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 (Rasmont et al. 2017) when taking a broad approach to Eucera (including Cubitalia, Synhalonia, Tetralonia, and Tetraloniella; Dorchin et al. 2018) and considering Halictus to consist of Halictus s. str. and its sister group Seladonia, the latter including Vestitohalictus (Danforth et al. 1999). As a measure of this stability, only six valid genera have been described for the European bee fauna since 1955, specifically the species-poor lineages Clavipanurgus, Flavipanurgus, and Simpanurgus (Warncke 1972), Hofferia and Stenoheriades (Tkalců 1984), and Chiasmognathus (Engel 2006) (Fig. 1). In contrast, some 20 genera have been described for the broader West Palaearctic region during this time.

Figure 1. 

Cumulative number of valid bee genera by year of description for Europe (as defined by Rasmont et al. 2017) (yellow dots) and the wider West Palaearctic region (blue dots). The recognition of genera follows Rasmont et al. (2017) with modifications as defined in the introduction.

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 (Dorchin et al. 2018), or conversely where a great deal of morphological variation has led to a proliferation of described genera that are paraphyletic (Litman et al. 2016). Integrating phylogenomic datasets with traditional morphological study allows the reciprocal illumination of morphological features in light of molecular evidence, and greatly facilitates the systematic identification of synapomorphies and homologous characters for diagnostic purposes (Bossert et al. 2020). The classification of the Panurginae presents aspects of these problems, and delineating the phylogenetic relationships between the different genera has proved challenging for several decades. This has led to numerous tribal classification schemes, as well as disagreement as to what constitutes a genus in some cases (Patiny 2001; Ascher 2004; Engel 2005; Michener 2007; Ascher and Engel 2017). For example, Engel (2005) places the Melitturgini sensu Patiny (1999a) within the Panurgini and distinct from the Meliturgulina, whereas Michener (2007) places both together in Melitturgini, and Michener (2007) takes a broad approach to Panurgus, including both Flavipanurgus and Simpanurgus as subgenera. Treatment of the tribe Panurgini has been particularly problematic, with some interpretations including a limited number of Old World taxa (Patiny 2001), or conversely including all Old World and even some New World taxa (Ascher 2004).

The lack of resolution from morphological analyses has recently been addressed through a phylogenomic approach using Ultraconserved Elements (UCEs; Bossert et al. 2022). An important finding of that study is that the Old World Panurginae are not a monophyletic group. The tribe Melitturgini, comprising only Camptopoeum and Melitturga, is well-separated from all other Old World genera which can be placed in a single large tribe, the Panurgini. Sister group to the Panurgini is the endemic North American lineage Perditini, and both these lineages are sister group to Melitturgini: Melitturgini + (Perditini + Panurgini). The Melitturgini likely diverged from the lineage that gave rise to the present-day Panurgini and Perditini 46.1 million years ago (95% highest posterior density 36.8-56.1 mya, Bossert et al. 2022), shortly after their most recent common ancestor (MRCA) colonised the Palaearctic. Both Panurgini and Perditini descend from this MRCA, indicating that Panurginae only geodispersed to the Old World a single time (Bossert et al. 2022). Another surprising finding is that one species described as Camptopoeum (Camptopoeum) baldocki Wood & Cross, 2017 on the basis of its seemingly distinctively long glossa (Wood and Cross 2017, the glossa itself being elongate, not possessing the elongate labial palp morphology used in the division between long-tongued and short-tongued bees, see Michener (2007)) is not actually part of the lineage forming Camptopeum and Melitturga (the Melitturgini), but instead is more closely related to the genera Flavipanurgus and Panurgus. Specifically, this species forms a sister group relationship with Flavipanurgus fuzetus Patiny, 1999, which has a short glossa consistent with other members of this genus (Patiny 1999b), but its placement together with C. baldocki renders Flavipanurgus paraphyletic.

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.

As demonstrated at a global scale (Pisanty et al. 2021; Bossert et al. 2022), the use of ultraconserved elements for phylogenetic analysis has considerably improved our understanding on the evolutionary relationships of andrenid bees, including the subfamily Panurginae. In the case of the Panurginae, the reciprocal analysis of morphological characters given our robust molecular phylogeny revealed that certain morphological features used to characterise genera of Old World Panurginae have been overvalued in the past and have incorrectly resulted in the association of Halopanurgus baldocki with the genus Camptopoeum.

Albeit separated by ~50 million years of divergence time (Bossert et al. 2022), certain species of Panurgini and Melitturgini share remarkably similar morphological features, leading authors to conclude close phylogenetic relationships until very recently. The most pertinent example is Camptopoeum, which was included with the two-celled members of the Panurgini by Michener (2007). Halopanurgus baldocki was described as a Camptopoeum (Camptopoeum) because of the elongate tongue, in which the first segment of the labial palpus is about as long as the second to fourth segments taken together. Indeed, based only on tongue morphology, H. baldocki is more similar to Camptopoeum (Camptopoeum) than it is to its sister species Halopanurgus fuzetus, and more similar to Camptopoeum (Camptopoeum) than to Camptopoeum (Epimethea), which have very short glossa. Tongue length within Old World panurgines is therefore clearly homoplasious.

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 (Danforth et al. 2019). Bee mouthparts represent a particularly intuitive example of a morphological structure facing selective pressure. All bee species examined in this study exhibit some degree of host plant specialization and most seem to be true oligoleges. It is expected that tongue length varies among species in respect to their host plant, and the appearance of bee species with physically long tongues within the short-tongued bee families such as Andrenidae (e.g. Shimizu et al. 2014), Colletidae (e.g. Laroca et al. 1989; Rozen and Wyman 2015), and Halictidae (e.g. Burger 2020) is well established, usually being associated with particular floral shapes that necessitate morphological adaptation to access particular resources. In the case of H. baldocki, their long tongues are used to access the nectaries of its host Frankenia laevis (Frankeniaceae) which are found at the base of a tubular corolla, necessitating a long tongue for a bee of only 4 mm in length (Wood and Cross 2017). Halopanurgus fuzetus in turn visits species of Spergularia (Caryophyllaceae, Wood and Cross 2017), which have an open floral structure, and therefore do not require a long tongue to access the nectaries despite their equally small body size. The ~7.5 million years of divergence time between the two Halopanurgus species (Bossert et al. 2022) was sufficient to allow their tongue morphologies to diverge, and it is intuitive that they represent adaptations towards nectar uptake from different host plants. This mirrors the situation in Camptopoeum (Camptopoeum) and Camptopoeum (Epimethea), which based on the very limited number of species whose foraging niches are well understood are specialists of Centaurea (Asteraceae) and Apiaceae, respectively (Friese 1926, TJW unpublished data). Like Frankenia, Centaurea flowers have individual florets in which nectar is found at the bottom of a tubular corolla, whereas in the Apiaceae used by Camptopoeum (Epimethea) species, the floral structure is open and does not require a long tongue to access nectaries.

Against this context, the description of new panurgine genera from the Arabian Peninsula and Central Asia (Engel 2019) based primarily on tongue morphology raises interesting questions. Placing close to Flavomeliturgula Patiny (now within a broad Panurgini, Bossert et al. 2022; Meliturgulina sensu Engel 2019), the genus Belliturgula Engel (Saudi Arabia) is diagnosed predominantly on the basis of tongue characters combined with body colouration (Engel 2019), and the genus Khuzimelissa Engel (Iran and Pakistan) is diagnosed mainly on the basis of tongue characters and additionally on the shape of the outer antennal sulcus. Both genera are monotypic, and were described from female material only, with no male specimens known. Given the labile nature of tongue length within Panurginae, and the lack of male material that was crucial for morphologically confirming differences between the genera in the present study, it is difficult to assess the status of these genera and the relationships between the species related to Flavomeliturgula with confidence.

From a biogeographical perspective, the genera closely related to Panurgus that have been confidently placed through genetic analysis (Bossert et al. 2022) show a West Mediterranean distribution, restricted to Iberia (Halopanurgus and Flavipanurgus) or with particular diversity in the western Maghreb (Panurgus; Patiny and Gaspar 2000; Patiny 2001; Lhomme et al. 2020). The only known collecting localities for Avpanurgus and Simpanurgus being in Algeria and Spain, respectively (Warncke 1972; Patiny 2001), means that they align with this overall pattern; the centres of diversity for other Panurgini clades are located further east, such as Asia (taxa related to Panurginus), and the Middle East to sub-Saharan Africa (taxa related to Meliturgula and Mermiglossa), and also for Camptopoeum whose centre of diversity is the Middle East (Patiny 2001). Though the placement of Avpanurgus and Simpanurgus in the group of genera related to Panurgus requires additional molecular investigation and confirmation, it forms the basis of a suitable hypothesis should fresh specimens become available.

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 3, see Münster-Swendsen 1970; Westrich 1989 for P. calcaratus, P. banksianus, and P. dentipes; Rozen 1971 for P. maroccanus, P. intermedius, P. pici), whereas Pachycephalopanurgus appear to be specialists of the subfamily Asteroideae (Table 3, see Cross 2020 for P. meridionalis). Clearly, a much greater sampling effort is needed for North African Pachycephalopanurgus species, but a nominal specialisation on Asteroideae forms the basis of a testable hypothesis. Why these two lineages of Panurgus seem to divide their efforts between these two lineages of Asteraceae is unclear, but a proposed mechanism is related to their pollen-collecting behaviour. Specifically, when foraging on Astericus (Asteroideae), Pachycephalopanurgus species focus on the non-ligulate disc florets and sweep pollen into their scopae whilst rapidly pulsing and moving their metasoma, a technique that seems unlikely to be effective in the Cichorioideae where only ligulate florets are present (Cross 2020). More broadly, with their spiralled scopal hairs and specialisation on Asteraceae, Panurgus appear to represent another independent lineage of bees that have converged on carrying their pollen dry (Portman and Tepedino 2017), in contrast to their closest relatives Flavipanurgus and Halopanurgus which carry their pollen moistened by nectar (Wood and Cross 2017; Cross and Wood 2018).

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.