Neopasites (Roig-Alsina, 1991)

Bossert, Silas, Copeland, Robert S., Sless, Trevor J. L., Branstetter, Michael G., Gillung, Jessica P., Brady, Seán G., Danforth, Bryan N., Policarová, Jana & Straka, Jakub, 2020, Phylogenomic and Morphological Reevaluation of the Bee Tribes Biastini, Neolarrini, and Townsendiellini (Hymenoptera: Apidae) With Description of Three New Species of Schwarzia, Insect Systematics and Diversity 4 (6), No. 1, pp. 1-29 : 23-24

Neopasites is a Subgenus of Biastes

Biastes and Neopasites as used previously (e.g., by Michener 2007, Ascher and Pickering 2020; Fig. 2 ) each comprise five described species from the Nearctic ( Neopasites ) and Palearctic ( Biastes ). Clear diagnostic features to separate the groups using morphology proved difficult to obtain. Michener’s (2007) identification key uses size ratios of the two submarginal cells but this character fails to identify B. truncatus (and other Melittoxena ) as Biastes ( Fig. 2 ). In these species, the second submarginal cell is shorter than the first, as in Neopasites . The most decisive character used in Michener’s (2007) key is the shape, position and pubescence of the pseudopygidial area on the fifth tergum of females. This character, which is illustrated in Bossert (2019, their Fig. 7 ), allows the separation of females but is not sufficient to justify the recognition of separate genera under the requirement of natural groups ( Figs. 1 and 2 ). Roig-Alsina (1991) indicated a possible paraphyly of Biastes in respect to Neopasites because of the pointed sting shape of Biastes truncatus . His study found the sting of other examined Biastes and Neopasites to be bifid apically, thus indicating a paraphyletic Biastes ( Roig-Alsina 1991) . It is this exact species ( B. truncatus ) that renders Biastes in the old sense paraphyletic in our study ( Figs. 1 and 2 ). Interestingly, the same species was regarded as distinctly different and was transferred into a new genus Melittoxena in one of the earliest treatments of the group, nearly 150 yr ago (based on the above mentioned differences in wing venation; Morawitz 1873). Melittoxena was synonymized with Biastes shortly thereafter ( Radoszkowski 1874, Friese 1895) and gained little subsequent attention in the field. However, it was resurrected by Popov (1933), who uses Melittoxena as a subgenus of Biastes based on comparative studies of male genitalia and terminal sterna. Despite careful illustrations, this work was not adopted by a broad scientific community either, likely because of language barriers and limited dissemination (but see Proshchalykin and Lelej 2004).

Our integrative assessment of the relationships of Biastes reveals the recognition of Melittoxena as our preferred approach to solving the problem of the paraphyly of Biastes . Melittoxena has clear morphological features and is diagnosable in both sexes. Its close relationship to the North American taxa is supported by molecular data, as well as morphological and biological similarities. As far as we know, all North American Biastes (subg. Neopasites ) are brood parasites of Dufourea , and so is B. (Melittoxena) truncatus , whereas the Old World Biastes s. str. use hosts of different genera ( Fig. 2 ; ‘ Dufourea clade’). Biastes (Melittoxena) popovi , for which hosts have not yet been observed, occurs in areas in which the only rophitine bees are Dufourea as well ( Proshchalykin and Lelej 2004).

Lastly, we formally synonymize the North American subgenera Neopasites s. str. and Micropasites , which were recognized by Michener (2007) for Neopasites ( Fig. 2 ). These two groups are both species-poor and very similar in their morphology. The main differences are the slightly larger body size of Neopasites and the distinctly reduced maxillary palps of Micropasites . Even though these differences are unambiguous, they do not suffice to support monophyly of the two species placed in the nominotypic subgenus Neopasites , as this group does not have any distinct apomorphic characters at the subgeneric level. The single distinguishing character of Micropasites is potentially a reduction of an ancestral state and could be connected to the overall reduction in body size.

Rhopalolemma is the Sister Genus to Townsendiella Members of the genus Rhopalolemma are rarely collected, enigmatic bees with previously unclear phylogenetic relationships. Conflicting phylogenetic signals of immature and adult morphological features render them a seemingly transitional form between Biastes and Townsendiella . Roig-Alsina (1991) described Rhopalolemma based on a single female adult and noted a resemblance with Townsendiella , but he also found internal structures, particularly those of the sting apparatus, to be synapomorphic with Neopasites . Based on a cladistic analysis of 22 adult morphological characters, he concluded that Rhopalolemma is ‘quite divergent, yet obviously a member of [this tribe]’ Biastini , i.e., of Biastes and Neopasites as used previously ( Fig. 2 ). A subsequent study significantly improved our understanding of the biology of Rhopalolemma through field observations, the description of a new species from both sexes, and detailed accounts of immature stages ( Rozen et al. 1997). Their cladistic analyses, however, revealed conflicting information regarding the phylogenetic position of the genus. While larval morphological characters support a sister group relationship to Townsendiella , adult and oocyte morphology indicate a closer relationship to Neopasites .

The molecular evidence presented herein allows us to shed light on this issue. Phylogenomics strongly supports a sister group relationship of Rhopalolemma and Townsendiella and indicates that larval similarities of these two groups are likely true synapomorphies ( Fig. 2 ). Adult morphological characters that supported Rhopalolemma + Biastes previously, such as the absence of a membranous flap on the S6 of female, the presence of a lateral keel on the same structure, and the absence of stipital combs (Roig- Alsina 1991, Rozen et al. 1997) appear plesiomorphic under this topology. However, certain presence/absence characters, such as the loss or reduction of the stipitial comb, have evolved in multiple bee groups and are likely associated with a parasitic lifestyle ( Michener 2007). The Rhopalolemma lineage diverged from the MRCA of Biastes around 43.0 mya and slightly later (39.6 mya) from Townsendiella . This long period provided ample time to acquire morphological and potential convergent change, especially since all these bees use closely related hosts, co-occur in the same habitats, and feed on the same few seasonally abundant floral resources ( Rozen et al. 1997). This applies to Townsendiella and Neolarra as well, which are the only bees of Neolarrini in the new sense which do not all attack Rophitinae ( Fig. 2 ). Losses and/or reductions of structures could represent adaptive features associated with changing life history traits over the past 46 million years in Neolarrini .

Lastly, the placement of Townsendiella requires a taxonomic change, since it renders Neolarrini in the new sense (and also the former Biastini ) paraphyletic ( Fig. 2 ). We compared the two possible options to solve this problem: 1) Raise Rhopalolemma to its own tribe Rhopalolemmini , representing only two described species and diagnosable by few morphological characters that are largely of internal nature and hard to access. This would have allowed retention of Townsendiellini , another monogeneric tribe with only five species, as well as Biastini with Biastes + Schwarzia (now 15 described species). Alternatively, 2) unite all three lineages in a larger tribal concept that provides better diagnosability and avoids oversplitting at tribal level. The cleptoparasitic Apidae seem already overly subdivided, as they represent only about 7.9% of all described bee species but nevertheless comprise 27.2% of all bee tribes, several of which are monogeneric (numbers based on data from the Discover Life database, Ascher and Pickering (2020)). We therefore decided to sink the tribe Townsendiellini into a larger tribal framework. Evaluating alternative two further revealed a much greater suite of morphological diagnostic characters for adults, mature, and first-instar larvae, as well as eggs, when including the sister group to the former Biastini , Neolarra (see characters in Fig. 2 ). Since Neolarra is also the sole representative of its tribe Neolarrini , we argue that consolidation of these lineages into a comprehensive tribal framework better represents their phylogenetic relationships and will facilitate future research on this group.

The tribe Neolarrini in this new sense can be diagnosed by multiple characters that can be expected to be apomorphic or plesiomorphic ( Fig. 2 ). However, polarization of these characters cannot be sufficiently assessed without a comprehensive analysis with phylogenomic data of a much wider sampling of nomadine taxa. Several diagnostic characters are likely shared with bees of the tribe Hexepeolini , to which the tribe Neolarrini may be most closely related ( Policarová et al. 2019). In contrast, other characters seem to be shared with phylogenetically much more distantly related cleptoparasitic tribes, such as Caenoprosopidini, which also have robust pedicels and only two submarginal cells. These characters therefore almost certainly evolved convergently and may be related to parasitism or miniaturization. In the particular case of distinguishing Neolarrini from Hexepeolini , these characters have practical importance despite their likely plesiomorphic nature.

Figures

Fig. 2. Summary of phylogenetic relationships of Neolarrini with all described species, except for Neolarra. Solid lines show relationships estimated with molecular data and placements with dashed lines are derived from morphology or taxonomic information. Mapped diagnostic characters are listed in Table 3. Larval morphological characters are indicated by a gray background. Information on bee and floral hosts is taken from various sources (Michener 1936,Torchio et al. 1967, Krombein et al. 1979, Warncke 1981, Warncke 1982, Janzon and Svensson 1984, Westrich 1990, Rozen and McGinley 1991, Rozen et al. 1997, Bogusch 2003, Proshchalykin and Lelej 2004, Rozen et al. 2009, Orr and Griswold 2015, Scheuchl and Willner 2016, Westrich 2018). The higher classification of plants follows the APG IV system (The Angiosperm Phylogeny group 2016). Warncke (1982) also lists Systropha curvicornis and S. planidens as hosts of Biastes emarginatus but the source for this information is unclear and has been doubted by other authors (Westrich 2018). No host information is available for Schwarzia and species for which boxes are gray.Asterisks (*) indicate newly described species.

Fig. 7. Female holotype of Schwarzia icipensis sp. nov. (A) Habitus, dorsal view. (B) Habitus, frontal view. Arrow points to region of supra-antennal area with slightly less dense punctation than surroundings. (C) Habitus, lateral view. (D) Details ofT4–T5.(E) Label information as deposited with the holotype.Scale bars show 1 mm.

Fig. 1. Fossil-calibrated chronogram of Neolarrini in the new sense (including Biastes, Neolarra, Rhopalolemma, Townsendiella and Schwarzia) based on 773 ultraconserved elements. Pie charts show possible ancestral ranges. Individual slices are scaled according to their probability as calculated through BioGeoBEARS. Bootstrap support (BS) values and posterior probabilities are omitted but correspond to 100 and 1.0 for all nodes, except for the branching of Oreopasites which has a lower BS value.Asterisks (*) indicate newly described species.Stem and crown ages of host taxa along the timeline on the left are taken from Cardinal et al. (2018). Scale bars next to specimen photographs indicate 2 mm length.