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Article

Formica picea and F. candida (Hymenoptera: Formicidae): Synonyms or Two Species?

by
Zoya A. Zhigulskaya
1,
Sergei V. Shekhovtsov
1,2,*,
Tatiana V. Poluboyarova
2 and
Daniil I. Berman
1,*
1
Institute of the Biological Problems of the North FEB RAS, Magadan 685000, Russia
2
Institute of Cytology and Genetics SB RAS, Novosibirsk 630090, Russia
*
Authors to whom correspondence should be addressed.
Diversity 2022, 14(8), 613; https://doi.org/10.3390/d14080613
Submission received: 30 June 2022 / Revised: 19 July 2022 / Accepted: 26 July 2022 / Published: 29 July 2022
(This article belongs to the Special Issue Phylogeny and Phylogeography of the Holarctic)
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Abstract

:
Ants of the «Formica picea—F. candida» complex are widespread across Eurasia. However, it is still a matter of debate if it constitutes one or two species. In this study, we collected a sample of specimens from different parts of Eurasia, sequenced the mitochondrial cox1 and cytb genes, as well as three nuclear loci—wg, Top1, and ITS2—and analyzed the available published data. We found this complex to contain a new, yet undescribed, taxon that has a large distribution in Siberia and East Asia. Thus, the «Formica picea—F. candida» complex consists of at least three taxa with distinct distributions.

1. Introduction

The taxonomic position of many widespread and abundant ant species remains uncertain [1,2]. Among them are the species of the «black bog ant» complex, Formica picea Nylander, 1846 and F. candida Smith, 1878. Members of this complex are found from West Europe to Kamchatka, as well as from the valleys of northern rivers to Tibet (Figure 1).
Morphological variations within the complex were studied by Dlussky [11] based on extensive collections. Dlussky [11] concluded that there is no ground to split it into several species. Later on, Bolton [12] suggested that the name F. candida has the priority over F. picea; this was picked up by some—but not all—of the scientists. Seifert [13] suggested that F. picea and F. candida are two separate species, based on the features of pubescence and some morphometric parameters. According to Seifert [13], the distribution of F. picea includes Europe, the Caucasus, and the West Siberian Lowlands, and that of F. candida is in Central Asia, the Altai Mountains, and East Siberia. The habitats of F. picea include the bogs and European mountains above the forest belt, while F. candida lives in diverse habitats, including river floodplains and dry steppes of Asia.
However, Zakharov et al. [14] refuted Seifert’s [13] conclusion, stating that the variation of pubescence within the European populations of F. picea is higher than the proposed differences between the species. They also stated that there is a smooth gradient of morphological variation from Europe to the Far East. Based on this, the authors returned to treating F. picea and F. candida as synonyms.
Molecular genetic analysis is increasingly used to resolve problematic questions in ant taxonomy, due to its high resolution and its potential to detect cryptic taxa. [15] There were several molecular genetic attempts to resolve the relationships in the «F. picea—F. candida». Goropashnaya [3] performed a phylogenetic analysis based on the mitochondrial cytb gene. She demonstrated that the complex is split into two clades: one restricted to Europe and West Siberia and the other, to Central Asia. Later Goropashnaya et al. referred to these clades as a pair of species [5]. Antonov and Bukin [16] studied a sample of cytb sequences of specimens from several regions of the Palearctic identified as F. candida and F. picea. They concluded that genetic distances within F. candida are higher than those between the two species. Important datasets were also obtained by Chen et al. [7] and Schär et al. [4], based on the mitochondrial cox1 gene.
Therefore, the status of the «F. picea—F. candida» species complex remains uncertain. The problem with molecular data is that very similar sequences can be deposited under different species names depending on the authors’ viewpoint on this matter. Moreover, some authors sequenced the cytb gene, and the others sequenced cox1, so the resulting samples cannot be compared directly.
We collected a sample of the «F. picea—F. candida» complex specimens from the Northern Palearctic. Moreover, we studied the diversity, geographic and habitat distribution, and ecology of its population from the north of the Russian Far East [17]. The most important specimens were identified by Dlussky and Radchenko, who are specialists in the genus Formica; both consider this complex a single species (Radchenko: [18], personal communication). Here, we attempt to resolve the issue on the «F. picea—F. candida» complex using molecular analysis, based on the mitochondrial cox1 and cytb genes, as well as three nuclear loci, with the integration of the available GenBank sequences obtained by other authors.

2. Materials and Methods

We collected a set of Formica specimens from Eurasia (Figure 1, Table 1). DNA was isolated from single ethanol-fixed worker ants using the commercial silica columns (BioSilica, Novosibirsk, Russia), as described in [4]. A fragment of the mitochondrial cytochrome c oxidase subunit 1 (cox1) gene was amplified using the universal primers LCO1490m (5′-TACTC-AACAA-ATCAC-AAAGA-TATTG-G-3′; modified from [10]) and HCO2198 (5′-TAAAC-TTCAG-GGTGA-CCAAA-AAATC-A-3′; [19]). A part of the cytochrome b (cytb) was amplified using the primers Fcbl-F (5′-ACCCT-CACCT-GTAAA-TATTT-CTT-3′) and Fcbl-R (GGAAT-AGATC-GTAAA-ATTGC-AT-3′) designed in this study. PCR was performed using the Biomaster HS-Taq PCR Mix (Biolabmix, Novosibirsk, Russia).
Three nuclear loci were amplified using the primers designed in this study: a fragment of the wingless (wg) gene, with FWg-F (5′-CGTGG-TCGGC-GATAA-TCTA-3′) and FWg-R (5′-CACCA-CCACC-TCCTG-AGTCT-3′); topoisomerase 1 (Top1), with FTPO-F (5′-GAACC-ATTGC-CACCC-ATAGT-3′) and FTPO-R (5′-AGCGC-CAGCT-TGTCA- ATAAA-3′); the ribosomal internal transcribed spacer (ITS2), with FITS2-Fw (5′-TCATT-AACGT-TCCGG-AGGTC-3′) and FITS2-Rv (5′-TAAAA-TCGTT-GGCCC-TTACG-3′).
The obtained DNA fragments were visualized by agarose gel electrophoresis; unincorporated primers and nucleotide phosphates were removed using the shrimp alkaline phosphatase/E. coli exonuclease I mix (New England Biolabs, Ipswich, MA, USA). Sanger sequencing was performed on a 3130xl DNA Analyzer (Applied Biosystems, Framingham, MA, USA) in the SB RAS Genomics Core Facility (ICBFM SB RAS, Novosibirsk, Russia) using both forward and reverse primers. The obtained sequences were deposited in GenBank under accession numbers ON228270-ON228284, ON220872-ON220887, and ON862896-ON862909. Sequences obtained by other authors were also used in this study (see Table 1 for GenBank accessions). This dataset includes the cytb sequence for the F. candida neotype (AY786154).
Phylogenetic trees were constructed using the Maximum Likelihood (ML) algorithm and Bayesian Inference, as described in [20]. ML trees were built in RAxML v. 8.2.12 (A. Stamatikis, Hedelberg, Germany) [21], using the GTR + I + G model, as suggested by MrModeltest v.2.0 (J. Nylander, Uppsala, Sweden) [22]. Bayesian analysis was made in MrBayes v. 3.4 (F. Ronquist et al., Stockholm, Sweden) [23] as two simultaneous independent analyses from different random starting trees. There were 20 million generations performed; 25% of the generations were discarded as burn-in.

3. Results

We sequenced fragments of the mitochondrial cox1 and cytb loci for our sample (Table 1) and constructed phylogenetic trees. The final alignment for cox1 contained 593 bp; for cytb, 693 bp. On the cytb tree (Figure 2) the «F. picea—F. candida» complex was split into two big clades. Nucleotide distances between them were as large as those among other Formica species. One of the clades included the specimens from Kyrgyzstan, Europe, the Urals, the Caucasus, and Tibet. The sequences from Kyrgyzstan that included the F. candida neotype fell into a well-supported subclade. The rest of the specimens (shown on Figure 2 as F. picea) formed a group with no statistical support. This group included F. picea (including a specimen from southern Finland, the terra typica of F. picea), as well as those submitted to GenBank as F. candida. The second clade (shown on Figure 2 as Formica sp.) contained the specimens from West and East Siberia, the Russian Far East, China, and Korea. For cytb, the average p-distances between F. candida and F. picea were 1.34%; between F. picea and Formica sp., 3.25%; between F. candida and Formica sp., 3.35%. The mean p-distance within F. picea was 0.81%; within F. candida, 0.06%; within Formica sp., 1.05%.
The tree constructed using the cox1 gene (Figure 3) was built on more specimens than the cytb tree. However, there were no data for Kyrgyzstan, where the neotype of F. candida was described, or other regions of Central Asia, and there were few F. picea specimens. On the cox1 tree, the «F. picea—F. candida» complex was also found to contain two clades: one corresponding to F. picea (including terra typica, i.e., the region where the original type specimens were collected) and the other to Formica sp. The average p-distances between F. picea and Formica sp. were 2.52%; within the species, they were 0.57 and 0.38%, respectively. We should also note that the cox1 tree contained as many as three clades, with specimens identified as F. gagatoides.
The final alignment for the wg locus included 312 bp; for Tpo1, 717 bp; for ITS2, 678 bp. Sequences of wg and TPO of F. picea, Formica sp., and F. gagatoides were identical, except for some degenerate positions. In the ITS sequence, F. picea and Formica sp. could be distinguished by one A<>G substitution in position 216 of the alignment, while these two taxa differed from F. gagatoides by two substitutions and one short indel.

4. Discussion

In this study, we analyzed the dataset of the «F. picea—F. candida» complex in order to find out if F. picea and F. candida are synonyms or two distinct species. The results were unexpected. The sample, indeed, contained two clades: one with F. candida and F. picea specimens and the other representing a previously unknown taxon (Figure 2). For mitochondrial sequences, genetic distances between these clades were as high as between the well-established species of the genus Formica. This is in line with earlier findings that recovered multiple cryptic species within the genus Formica [24,25], as well as other well-studied genera, such as Pheidole [26,27], Myrmica [28,29], Lasius and Cardiocondyla [24], etc. For the nuclear sequences, however, the differences were not as high: wg and Tpo1 gene fragments were identical, and only one substitution distinguished F. picea from Formica sp. On the other hand, F. gagatoides was also very close to these taxa, differing from F. picea by two substitutions and one indel in ITS2, with two other genes being identical. It is well known that nuclear DNA has a lower substitution rate compared to the mitochondrial genome, and closely related ant species may have few distinctive positions or none at all. From the data obtained in [4], one can see that there are very few differences in the nuclear sequences of the whole F. picea/F. gagatoides/F. lemani/F. fusca/F. neorufarbis group. This is the usual situation that is found in ants, e.g., in the well-studied Formica rufa group, several species acknowledged by myrmecologists cannot be distinguished by nuclear markers and even show significant interspecific hybridization [30,31]. A similar case can also be observed in the genus Proformica [32]. Thus, we can conclude that the Asian Formica sp. is apparently distinct genetically from F. picea and F. candida, but it is unclear whether it should be regarded as a separate species or as a subspecies.
F. candida was initially described by Smith [33] based on a single specimen. This specimen was collected “On the road across the Pamir, from Sarikol to Panja”, which is probably somewhere near the easternmost part of China, on the border with Tajikistan. According to [13], this specimen was lost, so he fixed a neotype from Kyrgyzstan. This location is quite remote (about 315 km straight line distance in a mountainous area) from the original one. Our sample contained a cytb sequence of the neotype (AY786154). We can state that, so far, the F. candida clade is limited to the available specimens from Kyrgyzstan and was not found elsewhere.The type specimen of F. picea is old and highly damaged [13]. It was collected in the vicinity of Helsingfors (currently Helsinki, Finland) with no precise information on its whereabouts. Both locations available in our sample are several dozen km from Helsinki. Given the fact that no other group of the complex was found in Finland, we can suggest that these accessions represent the «real» F. picea.
Whether F. picea and F. candida are reciprocally monophyletic remains an open question. On our cytb tree F. picea was not supported as a clade (Figure 2), but more data are needed to verify that.
Based on the data on the type specimen origin, we cannot assign the Formica sp. clade to either F. picea or F. candida and have to conclude that it represents a new taxon that is still to be described. From the maps, we can see that all three ant taxa have distinct distributions: Formica sp. is found in Asian Russia, Siberia, and East Asia; F. candida, in Central Asia; F. picea, in Europe, with a single finding in Tibet. As suggested by multiple authors, morphological differences between these taxa are elusive [11,13,18]. There might be some differences in ecological preferences of these species: the European F. picea is found in swamps or in the alpine belt of mountains. The Asian Formica sp. is considered to be eurytopic in Siberia, while in the Russian Far East, it is found mostly in floodplains ([11] and our observations). However, it remains to be proved that these ecological differences coincide with the distribution boundaries of these species.

5. Conclusions

By trying to resolve the relationships within the «F. candida—F. picea» complex, in order to separate these two species, we found a new third member of this complex. It is important to note that genetic distances between F. candida and F. picea are significantly smaller than between them and the newly found taxon. The latter seems to not be the only cryptic taxon in this group: we obtained preliminary evidence that F. gagatoides might also represent as many as three cryptic taxa.

Author Contributions

Conceptualization, Z.A.Z. and D.I.B.; methodology, S.V.S. and T.V.P.; investigation, S.V.S. and T.V.P.; data curation, S.V.S.; writing—original draft preparation, D.I.B.; writing—review and editing, Z.A.Z. and S.V.S.; visualization, D.I.B. and S.V.S.; supervision, D.I.B.; project administration, D.I.B.; funding acquisition, D.I.B. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the State Budget Projects no. 1021060307698-5 (Faunogenesis and adaptive strategies of poikilothermic animals in extreme environments of the North) and no. FWNR-2022-0022.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The obtained sequences were deposited in GenBank under accession numbers ON228270-ON228284 (cytb) and ON220872-ON220887 (cox1).

Acknowledgments

We are grateful to N.A. Bulakhova, E.B. Fedoseeva, N.G. Gagarinova, T.V. Popkova, Yu. N. Sundukov, S.V. Chesnokova, Z.M. Yusupov and J. Sorvari for their help with specimen collection. Sanger sequencing was performed in SB RAS Genomics Core Facility (ICBFM SB RAS, Novosibirsk, Russia).

Conflicts of Interest

The authors declare no conflict of interest.

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Diversity 14 00613 g001 550
Figure 1. Specimens of the «F. picea—F. candida» complex used in this study. Red squares, F. picea; green diamonds, F. candida; blue circles, Formica sp. Specimen numbers refer to Table 1.
Figure 1. Specimens of the «F. picea—F. candida» complex used in this study. Red squares, F. picea; green diamonds, F. candida; blue circles, Formica sp. Specimen numbers refer to Table 1.
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Diversity 14 00613 g002 550
Figure 2. Phylogenetic tree constructed using cytb sequences. Numbers near branches indicate ML bootstrap support/Bayesian posterior probabilities. GenBank accessions given in parentheses; sequences obtained in this study are shown in bold.
Figure 2. Phylogenetic tree constructed using cytb sequences. Numbers near branches indicate ML bootstrap support/Bayesian posterior probabilities. GenBank accessions given in parentheses; sequences obtained in this study are shown in bold.
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Figure 3. Phylogenetic tree constructed using cox1 sequences. Numbers near branches indicate ML bootstrap support/Bayesian posterior probabilities. GenBank accessions given in parentheses; sequences obtained in this study are shown in bold.
Figure 3. Phylogenetic tree constructed using cox1 sequences. Numbers near branches indicate ML bootstrap support/Bayesian posterior probabilities. GenBank accessions given in parentheses; sequences obtained in this study are shown in bold.
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Table
Table 1. Specimens used in this study.
Table 1. Specimens used in this study.
LocationSpeciescox1cytb
Formica picea
1United Kingdom: Cors Goch National Nature Reserve, S. Wales-AY786145
(as F. candida) [3]
2Denmark: N55.83 E12.56LT977411 [4]-
3Sweden: Trajmossen, Brattforsheden-AY786144
(as F. candida) [3]
4Sweden: Varmland-JX170886 [5]
5Estonia: Torma-AY786147
(as F. candida) [3]
6Finland: Nylandia, Raasepori, Harpar StortraesketMZ607401 * [6]-
7Finland: Helsinki, Vihti-AY786146 *
(as F. candida) [3]
8Russia: Novgorod oblast-AY786148
(as F. candida) [3]
9Armenia: Aragaz mtn, N40.43203 E44.23642ON220876ON228281
10Russia: Moscow oblast, Odintsovo district, raised bog, moss tussock, N55.733 E36.850ON220886-87ON228278-79
11Russia: Moscow oblast, collected by G. Dlussky in 2000-AY786149
(as F. candida) [3]
12Russia: Nizhniy, Novgorod oblast, Kerzhenskiy Natural Reserve, Vishenskoye swamp, N56.467 E44.500ON220875ON228280
13Russia: Sverdlovsk oblast, Revda-AY786151
(as F. candida) [3]
14Russia: Sverdlovsk oblast, Yekaterinburg-AY786150
(as F. candida) [3]
15Russia: Perm oblast, 30 km SSW of Kachkanar-AY786152
(as F. candida) [3]
16China: Quinghai, Tibet-AY786157
(as F. candida) [3]
Formica candida
17Kyrgyzstan: Alai Valley-AY786154 **, AY786153 [3], JX170887 [5]
18Kyrgyzstan: Tian-Shan-AY786155-AY786156 [3]
Formica sp.
19Russia: Novosibirsk oblast, Iskitim district, Listvyanskiy town, N54.450 E83.483ON220885-
20Russia: Altai Republic, Ongudai town, N50.733 E86.133ON220880ON228273
21Russia: Buryatia Republic, Kizhinga town, N51.84639 E109.91278ON220883-84ON228270, ON228274
22Russia: Magadan oblast, 15 km from Yagodnoye town, bank of Sokhatina river, N62.517 E149.617ON220878ON228277
23Russia: Magadan oblast, 16 km from Yagodnoye town, bank of Detrin river, N62.750 E150.467ON220879ON228271
24Russia: Magadan oblast, Arman town, high floodplain, N59.667 E150.117ON220872ON228275
25Russia, Kamchatka oblast, N53.19 E158.48LT977377
(as F. candida) [4]		-
26Russia: Primorye krai, Lazo town, Lazovka river, N43.38056 E133.89778ON220881ON228276
27Russia: Primorye krai, Sinii Utes town, N43.06222 E131.35472ON220882ON228272
28China: Harbin, HelongJiangKX665031-32
(as F. candida) [7]		-
29China: Yanbian, JilinKX665026-27
(as F. candida) [7]		-
30South KoreaMT800217
(as F. candida) [8]		-
31Xilin Gol League, Inner MongoliaKX665022, KX665024 (as F. candida) [7]-
32Ulanqab, Inner MongoliaKX665023, KX665025 (as F. candida) [7]-
33Helan Mountains, Inner MongoliaKX665019-21
(as F. candida) [7]		-
34Qinglong, HebeiKX665028
(as F. candida) [7]		-
35China: HebeiHQ619704, HQ619710 (as F. candida) [9]HQ651081, HQ651074
(as F. candida) [9]
36Xiaowutai Mountain, HebeiKX665029-30
(as F. candida) [7]		-
37Zhong-Tiao Mountains, ShanxiKX665033
(as F. candida) [7]		-
38Liupan Mountains, NingxiaKX665034
(as F. candida) [7]
Outgroups
F. lemani Belarus: Vitebsk oblast, Braslav district, bank of Uklya lake, N55.60001 E27.333918ON220877ON228284
F. lemani Magadan, Arman town high river terrace, N59.867 E150.567ON220872ON228283
F. lemani China-HQ651082, HQ651086 [9]
F. lemani Magadan-JX170882 [10]
F. gagatoides China: Ningxia-HQ651073 [9]
F. gagatoides ChinaKX665069, KX665071, KX665072 [7], HQ619703-
F. gagatoides CanadaJN291934-
F. gagatoides NorwayLT977396, LT977398 [4]-
F. gagatoides Russia: Magadan oblast, Arman town, N59.667 E150.117ON220874ON228282
Locations refer to Figure 1. Sequences obtained in this study shown in bold; *, terra typica; **, type specimen. If an accession was deposited under another species name, this is acknowledged in parentheses; references to published articles are given whenever possible.
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MDPI and ACS Style

Zhigulskaya, Z.A.; Shekhovtsov, S.V.; Poluboyarova, T.V.; Berman, D.I. Formica picea and F. candida (Hymenoptera: Formicidae): Synonyms or Two Species? Diversity 2022, 14, 613. https://doi.org/10.3390/d14080613

AMA Style

Zhigulskaya ZA, Shekhovtsov SV, Poluboyarova TV, Berman DI. Formica picea and F. candida (Hymenoptera: Formicidae): Synonyms or Two Species? Diversity. 2022; 14(8):613. https://doi.org/10.3390/d14080613

Chicago/Turabian Style

Zhigulskaya, Zoya A., Sergei V. Shekhovtsov, Tatiana V. Poluboyarova, and Daniil I. Berman. 2022. "Formica picea and F. candida (Hymenoptera: Formicidae): Synonyms or Two Species?" Diversity 14, no. 8: 613. https://doi.org/10.3390/d14080613

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