glutinifer EL214-14; c. H. limosus ML80111HL (not sequenced); d. H. paludosoides YL4339; e. H. sp. 1 HRL1647; f. H. sp. 3 RGT131109-02. — Scale bar: d = 5 cm. — Photos by: a–b. E. Larsson; c. M. Loizides; d. Y. Lamoureux; e. A. Paul; f. R.G. Thorn.

Fig. 16

Hygrophorus limosus sp. nov. a–b. Collections ML80111HL (not sequenced) & ML810192HL in situ; c. spores; d. basidia (insert: basal clamp); e–f. hymenium with basidia, basidioles and cystidioid elements; g. pileipellis, hyphae embedded in gelatinous matrix; h. floccules on stipe. — Scale bars: c–d = 5 μm; e–f = 10 μm; g–h = 20 μm. — Photos by: a–b. M. Loizides.

Fig. 17

Overview of sect. Fuscocinerei and sect. Nudolidi. a. H. mesotephrus EL338-11; b. H. betulae (? = H. adiaphorus); c. H. cf. mesotephrus TENN071861; d. H. tennesseensis HRL0940 (published as H. bakerensis); e. H. bakerensis (not sequenced but from Mt Baker, WA-USA). — Photos by: a. E. Larsson; b. K. Bendiksen; c. R.A. Swenie; d–e. R. Lebeuf.