Research Article |
Corresponding author: Thomas J. Wood ( thomasjames.wood@umons.ac.be ) Academic editor: Michael Ohl
© 2022 Thomas J. Wood, Sébastien Patiny, Silas Bossert.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Wood TJ, Patiny S, Bossert S (2022) An unexpected new genus of panurgine bees (Hymenoptera, Andrenidae) from Europe discovered after phylogenomic analysis. Journal of Hymenoptera Research 89: 183-210. https://doi.org/10.3897/jhr.89.72083
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Establishing a higher classification of bees based on morphology alone can fail to capture evolutionary relationships when morphological characters either vary very little between distantly related groups, or conversely vary greatly between closely related species. This problem is well represented in the subfamily Panurginae, for which a recent global revision based on phylogenomic data unexpectedly revealed that two Old World species previously placed in Camptopoeum Spinola and Flavipanurgus Warncke, are in fact most closely related to each other, and together form a sister group relationship to the remaining Flavipanurgus and Panurgus Panzer combined. To rectify this situation, we here establish an expanded phylogenomic data set of Old World Panurgini and re-assess generic and subgeneric concepts for the tribe. To solve the paraphyly of Camptopoeum and Flavipanurgus, we establish the new genus Halopanurgus gen. nov. containing the species H. baldocki (Wood & Cross), comb. nov. and H. fuzetus (Patiny), comb. nov., both of which are restricted to coastal sands, saltmarshes, and inland saline lagoons in the extreme south of Portugal and south-west of Spain. Re-evaluation of four recently used subgenera in Panurgus strongly supports a simplified classification of two subgenera; Pachycephalopanurgus Patiny, stat. rev. including Micropanurgus Patiny syn. nov., and Panurgus s. str. including Euryvalvus Patiny. Pachycephalopanurgus species seem to be oligoleges of Asteroideae (Asteraceae), whereas Panurgus s. str. may be oligoleges of Cichorieae (Asteraceae). Our findings reinforce the challenges of establishing a phylogenetically sound classification of Panurginae using morphology alone and illustrate that even in well-studied regions like Europe unrecognised genera can persist in underexplored corners of the continent.
Asteraceae, halophile, Iberian endemic species, solitary bees, taxonomy
The bee fauna of Europe boasts the longest history of study, and as such has a relatively stable system of taxonomic classification. Depending on taxonomic interpretation, 73 bee genera are known from Europe (
Key to maintaining stable bee genera for the future is the use of large-scale molecular revisions to re-evaluate lineages where generic boundaries are ambiguous due to morphological intergradation (
The lack of resolution from morphological analyses has recently been addressed through a phylogenomic approach using Ultraconserved Elements (UCEs;
Given this paraphyly, the main objectives of the current work are therefore to reassess the diagnosability of Flavipanurgus and Panurgus, re-evaluate the current usage of subgenera for Panurgus, and identify morphological criteria to allow for recognition of these different lineages. Considering morphological, molecular, and ecological aspects, we describe the new genus Halopanurgus gen. nov. to ensure that all genera are strictly monophyletic. We also take the opportunity to discuss the relationships between the different West Mediterranean genera of Panurgini, as this region is clearly a particular centre of their Old World diversity, and lastly we propose a simplified subgeneric classification for the genus Panurgus.
To better understand the phylogenetic relationships of Panurgus and its currently used subgenera, as well as of Flavipanurgus, and Halopanurgus gen. nov., we assembled a taxon-dense sampling of Old World Panurginae. We obtained DNA sequence data from a recently published phylogeny of Andrenidae (
The scientific names of the included species with their collection localities and voucher depositories. NCBI SRA IDs marked with an asterisk (*) indicate samples that are newly published. Most voucher specimens are labelled with a green coloured label which carries the voucher code. UCE assemblies of the newly generated sequence are available on the FighShare repository associated with this article (10.6084/m9.figshare.15033552). Acronyms for the collection depositories: Cornell Univ. Insect Collection (CUIC); Collection Silas Bossert (CSB); University of Mons-Hainaut, Mons, Belgium (UMH); Collection Thomas Wood, Mons, Belgium (CTW).
Taxon | Locality | Voucher depository | Collector / Identifier | Voucher Code | SRA |
---|---|---|---|---|---|
Camptopoeum (Camptopoeum) frontale | Turkey: Agr I, Gögoglu | UMH | P. Rasmont / D. Michez | BND-1981 | SRR16232743 |
Camptopoeum (Camptopoeum) negevense | Israel: S Negev, 13 km N Shizzafon Jct. | n/a | from |
Camp 41 | SRR16232742 |
Clavipanurgus desertus | Morocco: S. Anezal | CSB | Michez & Patiny / Michez & Patiny | BND-1982 | SRR16232741 |
Flavipanurgus flavus | Portugal: Algarve, Aljezur | CTW | T. J. Wood / T. J. Wood | BND-2119 | SRR16232720 |
Flavipanurgus ibericus | Portugal: Alentejo, Mértola | CSB | I. C. Cross / T. J. Wood | BND-2117 | SRR16232718 |
Flavipanurgus kastiliensis | Portugal: Pardelhas, Vila Real | CTW | T. J. Wood / T. J. Wood | BND-2118 | SRR16232717 |
Flavipanurgus venustus | Spain: Doñana | UMH | F.P. Molina / D. Michez | BND-1926 | SRR17049175 |
Halopanurgus baldocki | Portugal: Algarve, Cacela Velha | CSB | T. J. Wood / T. J. Wood | BND-1923 | SRR16232744 |
Halopanurgus fuzetus | Portugal: Algarve, Cacela Velha | CTW | T. J. Wood / T. J. Wood | BND-2120 | SRR16232719 |
Macrotera (Macroterella) mortuaria | USA: NV, Clark Co., Sacatone Wash | BBSL | T. Griswold / T. Griswold | BND-2005 | SRR16232673 |
Melitturga (Melitturga) clavicornis | France: Hérault, Causse de la Selle | n/a | from |
Mecl 73 | SRR16232665 |
Meliturgula (Meliturgula) scriptifrons | South Africa: Limpopo, 77 km S Ellisras | CUIC | B.N.D. / B.N.D. #CUIC code: 04-22 | BND-1037 | SRR16232644 |
Neffapis longilingua | Chile: Coquimbo Region, Vicuña | RPSP | L.Packer / L. Packer | BBX-694 | SRR16232638 |
Panurgus (Pachycephalopanurgus) acutus | Morocco/SW: 15 km NE Agadir | CSB | C. Schmid-Egger / S. Patiny | BND-1952 | SRR16232763 |
Panurgus (Pachycephalopanurgus) calceatus | Morocco: Errachidia-Erfoud | UMH | Michez & Patiny / Michez & Patiny | BND-1931 | SRR17049183 |
Panurgus (Pachycephalopanurgus) canescens | Spain: Sierra Nevada | UMH | J. Ortiz-Sánchez / S. Patiny | BND-1932 | SSR17049182 |
Panurgus (Pachycephalopanurgus) convergens | Morocco: Anezal | UMH | Michez & Patiny / Michez & Patiny | BND-1933 | SSR17049181 |
Panurgus (Pachycephalopanurgus) farinosus | Morocco: Marrakech | UMH | Michez & Patiny / Michez & Patiny | BND-1936 | SSR17049180 |
Panurgus (Pachycephalopanurgus) nigriscopus | Morocco: Drâa-Tafilalet, Ouarzazate | CSB | Michez & Patiny / Michez & Patiny | BND-1938 | SRR16232758 |
Panurgus (Pachycephalopanurgus) rungsii | Morocco: Drâa-Tafilalet, Ouarzazate | CSB | Michez & Patiny / Michez & Patiny | BND-1943 | SRR16232737 |
Panurgus (Panurgus) avarus | Morocco: Drâa-Tafilalet, Ouarzazate | CSB | Michez & Patiny / Michez & Patiny | BND-1929 | SRR16232762 |
Panurgus (Panurgus) banksianus | France: Pyrénées-Or. Eyne, cabane météo | UMH | D. Michez / D. Michez | BND-1930 | SRR16232761 |
Panurgus (Panurgus) calcaratus | Spain: Province of Almería | UMH | J. Ortiz-Sánchez / S. Patiny | BND-514 | SSR17049179 |
Panurgus (Panurgus) cephalotes | Portugal: Trás-os-montes, Espinhosela | CTW | T. J. Wood / T. J. Wood | BND-1985 | SSR17049178 |
Panurgus (Panurgus) dentatus | Morocco: Drâa-Tafilalet, Imider | UMH | Michez & Patiny / Michez & Patiny | BND-1934 | SSR17049177 |
Panurgus (Panurgus) dentipes | France: Marseilles, Campus Luminy | UMH | D. Michez / D. Michez | BND-1935 | SRR16232760 |
Panurgus (Panurgus) maroccanus | Morocco: Drâa-Tafilalet, Ouarzazate | CSB | Michez & Patiny / Michez & Patiny | BND-1937 | SRR16232759 |
Panurgus (Panurgus) niloticus | Morocco: Drâa-Tafilalet, Ouarzazate | UMH | Michez & Patiny / Michez & Patiny | BND-1939 | SRR16232757 |
Panurgus (Panurgus) perezi | Portugal: Trás-os-montes, Vila Real | CTW | T. J. Wood / T. J. Wood | BND-1940 | SSR17049176 |
Panurgus (Panurgus) pici | Morocco: Drâa-Tafilalet, Ouarzazate | UMH | Michez & Patiny / Michez & Patiny | BND-1941 | SRR16232740 |
Panurgus (Panurgus) pyropygus | Morocco: Drâa-Tafilalet, Ouarzazate | CSB | Michez & Patiny / Michez & Patiny | BND-1942 | SRR16232738 |
Panurgus (Panurgus) siculus | Malta: Southeastern District, Għaxaq | UMH | Michez & Balzan / D. Michez | BND-1944 | SRR16232736 |
Perdita (Hesperoperdita) trisignata | USA: California | n/a | from |
PeHe 77 | SRR16232659 |
Perdita (Pygoperdita) californica | USA: CA, Contra Costa Co., Donner Cyn. | n/a | B. Danforth / n. a. | BND-518 | SRR16232713 |
Plesiopanurgus (Zizopanurgus) zizus | Morocco: Drâa-Tafilalet, Ouarzazate | CSB | Michez & Patiny / Michez & Patiny | BND-1945 | SRR16232657 |
The molecular lab procedures for UCE sequencing of the nine newly analysed samples are detailed in
We estimated phylogenetic relationships with the maximum likelihood implementation IQ-Tree (v. 2.1.3;
Newly generated SPAdes assemblies, the concatenated alignment, tree files, and the input files used to generate the phylogeny are deposited in a FigShare online repository associated with this article (10.6084/m9.figshare.15033552). Unprocessed Illumina sequence reads generated for this study are deposited in the NCBI Sequence Read Archive (SRA) under BioProject PRJNA783908 or under the individual identifiers listed in Table
Pollen was removed from Panurgus species whose pollen preferences have not previously been quantified to assess their pollen preferences following the methodology of Wood & Roberts (2018). The size of pollen loads on individual bees was estimated, ranging from a full load to a one-eighth load. Pollen grains were removed from the scopa using an entomological pin and transferred to a drop of water on a microscope slide. Grains were left to absorb water for a few minutes and then the slides were gently heated to allow evaporation. Molten glycerine jelly stained with fuchsin was added, and the slide was sealed with a coverslip. The percentage of the load composed of different plant taxa was estimated along three randomly selected lines across the cover slip at a magnification of ×400. The percentage of the load was estimated by the relative area of the slide occupied by each plant species, rather than the absolute number of grains. Pollen species representing < 2% of the load were excluded from further analysis because their presence might have arisen from contamination. The percentages of pollen collected were multiplied by the overall size of each load to give a final weighting i.e., a taxon comprising 50% of a ¾ full pollen load would receive a weight of 37.5, whereas a taxon with 100% of a full (1/1) pollen load would receive a weight of 100.0. Pollen loads were identified to the lowest taxonomic level possible using a reference collection assembled during the project, in most cases to subfamily. Host range (dietary specialisation) was characterised following the criteria of
Morphological terminology follows
Combining the newly presented UCE sequences of Panurgus with previously published data led to a concatenated sequence alignment of 1,289,627 DNA nucleotides and 35 species. The maximum likelihood analysis with IQ-Tree produced a highly supported phylogeny that resolves the phylogenetic relationships among the examined genera and specifically of the subgenera of Panurgus (Fig.
Maximum Likelihood phylogeny of Panurgus, Flavipanurgus, and the newly described genus Halopanurgus gen. nov., based on 2,055 ultraconserved elements. Taxonomic names reflect the nomenclatural changes proposed in this study. Node support corresponds to 100 ultrafast bootstrap support values unless indicated otherwise.
Our phylogeny shows that Flavipanurgus in its previous sense, i.e., including “Flavipanurgus” fuzetus, is not a monophyletic group (Fig.
The presented molecular-phylogenetic relationships allow us to illuminate the subgeneric concepts of Panurgus with the four subgenera Euryvalvus, Micropanurgus, Panurgus, and Pachycephalopanurgus as established by
Camptopoeum baldocki Wood & Cross, 2017
Halopanurgus can be recognised as a panurgine because of its black body with yellow maculations on the head, mesosoma, and metasoma, its small size (4–5 mm), its two submarginal cells, apically truncate marginal cell, poorly developed femoral scopa, two subantennal sutures, and weak facial fovea, these shining, hairless. It is best diagnosed with reference to other similar small, yellow-marked genera with two submarginal cells, as broad characters like those used for tribal classification by
Halopanurgus can be confused with Camptopoeum because of the similar structure of the male S7 and genital capsule. Camptopoeum has S7 as broad as long or slightly longer than broad, almost parallel sided, and with a broad apical notch (Fig.
Separation from Flavipanurgus is simple in the male sex, as Flavipanurgus has S7 clearly broader than long, and deeply excavated apicomedially (Figs
Halopanurgus can be rapidly separated from Simpanurgus because it lacks distinctively flattened fore tarsi and clavate antennae (Figs
Panurgine male sternum seven 12 Halopanurgus baldocki 13 Avpanurgus flavofasciatus 14 Camptopoeum (Epimethea) variegatum 15 Flavipanurgus flavus 16 Flavipanurgus kastiliensis 17 Panurgus (Panurgus) calcaratus 18 Panurgus (Panurgus) dentipes 19 Panurgus (Pachycephalopanurgus) farinosus.
Small (4–5 mm) black bees with extensive yellow maculations on head, mesosoma, and metasoma; pronotal lobe, metanotum, and at least some parts of terga always yellow marked, otherwise variable. Male with at least clypeus always yellow, centrally with two small black maculations (Fig.
Panurgine faces 20 Halopanurgus baldocki comb. nov. male 21 Avpanurgus flavofasciatus male 22 Halopanurgus fuzetus comb. nov. female 23 Flavipanurgus granadensis female 24 Flavipanurgus kastiliensis male 25 Simpanurgus phyllopodus male, including 26 male antennae and 27 male fore tarsi.
Face with fine and weak punctures, not strongly contrasting underlying integument (Figs
The name is a combination of the prefix Halo- (Greek for salt) with the genus name Panurgus because of the pronounced affinity for saline soils shown by the two constituent species, both being restricted to saltmarshes, coastal sands, and inland saline lagoons (Wood & Cross 2017; Cross & Wood 2018;
Flavipanurgus Warncke, 1972: 69. Type species: Panurgus flavus Friese, 1897
No genetic samples were available for F. granadensis (Warncke, 1987) or F. merceti (Vachal, 1910). However, examination of males of these two species shows that they clearly belong in Flavipanurgus: S7 is deeply excavated apicomedially, and the genital capsule has the gonocoxae lacking apical points along with flattened and apically spatulate gonostyli (Figs
Six species, Flavipanurgus flavus (Friese, 1897), Flavipanurgus granadensis (Warncke, 1987), Flavipanurgus ibericus (Warncke, 1972), Flavipanurgus kastiliensis (Warncke, 1987), Flavipanurgus merceti (Vachal, 1910), and Flavipanurgus venustus (Erichson, 1835).
Panurgus Panzer, 1806: 209. Type species: Andrena lobata Panzer, 1799 = Apis calcarata Scopoli, 1763
Eriops Klug, 1807: 207, 227. Type species: Andrena lobata Panzer, 1799 = Apis calcarata Scopoli, 1763, monobasic.
Eryops Latreille, 1811: 716, unjustified emendation of Eriops Klug, 1807
Panurgus (Euryvalvus) Patiny, 1999c: 316. Type species: Apis banksiana Kirby, 1802, by original designation.
The subgenus can be separated from Pachycephalopanurgus by the shape of the male S7 which is always broad, approximately as long as wide, and never strongly apicomedially excavated (Figs
All Panurgus species previously placed in Panurgus s. str. and Euryvalvus (
Revised subgeneric classification system for the genus Panurgus, with all globally known species.
SubgenusPanurgus s. str. Panzer, 1806 | SubgenusPachycephalopanurgus Patiny, 1999 stat. rev. |
---|---|
Panurgus afghanensis Warncke, 1972 | Panurgus acutus Patiny, 2002 |
Panurgus avarus Warncke, 1972 | Panurgus calceatus Pérez, 1895 |
Panurgus banksianus (Kirby, 1802) | Panurgus canescens Latreille, 1811 |
Panurgus buteus Warncke, 1972 | Panurgus convergens Pérez, 1895 |
Panurgus calcaratus (Scopoli, 1763) | Panurgus farinosus Warncke, 1972 |
Panurgus canarius Warncke, 1972 | Panurgus meridionalis Patiny, Ortiz & Michez, 2005 |
Panurgus cephalotes Latreille, 1811 | Panurgus minor Warncke, 1972 |
Panurgus corsicus Warncke, 1972 | Panurgus nigriscopus Pérez, 1895 |
Panurgus cyrenaikensis Warncke, 1972 | Panurgus ovatulus Warncke, 1972 |
Panurgus dargius Warncke, 1972 | Panurgus rungsii Benoist, 1937 |
Panurgus dentatus Friese, 1901 | |
Panurgus dentipes Latreille, 1811 | |
Panurgus intermedius Rozen, 1971 | |
Panurgus maroccanus Pérez, 1895 | |
Panurgus niloticus Warncke, 1972 | |
Panurgus oblitus Warncke, 1972 | |
Panurgus perezi Saunders, 1882 | |
Panurgus pici Pérez, 1895 | |
Panurgus platymerus Pérez, 1895 | |
Panurgus posticus Warncke, 1972 | |
Panurgus pyropygus Friese, 1901 | |
Panurgus siculus Morawitz, 1872 | |
Panurgus sidensis Warncke, 1987 | |
Panurgus vachali Pérez, 1895 |
Panurgus (Pachycephalopanurgus) Patiny, 1999c: 316. Type species: Panurgus rungsii Benoist, 1937, by original designation.
Panurgus (Stenostylus) Patiny, 1999c: 317. [not Stenostylus Pilsbury, 1898]. Type species: Panurgus ovatulus Warncke, 1972, by original designation syn. nov.
Panurgus (Micropanurgus)
Patiny, in
The subgenus can be separated from Panurgus s. str. by the shape of the male S7 which has the lateral corners strongly produced into long, apical projections, these bearing a short tuft of hairs laterally (Figs
All Panurgus species previously placed in Pachycephalopanurgus and Micropanurgus (
Compared to the baseline of
1 | Male S7 with extremely narrow stem, medially with apical projection that is deeply notched, forming a ‘Y’ shape, apical breadth greater than length (Fig. |
Avpanurgus Warncke |
– | Male S7 narrow or broad, notched or not, but never with a ‘Y’ shaped apical projection (Figs |
2 |
2 | Male antennae clavate, clearly broadened apically (Fig. |
Simpanurgus Warncke |
– | Male antennae not clavate, apical segments not noticeably broader than basal segments (e.g. Figs |
3 |
3 | Male S7 comparatively narrow, slightly broader than long, medially notched (Fig. |
Halopanurgus gen. nov. |
– | Male S7 broad, much broader than long, strongly excavated medially or not, but not narrowly notched (Figs |
4 |
4 | Body with yellow markings (except female of F. flavus (Friese, 1897)). Scopal hairs simple, not spiralled. Genitalia with gonocoxae lacking apical points, inner margin rounded, gonostyli flattened in lateral plane, spatulate (Figs |
Flavipanurgus Warncke |
– | Body never with yellow markings. Scopal hairs distinctively and minutely spiralled. Genitalia with gonocoxae usually with apical points (Figs |
Panurgus Panzer |
A total of 93 pollen loads were analysed from nine Panurgus species (Table
Host plant spectrum and inferred category of host use in Panurgus species. n total number of pollen loads, N number of pollen loads from different localities. Plant taxa AST, Asteraceae.
Species | n | N | Results of microscopic analysis of pollen grains (% pollen grains) | % Pure loads of preferred host | % Loads with preferred host | Host range |
---|---|---|---|---|---|---|
P. (Panurgus) | ||||||
Panurgus cephalotes | 28 | 15 | AST (Cichorioideae) 98.9, AST (Asteroideae) 1.1 | 100.0 | 100.0 | Broadly oligolectic (Asteraceae, Cichorioideae) |
Panurgus maroccanus | 14 | 5 | AST (Cichorioideae) 91.1, AST (Asteroideae) 9.9 | 100.0 | 100.0 | Possibly broadly oligolectic (Asteraceae, Cichorioideae) |
Panurgus perezi | 23 | 14 | AST (Cichorioideae) 100.0 | 100.0 | 100.0 | Broadly oligolectic (Asteraceae, Cichorioideae) |
P. (Pachycephalopanurgus) | ||||||
Panurgus calceatus | 10 | 2 | AST (Asteroideae) 65.9, AST (Cichorioideae) 26.0, AST (Carduoideae) 8.1 | 100.0 | 100.0 | Broadly oligolectic (Asteraceae) |
Panurgus canescens | 12 | 8 | AST (Asteroideae) 100.0 | 100.0 | 100.0 | Broadly oligolectic (Asteraceae, Asteroideae) |
Panurgus convergens | 2 | 2 | AST (Asteroideae) 100.0 | 100.0 | 100.0 | Possibly broadly oligolectic (Asteraceae, Asteroideae) |
Panurgus nigriscopus | 1 | 1 | AST (Asteroideae) 100.0 | 100.0 | 100.0 | Possibly broadly oligolectic (Asteraceae, Asteroideae) |
Panurgus ovatulus | 1 | 1 | AST (Asteroideae) 100.0 | 100.0 | 100.0 | Possibly broadly oligolectic (Asteraceae, Asteroideae) |
Panurgus rungsii | 2 | 2 | AST (Asteroideae) 94.0, AST (Carduoideae) 6.0 | 100.0 | 100.0 | Possibly broadly oligolectic (Asteraceae, Asteroideae) |
As demonstrated at a global scale (
Albeit separated by ~50 million years of divergence time (
This confusion that arose from misleading tongue morphology serves as a cautionary tale into panurgine classification. Tongue length can clearly be a labile morphological character and is not necessarily suitable for diagnosing suprageneric taxa (
Against this context, the description of new panurgine genera from the Arabian Peninsula and Central Asia (
From a biogeographical perspective, the genera closely related to Panurgus that have been confidently placed through genetic analysis (
A further line of evidence that can help inform our understanding of panurgine groups are their pollen preferences. Though the division of Panurgus into two subgenera is justified on the basis of the strong molecular and morphological evidence in the male sex, this division between Panurgus s. str. and Pachycephalopanurgus may also be reflected in their use of Asteraceae pollen. All known Panurgus species are oligoleges of Asteraceae, but Panurgus s. str. are specialists of the subfamily Cichorioideae (Table
Our thanks go to Esther Ockermüller and Martin Schwarz for access to the Warncke Collection, loan of material, and hospitality at Linz, and to Ian Cross for access to his personal collection. We also thank Pierre Rasmont for substantial assistance with photography. TJW is supported by an F.R.S.-FNRS fellowship “Chargé de recherches”. This work was supported by NSF grant DEB-2127744 and a Peter Buck fellowship to SB. The authors thank Laurence Packer, Zachary Portman, and an anonymous reviewer for comments that substantially improved the manuscript.