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Research Article
New suggestion of the species group reconstruction of genus Nomada Scopoli, 1770 (Hymenoptera, Apidae) from Korea
expand article infoKayun Lim‡§, Seunghwan Lee§
‡ Utah State University, Logan, United States of America
§ Seoul National University, Seoul, Republic of Korea

Corresponding author: Seunghwan Lee ( seung@snu.ac.kr )

Academic editor: Michael Ohl
© 2023 Kayun Lim, Seunghwan Lee.
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: Lim K, Lee S (2023) New suggestion of the species group reconstruction of genus Nomada Scopoli, 1770 (Hymenoptera, Apidae) from Korea. Journal of Hymenoptera Research 96: 805-816. https://doi.org/10.3897/jhr.96.106452
ZooBank: urn:lsid:zoobank.org:pub:DEFCAACD-E148-4CD6-8B29-24CE995C9D79
Open Access

Abstract

Genus Nomada, which includes approximately 800 species, is the largest genus in the subfamily Nomadinae and the sole genus in the tribe Nomadini. Its taxonomic classification is particularly challenging due to high morphological variations, making it one of the most controversial groups in the subfamily. In order to shed light on the complex classification of Nomada species and their tribal position, this study conducted a multi-locus phylogeny using one mitochondrial gene (COI) and five nuclear protein-coding genes (EF1α, Nak, Opsin, Pol Ⅱ, Wingless). The study focused on expanding the knowledge of some East Palearctic species, with the ultimate goal of reviewing species groups of Nomada present in Korea. In this study, we suggest that the ruficornis species group is polyphyletic. Some species should be moved to more appropriate species groups as follows: N. tsunekiana, N. emarginata, and N. flavopicta into the basalis species group; N. aswensis, N. kaguya, and N. taicho into the armata species group.

Keywords

Bees, Cleptoparasite, Nomada, Nomadinae, Molecular phylogeny, Multi-locus

Introduction

Nomada, the only genus in the tribe Nomadini and the largest genus in the subfamily Nomadinae, is composed of around 800 species (Smit 2018). This genus has a predominantly Holarctic distribution in all continents except Antarctica (Alexander 1994). Due to the high morphological diversity exhibited by this genus, its classification into subgroups has been a contentious issue, particularly at the species level, where identification is challenging. For example, the genus has been divided into various subgenera or even designated as new genera by Nearctic taxonomists, while most Palearctic taxonomists have insisted on the species group concept (Snelling 1986; Alexander 1994) Thereafter, Alexander (1994) reconstructed the genus using the species group concept in Nomada which are adducta, armata, basalis, belfragei, bifasciata, erigeronis, furva, gigas, integra, odontophora, roberjeotiana, ruficornis, superba, trispinosa, vegana, and vincta. Of these, the ruficornis species group, which is the largest among the 16 established groups, may be a paraphyletic group due to the lack of apomorphic characters (Alexander 1994). Moreover, he designated Nomada ruficornis Linnaeus as the type species of the ruficornis species group, but N. ruficornis has an apomorphic character that cannot be a common trait to the species group. For instance, the type species has a bifurcated mandible, while most species in the species group have a simple one. As such, the species that belong to the ruficornis species group are more like the remnants of the species that cannot be merged into the other species group (Mitai and Tadauchi 2007).

Nomada species from Korea have been classified into species groups primarily based on the work of Mitai and Tadauchi (Mitai and Tadauchi 2003, 2004, 2005, 2006, 2007, 2008), with an update by Won and Kim (Won and Kim 2013). Initially, molecular phylogenetics using a COI marker was employed by Won to resolve the species group complex of the Nomada in his Ph.D. dissertation (Won 2006). However, as the number of recorded species within Korea has increased and with improvements in molecular phylogenetics, further research is necessary to expand upon the previous study, which was limited in scope by analyzing 12 species and using a single marker.

Recently, with the advancement of phylogenomics and the use of ultra-conserved elements (UCEs), Sless et al. (2022) provided the new classification of the subfamily Nomadinae using UCE and Odanaka et al. (2022) showed paraphyly of ruficornis species group. On the other hand, Lim et al. (2022) noted that with variations in taxon sampling, the ruficornis species group is polyphyletic. However, the taxon sampling of the study was mainly focused on the species that have host information. In this study, the species group concept validity of the genus Nomada proposed by Alexander (1994) was tested using the molecular phylogenetic approach with an increased sampling of the ruficornis species group from Korea, which is currently subject to incomplete and controversial systematic classifications.

Methods

Taxon sampling

For this study, we included 74 species as an ingroup and selected 6 species from Ammobatoidini, Neolarrini, and Hexepeolini as an outgroup (See Suppl. material 1). Outgroup species were chosen due to its close relationship with Nomada based on Sless et al. (2022) and availability in NCBI database. To clarify the validity of the species group concept by Alexander (1994), we included Nomada ruficornis, N. roberjeotiana, N. bifasciata, N. armata, N. furva, as they represent the type species of various species groups. In total, sampling in this study encompasses 8 species groups out of the 16 species groups. We added 44 more Nomada species from Lim et al. (2022), out of which 17 species were newly sequenced for this study, and the remaining sequences were obtained from NCBI (Suppl. material 1).

DNA extraction, PCR amplification, and sequencing

To extract total genomic DNA, we ground up either the detached midleg, head of the alcohol vouchers or dried specimens. The wet lab work protocol was consistent with the supplementary information 3 from Lim et al. (2022). We utilized one mitochondrial protein-coding gene, namely the cytochrome oxidase subunit I gene (COI), and five nuclear protein-coding genes (EF-1α, long-wavelength rhodopsin (opsin), NaK, pol II, and wingless) to maintain consistency with Lim et al. (2022). All DNA vouchers were deposited in the Insect Biosystematics Laboratory at Seoul National University.

Sequencing alignments

We utilized SeqMan Pro version 7.1.0 (DNASTAR, Inc., Madison, WI, U.S.A.) to assemble, check, and trim the raw sequence data. The sequence alignment of all six genes was conducted using MAFFT version 7 (https://mafft.cbrc.jp/alignment/server/), and the sequences were adjusted in Mega 7 with the amino acid translation option. In cases where the length of certain genes differed between the NCBI data and the newly obtained sequences, longer sequences were removed. Finally, the aligned sequences were combined using SequenceMatrix Windows ver. 1.8 (Vaidya et al. 2011).

Phylogenetic analyses

We conducted phylogenetic analyses using two methods, Bayesian inference (BI) and Maximum likelihood (ML). Different potential partitioning schemes, considering codon position and genes, and nucleotide substitution models were assessed using ModelFinder2 (Kalyaanamoorthy et al. 2017) within IQ-TREE 2.2.3 (Minh et al. 2020) using “TESTNEWMERGE” option. Following the implementation of the most suitable partitioning scheme and substitution models, IQ-TREE2 generated a ML tree, and nodal supports were determined through 1000 ultrafast bootstrap replicates (Hoang et al. 2018).

On the other hand, because some models, such as TIM, TNe, TN models, were not applicable in MrBayes 3.2.7 for BI (Ronquist et al. 2012), we excluded the unavailable models in MrBayes by using the “-mset” option to restrict the testing procedure with the “TESTMERGEONLY” (See Suppl. material 2). To conduct the MrBayes analysis, we ran 20 million Markov chain Monte Carlo (MCMC) generations, and trees were sampled every 100 generations. We executed one cold chain and three heated chains for each MCMC analysis. We examined the outcome with Tracer 1.7.1 (Rambaut et al. 2018) and discarded the first 2,500,000 sampled trees as burned in.

Results

The dataset used for the phylogenetic reconstruction contained 660 bp of COI, 442 bp of ef1a, 870 bp of Nak, 459 bp of Opsin, 840 bp of Pol2, 456 bp of Wng, for a total of 3727 bp of the nucleotide sequence. Phylogenies obtained through BI and ML support for the monophyly of Nomada.

Although the monophyly of the tribe Nomadini remains notably stable, the ruficornis species group showed polyphyly, which is consistent with Lim et al. (2022). For example, N. imbricata and N. lathburiana, previously categorized within the ruficornis species group, were nested within the bifasciata species group. Similarly, N. tsunekiana, N. emarginata, and N. flavopicta were clustered with the basalis species group. Furthermore, the roberjeotiana species group showed paraphyly in both ML and BI. Notably, the bifasciata species group formed a well-supported subclade (BS=88, PP=97) with N. lathburiana and N. imbricata, previously considered part of the ruficornis species group.

When it comes to the armata species group, it was also revealed as paraphyletic due to the N. kaguya and N. aswensis, which were previously treated as the ruficornis species group as well, and N. taicho, formerly treated as furva species group according to the Alexander and Schwarz (1994). Because multiple species that were originally placed within the ruficornis species group radiated into multiple species groups, a polyphyly of this species group was confirmed in this study.

Discussion

Phylogeny of subfamily Nomadinae

Alexander first conducted species group classification in the genus Nomada in 1994. There has been a range of prior attempts to proceed with the comprehensive reconstruction of the entire genus Nomada, but after he reconstructed the genus into 16 species groups via cladistic analysis, this classification has been commonly used in its morphological taxonomy (Alexander 1994; Mitai and Tadauchi 2007; Proshchalykin and Lelej 2010; Smit 2018; Lim et al. 2022; Odanaka et al. 2022; Lim and Lee 2023). However, he mentioned that one of the species groups, the ruficornis species group, may be a paraphyletic group that belongs to a remnant of a more comprehensive clade without relatively distinct apomorphic subunits such as in armata and basalis species group (Alexander 1994; Mitai and Tadauchi 2007). Because of this uncertainty, there was confusion about which species was included in which groups. For example, Nomada ginran Tsuneki, 1973 was treated as a bifasciata species group (Mitai and Tadauchi 2004). However, it was reconstructed as a member of the armata species group later (Mitai and Tadauchi 2007). Won also indicated in his PhD thesis that the bifasciata species group, trispinosa species group, and partial ruficornis species group were not clearly congruent with the classification by Alexander (1994) using mitochondrial COI gene (Won 2006). Nevertheless, he did not propose a newly modified classification.

In Odanaka et al. (2022), the largest number of Nomada was exploited for phylogenetic analysis compared to the previous investigations and suggested that the ruficornis species group is paraphyletic, with highlighting potential new species group. In this study, we suggest that the ruficornis species group is polyphyletic, which is congruent with Lim et al. (2022) but with the expanded sampling of East Palearctic species. The discrepancy between the previous classification and redesignation will be discussed below based on Fig. 1.

Figure 1. 

Phylogenetic trees (ML/ BI) of genus Nomada (Photo: Kayun Lim).

Node A

Nomada tsunekiana Schwarz, 1999, which is distributed only in Korea has been considered as the ruficornis species group (Won and Kim 2013). However, it formed a subclade within the basalis species group in this study. According to Alexander (1994), the diagnostic characters of the basalis species group were as follows: 1) mandible simple and round at tip; 2) first flagellar segment. evidently longer than the second or the first two flagella equal in length; 3) malar space closed posteriorly; 4) pygidial plate rounded; 5) margin of the hind tibia with dense straight hair. Among these characters, the 2nd characteristic is the most distinctive character to distinguish the species group from the ruficornis species group. In N. tsunekiana, most of the mentioned characters can be applied to its description except the 5th character as the setae are absent on its hind tibial setae. However, the species is more likely to be placed in the basalis species group rather than the ruficornis species group since it should have a distinctly shorter first flagella to belong to the ruficornis species group (Fig. 2). Therefore, N. tsunekiana, N. emarginata, N. flavopicta should be moved to basalis species group and the absent of hind tibial setae should be accepted as an exception because N. emarginata is also historically placed in the ruficornis species group and possess no setae on the hind tibiae (Smit 2018). The complexity of the roberjeotiana species group might have arisen due to the sampling limitation because the analyses for N. obtusifrons and N. argentata were based on only COI data. Therefore, a more comprehensive taxon sampling should be conducted to enhance the resolution of the roberjeotiana species group.

Figure 2. 

N. tsunekiana female. left, antennae in ventral view; right, hind tibiae (Photo: Kayun Lim).

Node B

The bifasciata species group comprises 21 species worldwide and one of the well-known apomorphic characters is distinctly produced and backwardly curved setae, which is two or three in number on the margin of hind tibiae of the females (Alexander 1994). However, the species group formed the subclade with N. lathburiana, and N. imbricata, which were placed in the ruficornis species group (Alexander 1994), indicating the classification of bifasciata species group may need modification as the apomorphic character for it cannot be applied to these two species. Otherwise, the new species group must be designated with N. lathburiana and N. imbricata. For example, the females of N. lathburiana possess three or four stout and straight setae (Smit 2018), and females of N. imbricata usually have about three, posteriorly curved setae on their hind tibiae (Personal observation). Alexander (1994) agreed that N. imbricata has a similar appearance to the species in the bifasciata species group, but he did not include the N. imbricata in the bifasciata species group because males did not have the apomorphic morphology. Consequently, further investigation of morphology with the increased taxon sampling must be conducted to resolve these species group complexes.

Node C

The expanded multi-gene phylogeny in this study supports the designation of N. ginran within the armata species group, as proposed by Mitai and Tadauchi (2007) because the N. ginran forms the same clade with Nomada armata Herrich-Schäffer, 1839, which is the type species of the armata species group. On the other hand, N. aswensis and N. kaguya were previously treated as the ruficornis species group, and N. nipponica, which was previously considered as the trispinosa species group, also formed the same clade with N. armata. Moreover, N. taicho, formally classified as the furva species group by Alexander and Schwarz (1994), was nested in the armata species group. Therefore, it might be plausible to move N. aswensis and N. kaguya to the armata species group. Traditionally, the ruficornis species group has been considered to have evidently shorter first flagellum than the second, while it is nearly equal in length in N. aswensis females (Mitai and Tadauchi 2007). Also, N. kaguya shares morphological characteristics with N. aswensis and N. ginran, such as stout setae and a generally small body size of less than 8 mm (Won and Kim 2013). However, its first flagellum is distinctly shorter than the second one, suggesting that flagellum length may not serve as a definitive apomorphic character for the ruficornis species group. Therefore, the redesignation of the ruficornis species group with vast sampling of the East Palearctic species must be conducted. When it comes to the N. taicho, it should be moved into the armata species group because of both morphological and molecular evidence. To be specific, it lacks the strongly curved gonostylus with sinuate hair to be furva species group according to the classification by Alexander (1994) and does not form the same subclade with the other species of the furva species group.

Conclusion

In this study, the review of species groups in genus Nomada, with a particular focus on the East Palearctic species, was conducted. Most of the species groups from the traditional classification by Alexander (1994) did not form monophyly. However, this discrepancy may not necessarily stem from inaccuracies in the traditional classification but rather from exceptions found among East Palearctic species, especially those from Northeast Asia. This is attributed to Alexander’s limited examination of collections by Tsuneki, a Nomada taxonomist from Japan. Consequently, the current classification must be expanded with these exceptions as described in the discussion and some species should be moved to the appropriate species group, including N. tsunekiana, N. emarginata, and N. flavopicta into the basalis species group, and N. aswensis, N. kaguya, and N. taicho into the armata species group. When it comes to the bifasciata species group complex, future study must be proceeded with a broad array of taxa to confirm if the two species, N. lathburiana and N. imbricata manifestly form an independent subclade with the basalis species group or remain nested within the bifasciata group. The updated species list with species group reconstruction can be found in Table 1.

Table 1.
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Species list of Nomada from Korea with new suggestion of the species group designation.

No. Recorded species Previous species group This study
1 Nomada abtana Tsuneki, 1973 ruficornis ruficornis
2 Nomada adustaspinae Lim & Lee, 2023 ruficornis ruficornis
3 Nomada amurensis Radoszkowski, 1876 ruficornis ruficornis
4 Nomada aswensis Tsuneki, 1973 ruficornis armata
5 Nomada atra Lim & Lee, 2023 ruficornis ruficornis
6 Nomada biaulacis Lim & Lee, 2023 ruficornis ruficornis
7 Nomada calloptera Cockerell, 1918 ruficornis ruficornis
8 Nomada comparata Cockerell, 1911 bifasciata bifasciata
9 Nomada esana Tsuneki, 1973 ruficornis ruficornis
10 Nomada fervens Smith, 1873 ruficornis ruficornis
11 Nomada flavoguttata (Kirby, 1802) ruficornis ruficornis
12 Nomada fulvicornis jezoensis Matsumura, 1912 ruficornis ruficornis
13 Nomada fusca Schwarz, 1986 ruficornis ruficornis
14 Nomada galloisi Yasumatsu & Hirashima, 1953 roberjeotiana roberjeotiana
15 Nomada ginran Tsuneki, 1973 armata armata
16 Nomada guttulata Schenck, 1861 ruficornis ruficornis
17 Nomada hakonensis Cockerell, 1911 ruficornis ruficornis
18 Nomada hakusana hakusana Tsuneki, 1973 roberjeotiana roberjeotiana
19 Nomada harimensis Cockerell, 1914 ruficornis ruficornis
20 Nomada icazti Tsuneki, 1976 ruficornis ruficornis
21 Nomada japonica Smith, 1873 basalis basalis
22 Nomada kaguya Hirashima, 1953 ruficornis ruficornis
23 Nomada koreana Cockerell, 1926 ruficornis ruficornis
24 Nomada lathburiana (Kirby, 1802) ruficornis ruficornis
25 Nomada leucophthalma (Kirby, 1802) ruficornis ruficornis
26 Nomada maculifrons Smith, 1869 ruficornis ruficornis
27 Nomada montverna Tsuneki, 1973 ruficornis ruficornis
28 Nomada nipponica Yasumatsu & Hirashima, 1951 trispinosa armata
29 Nomada okamotonis Matsumura, 1912 roberjeotiana roberjeotiana
30 Nomada okubira Tsuneki, 1973 furva furva
31 Nomada opaca Alfken, 1913 ruficornis ruficornis
32 Nomada pacifica Tsuneki, 1973 ruficornis ruficornis
33 Nomada panzeri orientis Tsuneki, 1973 ruficornis ruficornis
34 Nomada pekingensis Tsuneki, 1986 trispinosa trispinosa
35 Nomada pulawskii Tsuneki, 1973 furva furva
36 Nomada pyrifera Cockerell, 1918 ruficornis ruficornis
37 Nomada roberjeotiana aino Tsuneki, 1973 roberjeotiana roberjeotiana
38 Nomada sabaensis Tsuneki, 1973 ruficornis ruficornis
39 Nomada sexfasciata Panzer, 1799 superba superba
40 Nomada shirakii Yasumatsu & Hirashima, 1951 ruficornis ruficornis
41 Nomada shoyozana Tsuneki, 1986 roberjeotiana roberjeotiana
42 Nomada striata Fabricius, 1793 ruficornis ruficornis
43 Nomada taicho Tsuneki, 1973 furva armata
44 Nomada temmasana temmasana Tsuneki, 1986 roberjeotiana roberjeotiana
45 Nomada tsunekiana Schwarz, 1999 ruficornis basalis

Acknowledgement

We extend our sincere thanks to Mr. Jan Smit, the Nomada taxonomist from the Netherlands, for his invaluable guidance and the west Palearctic specimens he provided. We also express our deep appreciation to Mr. Keiichi Otsui for contributing the valuable Japanese specimens. Lastly, we deeply thank to Michael Branstetter, Jeremy Jensen, and Jaeseok Oh for improving the manuscript with valuable comments and suggestions.

The study received assistance through various sources. Firstly, it was conducted with assistance from the R&D Program for Forest Science Technology (Project No. 2021362B10-2223-BD01), which was provided by the Korea Forest Service (Korea Forestry Promotion Institute). Additionally, this study was partially supported by the Korea National Arboretum (project no. KNA 1-2-44, 23-2). Moreover, this research received support from the Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Education (NRF2020R1I1A2069484). Lastly, this work was supported by a grant from the National Institute of Biological Resources (NIBR) funded by the Ministry of Environment (MOE) of the Republic of Korea (NIBR202307202).

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Supplementary materials

Supplementary material 1 

NCBI accession numbers

Kayun Lim, Seunghwan Lee

Data type: docx

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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Supplementary material 2 

Model selection for BI

Kayun Lim, Seunghwan Lee

Data type: docx

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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