http://orcid.org/0000-0001-8376-1857
Figures
Abstract
Melaphidina aphids (Rhus-gall aphids; Eriosomatinae: Fordini) comprise five genera from eastern Asia and one monotypic genus from eastern North America. Melaphidina are unique in feeding on plant species of Rhus subgenus Rhus (Anacardiaceae), on which they form galls during the summer. The phylogenetic relationships among some species of Melaphidina aphids remain controversial. In this study, we sought to resolve the backbone phylogeny of Melaphidina aphids by sampling 15 accessions representing all six genera, all species, and all subspecies except Meitanaphis microgallis using 20 gene regions: five nuclear genes as well as 13 protein-coding genes and two rRNA genes of the mitochondrial genome. Phylogenetic analyses included Bayesian and maximum likelihood methods. Independent analyses of nuclear and mitochondrial genes returned congruent topologies, and analyses of all gene regions combined showed well-supported relationships among Melaphidina species. In particular, these were: (1) Nurudea (excluding N. ibofushi) is sister to a clade composed of the five remaining genera; (2) the monotypic North American genus Melaphis is sister to a clade comprising the four remaining genera; and (3) (Schlechtendalia + N. ibofushi) is sister to the clade (Floraphis (Meitanaphis + Kaburagia). Our results support the transfer of Meitanaphis flavogallis to Kaburagia as an additional subspecies or species, and the recognition of Floraphis as a distinct genus. This study provides important molecular resources for subsequent evolutionary studies using more nuclear genes on the Melaphidina aphids and their close allies.
Citation: Ren Z, von Dohlen CD, Harris AJ, Dikow RB, Su X, Wen J (2019) Congruent phylogenetic relationships of Melaphidina aphids (Aphididae: Eriosomatinae: Fordini) according to nuclear and mitochondrial DNA data with taxonomic implications on generic limits. PLoS ONE 14(2): e0213181. https://doi.org/10.1371/journal.pone.0213181
Editor: Bi-Song Yue, Sichuan University, CHINA
Received: November 19, 2018; Accepted: February 16, 2019; Published: February 28, 2019
This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Data Availability: All relevant data are in the paper.
Funding: This work was financially supported by the National Natural Science Foundation of China (grant number 31870366, 31170359), the Key Laboratory of Medicinal Animal and Plant Resources of the Qinghai-Tibet Plateau in Qinghai Province (grant number 2017-ZJ-Y13), the National High Technology Research and Development “863” Program (grant number 2014AA021802), the Hundred-Talent Project in Shanxi Province, Shanxi Scholarship Council of China (grant number 2013-020), the Endowment Program of the Smithsonian Institution, and the Laboratory of Analytical Biology, the Small Grants Program and the Global Genome Initiative of the National Museum of Natural History. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Rhus-gall aphids (Melaphidina) feed on the developing shoots or leaves of sumac, namely, species of Rhus subgenus Rhus (Anacardiaceae), on which they induce galls. The galls are called wu-bei-zi in China and are important in traditional medicine, rubber production, and improving leather quality because of their rich tannin contents [1–3]. Rhus-gall aphids were formerly placed in the subtribe Melaphidina within the tribe Fordini by Heie [4], Blackman & Eastop [5], and Remaudière & Remaudière [6], but they were later raised to tribe Melaphidini by Zhang et al. [1] and Heie & Wegierek [7]. The most current classification synonymizes Melaphidini with Fordini, without additional subtribal recognition [8]. Nevertheless, the Melaphidina aphids form a well-supported clade within Fordini according to recent molecular phylogenetic analyses [9–10]. Melaphidina aphids traditionally comprised six genera: Floraphis, Kaburagia, Melaphis, Meitanaphis, Nurudea and Schlechtendalia [1,11], although some disagreements have arisen over whether Floraphis and Meitanaphis comprise genera distinct from Nurudea and Schlechtendalia, respectively [10,12] or not [8]. In this study, we follow the generic delimitation of Eastop & Hille Ris Lambers [11] and Zhang et al. [1] and refer to six genera of Melaphidina aphids for the convenience of discussion.
Melaphidina aphids exhibit a classical eastern Asian—eastern North American biogeographic disjunction, which is common among many groups of plants and animals [13–21]. Melaphidina has the greatest diversity in eastern Asia, while only one monotypic genus (Melaphis) is native to North America [1,11,22–23]. Melaphidina also have complex life cycles with cyclical parthenogenesis over multiple generations, which sequentially feed on sumac plants as primary hosts in summer and mosses as secondary hosts in winter [1–2,24]. The aphid-sumac-moss association is unique and represents a potential model for studying species interactions across kingdoms within the context of the biogeographic disjunction, which occurs similarly in both Melaphidina and their sumac hosts [9,12,25]. However, the utility of this system for biogeographic and co-evolutionary research has been incompletely realized due to limited by poorly resolved phylogenetic relationships within Melaphidina.
Prior studies on the phylogeny of Melaphidina have been largely constrained by limited sampling or have failed to find high support for relationships among the genera and species. Two prior studies focused on resolving phylogenetic relationships within the family Aphididae and the tribe Fordini, respectively, from the nuclear EF-1α gene [26] and EF-1α and mitochondrial COI gene [27]. These studies sampled only three of six genera of Melaphidina. Two additional studies focused on Melaphidina specifically, but showed low support for relationships among the genera [9,12]. Li et al. [10] investigated the monophyly of the subfamily Eriosomatinae, including nine Melaphidina species, and Bayesian inference supported Melaphidina monophyly and generic relationships, but MP and ML analyses were less supportive. Recently, Ren et al. [28] investigated the evolutionary relationships within Melaphidina using sequences of the complete mitochondrial genome, which revealed relatively strong support at many internal nodes but could not resolve the position of the North American Melaphis with high support across all analyses. Therefore, additional work on the phylogeny of Melaphidina using nuclear data is needed.
The primary objectives of this study were to (1) further test the phylogenetic relationships of all six genera of Melaphidina aphids using five nuclear genes combined with the 13 protein-coding genes and two rRNA genes of mitochondrial genomes; and (2) explore the taxonomic implications for Melaphidina aphids in light of the phylogenetic framework, especially concerning the generic limits. Our sampling of nuclear genes comprised Elongation factor 1 alpha (EF-1α), Histone H3 (H3), Wingless (WG), 18S ribosomal RNA (18S rRNA) and long—wavelength rhodopsin (LWO), which we obtained by genome skimming via low- to high-density shotgun sequencing of total genomic DNA [29].
Results
Altogether, the five nuclear genes and 15 mitochondrial genes represented 19,371 characters, of which 5,614 (29.0%) were polymorphic, and 3,709 (19.1%) were parsimony-informative (Table 1). Independently, the protein-coding genes of the mitochondrial genome had a concatenated length of 10,988 bp in length and the two ribosomal RNA genes comprised 2,081bp. The five nuclear genes had more variable sites than the mitochondrial genes, mainly distributed in the intron regions.
All the aphid specimens were alate viviparous females and we identified them according to the taxonomy of Zhang et al. [1]. All the samples were collected from China except for Melaphis rhois from United States of America and deposited at the School of Life Science, Shanxi University, China.
Independent analyses of each of the five nuclear genes yielded topologies with high support for clades, especially comprising species within the same genus, but the relationships among deep nodes had low support (e.g., ML bootstrap < 60%). Nevertheless, the analyses of five concatenated nuclear genes with indels coded as new characters resulted in the highly supported topologies that were the same as the mitochondrial BI and ML trees.
We concatenated the 15 mtDNA genes with the five nuclear datasets based on the results of an ILD test (P = 0.38 > 0.01). The concatenated dataset yielded ML and BI topologies that were congruent with topologies obtained from analyses of the 15 mtDNA genes and, independently, the concatenation of the five nuclear genes (Fig 1).
Numbers on the branches show the Bayesian posterior probabilities (PP, left) and bootstrap values from maximum likelihood (BS, right) analyses. Stars represent nodes with 1.00 PP and 100% BS.
The concatenated nuclear and mitochondrial dataset showed that the six genera of Melaphidina aphids composed five generally well-supported clades: Nurudea, Melaphis, Schlechtendalia, Floraphis, and Meitanaphis + Kaburagia. The topology supported Nurudea except N. ibofushi as sister to a clade of the remaining species with high support (ML-BS = 100%, BI-PP = 1.00), and the North American Melaphis was sister to a clade of Schlechtendalia + N. ibofushi, Floraphis, and Meitanaphis + Kaburagia (ML-BS = 99%, BI-PP = 1.00). Schlechtendalia + N. ibofushi was sister to the clade (Floraphis (Meitanaphis + Kaburagia)) with low support (BI-PP = 0.8 < 0.90, ML-BS = 75%). Kaburagia + Meitanaphis formed a clade with ML-BS = 93% and PP = 1.00 that was sister to Floraphis (BS = 95% for RAxML analysis, BI-PP = 1.00).
Discussion
The phylogenetic analyses of concatenated nuclear and mitochondrial data show well-resolved relationships among all species across the six Melaphidina genera: (1) Nurudea (excluding N. ibofushi) is sister to a clade composed of all other genera; (2) the monotypic North American genus Melaphis is sister to the clade comprising the other four genera; (3) the Schlechtendalia + N. ibofushi clade is sister to the clade of Floraphis (Meitanaphis + Kaburagia); (4) Kaburagia and Meitanaphis from eastern Asia comprise a clade that is sister to Floraphis; and (5) Meitanaphis is paraphyletic, with M. flavogallis sister to the clade of four subspecies of Kaburagia, and its type species, M. elongallis, is sister to the Meitanaphis flavogallis + Kaburagia clade.
The well-resolved phylogeny provides important insights into the generic limits of Melaphidina aphids. Our results strongly support recognizing Floraphis Tsai & Tang as a distinct genus [30]. Floraphis was synonymized with Nurudea Matsumura by Eastop & Hille Ris Lambers [11], and this treatment was accepted by Blackman & Eastop [22], Remaudière & Remaudière [6] and Favret [8]. However, Zhang et al. [1] maintained Floraphis as a separate genus on the basis of the numbers of antennal segments, presence or absence of stigma on the forewing, host plant preferences, and gall shapes. Previous molecular studies have also supported the recognition of Floraphis [9,12]. However, the phylogenetic position of Floraphis has not been well resolved. It was placed as sister to Melaphis with low support values (PP = 0.77, BS < 50% [12]; PP = 0.83 [9]). A recent analysis using 15 mitochondrial genes supported Floraphis as sister to the Kaburagia + Meitanaphis [28], as does our current phylogeny using five nuclear genes in addition to the mitochondrial data. Thus, the accumulating evidence is converging on a consensus of Floraphis as distinct from Nurudea and as sister to the Meitanaphis + Kaburagia clade.
Meitanaphis was erected by Tsai & Tang [30] with M. elongallis as type species. Tang [31] and Xiang [32] described two new species, M. flavogallis and M. microgallis, on Rhus punjabensis and R. potaninii, respectively. Past studies [12,28], as well as our current study, show that Meitanaphis is paraphyletic with its type species M. elongallis [30] as sister to a clade consisting of M. flavogallis and Kaburagia, and M. flavogallis sister to the clade of four Kaburagia subspecies. Yang et al. [33] noted that the antennal characters of M. elongallis are very distinct from other Melaphidina genera, whereas those of M. flavogallis are very similar to Kaburagia species. These authors suggested that Meitanaphis be revised and recommended that M. flavogallis be transferred to Kaburagia, thus rendering both Kaburagia and Meitanaphis monophyletic [33]. Our results also show Meitanaphis to be paraphyletic, with type species M. elongallis [30] sister to a clade consisting of M. flavogallis and Kaburagia, and with M. flavogallis sister to the clade of the four Kaburagia subspecies. Meitanaphis flavogallis could be transferred to Kaburagia as a new subspecies or as a species sister to the four Kaburagia subspecies. A comprehensive analysis of all diagnostic morphological characters, as well as sequence data, from wider population sampling of all Kaburagia and Meitanaphis subspecies/species is called for to resolve the taxonomy of Meitanaphis, as well as Kaburagia. Additionally, Meitanaphis has previously been considered as a synonym of Schlechtendalia [8,11]. However, this is clearly rejected by our results and prior studies, which show generic-level distances between Meitanaphis and Schlechtendalia and support them as distinct genera [10,12,28].
The monophyly of Kaburagia Takagi has been challenged recently by molecular data [12]. Kaburagia was erected based on commercial galls exported from China [34] and currently contains four subspecies sensu Zhang et al. [1]. The four subspecies are distinguished on the basis of minor differences in the number of wax glands on the dorsum, tarsal I chaetotaxy, number of setae on the cauda, host plants, and gall shapes. Yang et al. [12] sampled the four subspecies of Kaburagia and three species of Meitanaphis and found Kaburagia to be paraphyletic with respect to M. flavogallis and M. microgallis. In contrast, Zhang & Qiao [26] and Ren et al. [9] found that the four subspecies of Kaburagia were monophyletic, but both of these studies included only the type species, M. elongallis. Our present study grouped the four Kaburagia subspecies with high support as a clade, to which M. flavogallis formed a sister relationship. The status of M. microgallis needs to be tested with additional samples and data.
Prior molecular studies have also uncovered taxonomic problems in Nurudea Matsumura. Zhang et al. [1] proposed a taxonomic treatment of Nurudea comprising three species: N. ibofushi, N. shiraii and N. yanoniella. Two species, N. shiraii and N. yanoniella, were included in Yang et al. [12], who found that the species formed a monophyletic group that was sister to the remaining Melaphidina. Ren et al. [9] included all three species and found that Nurudea was paraphyletic: N. shiraii and N. yanoniella formed a clade, but N. ibofushi was sister to Schlechtendalia chinensis and genetically very similar to that species. However, Ren et al. [9] utilized only three mitochondrial genes (COI, COII and Cytb) and a single nuclear gene (EF-1α). Our current analyses, which add evidence from more genes, replicate the findings of previous studies showing Nurudea to be paraphyletic. N. ibofushi may be best transferred to Schlechtendalia, where it could be classified as a subspecies of S. chinensis or a species very closely related to it [9,28]. However, further studies are needed to test the monophyly of Nurudea with broad sampling in both China and Japan before any formal taxonomic revision is made for the genus.
As currently classified, the monophyly of Schlechtendalia Lichtenstein is confirmed by molecular evidence. Bell [35] was first to describe aphid species forming galls on sumac leaves in China as Aphis chinensis. Lichtenstein [36] established the genus Schlechtendalia and transferred Aphis chinensis to it. The North American species, Melaphis rhois, was originally considered to represent a western population of S. chinensis. Subsequently, M. rhois experienced complicated nomenclatural turnover and was given names including Pemphigus sinensis Walker, Byrsocrypta rhois Fitch, and Melaphis chinensis Baker. Eastop & Hille Ris Lambers [11] treated Melaphis and Schlechtendalia as different genera, with species from China and North America assigned to S. chinensis and M. rhois, respectively. More recently, the circumscription of Melaphis and Schlechtendalia as independent genera has been supported by morphological and molecular evidence [1,9,12,28]. Our present study strongly supports recognition of Melaphis rhois and Schlechtendalia as distinct genera that are distantly related. The North American Melaphis rhois is sister to a clade comprising Schlechtendalia, Floraphis, and Meitanaphis + Kaburagia.
Here, we present a well-resolved phylogeny showing relationships among the genera of Melaphidina aphids. However, more extensive taxon sampling at the population, subspecies, and species levels, and incorporation of both morphological and ecological characters as well as additional molecular data are necessary to construct a thorough taxonomic revision of the group. With additional new data, we should be able to test among alternative hypotheses of relationships and revise the taxonomy of Melaphidina with greater certainty.
Materials and methods
Ethics statement
All the samples of Melaphidina aphids employed in this study were collected from the sumac galls that are not endangered, and these trees grow in public field where no permission for collection of leaves is needed.
Taxon sampling and DNA sequences
We collected live samples of species of Melaphidina aphids from mature, fresh sumac galls in the field (Table 1). From the galls, we extracted multiple individual aphids, which were genetically identical due to parthenogenetic development. We stored some of the collected individuals in 75% ethanol for taxonomic identification using microscopy and others in 100% ethanol for DNA extraction. We sampled from 15 accessions, which represented eleven species, including four subspecies, and all six genera of the Melaphidina aphids. We also sampled the closely related aphids, Baizongia pistaciae, from the tribe Fordini as an outgroup [26–27,37–39]. We deposited the voucher specimens at the School of Life Science of Shanxi University in China.
We extracted genomic DNAs using five individuals from the same gall with the DNeasy extraction kits (QIAGEN, Valencia, CA). We sent the DNAs to the Genomic Sequencing and Analysis Facility (GSAF), University of Texas, Austin for library construction and sequencing. Paired-end reads of 2x150 bp were generated on an Illumina NextSeq 500 platform with an insert size of 400 bp. We utilized the shotgun reads from genome skimming to obtain the five nuclear markers, 18S, EF-1α, H3, WG, and LWO by first mapping the reads to alignments of available sequences on GenBank and then performing de novo assemblies of reads in SPAdes [40]. We submitted the newly generated sequences of the nuclear markers to GenBank (Table 1). The accession numbers of the complete mitochondrial genome, from which the sequences of the 13 mitochondrial protein-coding genes and two rRNA genes were available, are also shown in Table 1.
Phylogenetic analysis
We performed phylogenetic analyses using five nuclear genes and 15 mitochondrial genes with separate and concatenated sequences. We aligned sequences using MAFFT v7.017 [41–42] implemented in Geneious 10 with default settings (http://www.geneious.com) [43], which allow for auto-selection among MAFFT algorithms for alignment based on data size. After alignment, we omitted highly variable regions within introns of nuclear genes before further analyses.
The protein-coding genes of the mitochondrial genome in species of Melaphidina are conserved in length with only a few gaps. Therefore, we coded indels only for the two mitochondrial rRNA genes and nuclear genes. We coded the indels as binary characters using the simple coding method of Simmons and Ochoterena [44] in SeqState [45]. We employed Sequence Matrix v1.8 [46] to combine the DNA data and binary characters.
For model-based analyses (see below), we set models of evolution according to results from jModelTest v.2.1.7 [47–48]. JModelTest resolved the best-fit models under the corrected Akaike Information Criterion (AICc), and we selected the highest-scoring models implemented in MrBayes: GTR + I + G model for COI, COII, COIII, ATP6, ND1, ND2, ND4, ND5, Cytb, WG, LWO and 16S rRNA genes; GTR + G model for ATP8, 12S rRNA, 18S, H3 and EF-1α; GTR + I model for ND3, ND4L and ND6 genes. We performed Bayesian phylogenetic analyses (BI) in MrBayes v.3.2.5 [49–50] for all individual genes, the combined nuclear genes, and the combined mitochondrial genes. We concatenated the mitochondrial genes because they are maternally inherited and represent a non-recombining locus. We also concatenated all the mitochondrial and nuclear genes based on the outcome of an incongruence length difference (ILD) test [51] in PAUP* [52]. For Bayesian analyses of individual genes, we treated binary indel codes as a separate partition, and performed two independent, simultaneous runs of the Markov Chain Monte Carlo (MCMC) for 10,000,000 generations starting from different random trees. We applied three hot and one cold chains for each run and sampled the cold chain every 1000 generations. We removed a burn-in of 2,500 trees, or 25%, and used the remaining trees to construct 50% majority-rule consensus trees to show posterior probabilities (PP) of clades; 50% majority-rules trees were visualized in FigTree v1.4.2 (http://tree.bio.ed.ac.uk/software/figtree/). We analyzed the concatenated dataset in MrBayes with partitions for each gene and for the binary indel codes. We applied unlinked model parameters to each partition. The model for the coded binary partitions was a default Standard Discrete Model in MrBayes [50].
We also conducted the maximum likelihood (ML) analyses using RAxML v.8.2 [53] with the same data partitioning as in the BI analysis. We selected the GTR continuous gamma model and performed bootstrapping with a random-number seed and 1000 replicates [54–55].
References
- 1.
Zhang GX, Qiao GX, Zhong TS, Zhang WY. Fauna Sinica Insecta, vol.14, Homoptera: Mindaridae and Pemphigidae. Beijing: Science Press. 1999.
- 2. Li ZG, Yang WY, Xia DJ. Study on the Chinese gallnuts. Forest Res. 2003;16: 760–767.
- 3. Wool D. Galling aphids: specialization, biological complexity, and variation. Annu. Rev. Entomol. 2004; 49: 175–192. pmid:14651461.
- 4. Heie OE. The Aphidoidea of Fennoscandia and Denmark. I. Fauna. Entomol. Scand. 1980; 9: 1–236.
- 5.
Blackman RL, Eastop VF. Aphids on the world's crops: an identification guide. Chichester: John Wiley & Sons. 1984.
- 6.
Remaudière G, Remaudière M. Catalogue of the world’s Aphididae (Homoptera Aphidoidea). Paris: INRA. 1997.
- 7. Heie OE, Wegierek P. Diagnoses of the higher taxa of Aphidomorpha (Hemiptera Sternorrhyncha). Redia. 2009; 92: 261–269.
- 8.
Favret C. Aphid species file. Version 5.0/5.0. 2018. [retrieval date on June 5th, 2018].
- 9. Ren ZM, Zhong Y, Kurosu U, Aoki S, Ma EB, von Dohlen CD, et al. Historical biogeography of eastern Asian—eastern North American disjunct Melaphidina aphids (Hemiptera: Aphididae: Eriosomatinae) on Rhus hosts (Anacardiaceae). Mol. Phylogenet. Evol. 2013; 69: 1146–1158. pmid:23973894
- 10. Li XY, Jiang LY, Qiao GX. Is the subfamily Eriosomatinae (Hemiptera: Aphididae) monophyletic? Turk. J. Zool. 2014; 38: 285–297.
- 11.
Eastop VF, Hille Ris Lambers D. Survey of the World’s Aphids. Junk W, The Hague, Netherlands. 1976.
- 12. Yang ZX, Chen XM, Havill NP, Feng Y, Chen H. Phylogeny of Rhus gall aphids (Hemiptera: Pemphigidae) based on combined molecular analysis of nuclear EF-1α and mitochondrial COII genes. Entomological Science. 2010; 13: 351–357.
- 13. Li H. Floristic relationships between eastern Asia an eastern North America. Transactions of the American Philosophical Society (Philadelphia). 1952; 42(2): 371–429.
- 14. Nordlander G, Liu Z, Ronquist F. Phylogeny and historical biogeography of the cynipoid wasp family Ibaliidae (Hymenoptera). Syst. Entomol. 1996; 21(2):151–166.
- 15. Wen J. Evolution of the eastern Asian and eastern North American disjunct distribution in flowering plants. Annu. Rev. Ecol. Syst. 1999; 30: 421–455.
- 16. Xiang QY, Soltis DE, Soltis PS, Manchester SR, Crawford DJ. Timing the eastern Asian-eastern North American floristic disjunction: molecular clock corroborates paleontological estimates. Mol. Phylogenet. Evol. 2000; 15(3): 462–472. pmid:10860654.
- 17. Xiang JY, Wen J, Peng H. Evolution of the eastern Asian—North American biogeographic disjunctions in ferns and lycophytes. J. Syst. Evol. 2015; 53(1): 2–32.
- 18. von Dohlen CD, Kurosu U, Aokic S. Phylogenetics and evolution of the eastern Asian-eastern North American disjunct aphid tribe, Hormaphidini (Hemiptera: Aphididae). Mol. Phylogenet. Evol. 2002; 23(2): 257–267. pmid:12069555.
- 19. Peña C, Nylin S, Wahlberg N. Biogeographic history of the butterfly subtribe Euptychiina (Lepidoptera, Nymphalidae, Satyrinae). Zool. Scr. 2010; 39(3): 243–258.
- 20.
Wen J, Ickert-Bond S, Nie ZL, Li R. Timing and modes of evolution of eastern Asian—North American biogeographic disjunctions in seed plants. In Long M, Gu H, Zhou Z. (Eds), Darwin's heritage today—Proceedings of the Darwin 200 Beijing International Conference. Beijing: Higher Education Press. 2010; 252–269.
- 21. Wen J, Nie ZL, Ickert-Bond SM. Intercontinental disjunctions between eastern Asia and western North America in vascular plants highlight the biogeographic importance of the Bering land bridge from late Cretaceous to Neogene. J. Syst. Evol. 2016; 54(5): 469–490.
- 22.
Blackman RL, Eastop VF. Aphids on the world’s trees: an identification and information guide. London: CAB International. 1994.
- 23.
Blackman RL, Eastop VF. Aphids on the world’s crops: an identification and information guide. 2nd ed. Chichester (UK): John Wiley & Sons. 2000.
- 24. Moran NA. A 48-million-year-old aphid-host plant association and complex life cycle: biogeographic evidence. Science. 1989; 245(4914): 173–175. pmid:17787877.
- 25. Yi T, Miller AJ, Wen J. Phylogenetic and biogeographic diversification of Rhus (Anacardiaceae) in the Northern Hemisphere. Mol. Phylogenet. Evol. 2004; 33(3): 861–879. pmid:15522809.
- 26. Zhang HC, Qiao GX. Molecular phylogeny of Pemphiginae (Hemiptera: Aphididae) inferred from nuclear gene EF-1α sequences. Bull. Entomol. Res. 2008; 98(5): 499–507. pmid:18826666.
- 27. Zhang HC, Qiao GX. Molecular phylogeny of Fordini (Hemiptera: Aphididae: Pemphiginae) inferred from nuclear gene EF-1α and mitochondrial gene COI. Bull. Entomol. Res. 2007; 97(4): 379–386. pmid:17645819.
- 28. Ren ZM, Harris AJ, Dikow RB, Ma EB, Zhong Y, Wen J. Another look at the phylogenetic relationships and intercontinental biogeography of eastern Asian-North American Rhus gall aphids (Hemiptera: Aphididae: Eriosomatinae): Evidence from mitogenome sequences via genome skimming. Mol. Phylogenet. Evol. 2017; 117: 102–110. pmid:28533083
- 29. Zhang N, Wen J, Zimmer EA. Congruent deep relationships in the grape family (Vitaceae) based on sequences of chloroplast genomes and mitochondrial genes via genome skimming. PLoS One. 2015; 11: e0152059. pmid:26656830.
- 30. Tsai PH, Tang C. The Classification of the Chinese gall aphids with description of three genera and six species from Meitan, Kweichow. The Transaction of the Royal Entomological Society of London. 1964; 97: 405–418.
- 31.
Tang C. The genus Meitanaphis and a new species from Chinese gallnut aphids. Research Report on Chinese Gallnuts. 1986; 1–39.
- 32. Xiang H. Studies of Chinese gall-nut aphids on Rhus potaninii Maxim. Entomotaxonomia. 1980; 2: 303–313.
- 33. Yang ZX, Chen XM, Feng Y, Chen H. Morphology of the antennal sensilla of Rhus gall aphids (Hemiptera: Aphidoidea: Pemphiginae): a comparative analysis of five genera. Zootaxa. 2009; 2204: 48–54.
- 34. Takagi G. Studies in the artificial multiplication of the sumac gall-aphid I. especially Schlechtendalia chinensis Bell. Bulletin of the Forest Experiment Station. 1937; 26: 22–23.
- 35. Bell J. Chinese galls. Pharm. J. 1851; 10: 128.
- 36. Lichtenstein H. Schlechtendalia. Stettiner Entomologische Zeitung 1883; 44: 240.
- 37. Ortiz-Rivas B, Martinez-Torres D. Combination of molecular data support the existence of three main lineages in the phylogeny of aphids (Hemiptera: Aphididae) and the basal position of the subfamily Lachninae. Mol. Phylogenet. Evol. 2010; 55(1): 305–317. pmid:20004730.
- 38. Nováková E, Hypšaa V, Kleinb J, Foottitc RG, von Dohlen CD, Moran NA. Reconstructing the phylogeny of aphids (Hemiptera: Aphididae) using DNA of the obligate symbiont Buchnera aphidicola. Mol. Phylogenet. Evol. 2013; 68(1): 42–54. pmid:23542003.
- 39. Wang Y, Huang XL, Qiao GX. The complete mitochondrial genome of Cervaphis quercus (Insecta: Hemiptera: Aphididae: Greenideinae). Insect Sci. 2014; 21(3): 278–290. pmid:24482299.
- 40. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 2012; 19(5): 455–477. pmid:22506599.
- 41. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002; 30(14): 3059–3066. pmid:12136088.
- 42. Katoh K, Kuma K, Toh H, Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 2005; 33(2): 511–518. pmid:15661851.
- 43. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012; 28(12): 1647–1649. pmid:22543367
- 44. Simmons MP, Ochoterena H. Gaps as characters in sequence-based phylogenetic analyses. Systematic Biol. 2000; 49(2): 369–381.
- 45. Müller K. SeqState—primer design and sequence statistics for phylogenetic DNA data sets. Applied Bioinformatics. 2005; 4(1): 65–69. pmid:16000015.
- 46. Vaidya G, Lohman DJ, Meier R. Sequence Matrix: concatenation software for the fast assembly of multigene datasets with character set and codon information. Cladistics. 2011; 27(2): 171–180.
- 47. Posada D. jModelTest: Phylogenetic model averaging. Mol. Biol. Evol. 2008; 25(7): 1253–1256. http://doi.org/10.1093/molbev/msn083. pmid:18397919.
- 48. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods. 2012; 9: 772. pmid:22847109.
- 49. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003; 19(12): 1572–1574. pmid:12912839.
- 50. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biol. 2012; 61(3): 539–542. pmid:22357727.
- 51. Farris JS, Källersjö M, Kluge AG, Bult C. Testing significance of incongruence. Cladistics. 1995; 10(3): 315–319.
- 52.
Swofford DL. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sunderland, Massachusetts: Sinauer Associates. 2002.
- 53. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014; 30(9): 1312–1313. pmid:24451623.
- 54. Felsenstein J. The number of evolutionary trees. Systematic Zool. 1978; 27(1): 27–33. http://doi.org/10.2307/2412810.
- 55. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985; 39(4): 783–791. pmid:28561359