13

Proc. Arthropod. Embryol. Soc. Jpn. 48, 13–18 (2017)Ⓒ 2017 Arthropodan Embryological Society of Japan
ISSN 1341–1527[REVIEW]

Molecular Phylogeny of Polyneoptera Based on the Mitochondrial
Genome and Focused on Phasmatodea*
Natuo KÔMOTO
Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, Owashi, Tsukuba, Ibaraki 305–8634,
Japan
E-mail: natuo@affrc.go.jp

1. Molecular phylogeny based on the mitochondrial
genomeTraditionally, insects have been classified based oncomparisons of morphological characters and estimations ofevolutionary trends. However, the use of morphological traits
may not be appropriate for the analysis of taxa with ancientradiation patterns which makes it difficult to identify theirsynapomorphies. Convergence can also be problematic andmay contribute to erroneous phylogenetic relationships.
Alternatively, the use of molecular phylogenetics can beadvantageous because the use of molecular data easily
produces a large number of unambiguous traits forcomparison.
Early molecular phylogenetic studies used a few genes,
such as ribosomal DNAs (rDNAs), to estimate phylogeny(Carmean et al., 1992; Kjer, 2004); conserved sequences andmultiple copies within the genome make it easy to clone
rDNAs. However, longer sequence data from increasing taxa
has been analyzed in more recent phylogenetic studies.
Mitochondrial DNA (mtDNA) has been used in various insect
phylogenetic studies (Nardi et al., 2003; Cook et al., 2005;
Kômoto et al., 2011, 2012; Tomita et al., 2011). Nucleotide
sequences of mtDNA longer than 10 kb can be obtained after
PCR-based cloning or random pyrosequencing relatively
easily because there are many mitochondria in the cytoplasm
and primers can be designed in conserved regions(Rasmussen and Noor, 2009; Nabholz et al., 2010). The
absence of recombination, introns, and paralogs helps toprecisely identify orthologous genes (Gissi et al., 2008).
Recently, phylogenomic approaches have been applied tovarious arthropods (Meusemann et al., 2010; Rota-Stabelli etal., 2011; Letsch et al., 2012). Sequencing technology isimproving rapidly, and extremely large data sets, such as
those in the genome or transcriptome, are becoming available
in various species. Ongoing genome projects, such as i5K and
1KITE, will usher in a new era of insect phylogenetic studies,but mitochondrial genome phylogenetics will still play animportant role, especially in detailed analyses of taxa notcovered by the genome projects.
2. Monophyly of Polyneoptera
Polyneoptera is a group of hemimetabolous insects that
includes 11 orders: Blattodea (cockroaches), Dermaptera(earwigs), Embioptera (webspinners), Grylloblattodea (icecrawlers), Isoptera (termites), Mantodea (praying mantises),
Mantophasmatodea (heelwalkers), Orthoptera (grasshoppers,
crickets, etc), Phasmatodea (stick and leaf insects), Plecoptera(stoneflies), and Zoraptera (angel insects). The phylogenetic
relationships of these orders and even the monophyly of
Polyneoptera have long been debated. Although the enlarged
anal fan of the hindwing is proposed as one of theautapomorphies of Polyneoptera, Embioptera and Zoraptera
do not have it, and Grylloblattodea and Mantophasmatodea
are apterous (Grimaldi and Engel, 2005). Ross (1955)
hypothesized that Zoraptera and Paraneoptera form amonophyletic clade while Plecoptera is sister to the clade
Paraneoptera + Holometabola. Kristensen (1975) reviewed
the preceding hypotheses and concluded that the monophylyof Polyneoptera was unclear. The unstable placement of thepolyneopteran orders in insect evolution is caused by deep
branching, which resulted in few synapomorphies and isassumed to date back to the late Paleozoic (Grimaldi andEngel, 2005). Recently, Yoshizawa (2011) showed that
Polyneoptera is monophyletic, based on a comparison of wingbase structures.
For phylogenetic analyses of taxa that share few
morphological traits because of deep branching or extreme
convergence, molecular phylogenies can help by providing
neutral traits. For example, the monophyly of Polyneoptera
has also been examined molecularly by many studies. Amongthe various genes applied to insect molecular phylogenetics,
ribosomal DNAs (rDNAs) were preferred in early studies
because conserved sequences among various species allow
easy cloning and sequence alignment. Many studies using* This article, which was accepted in 2013 and should have been published in 2014, was printed in 2017 being much delayed due to various circumstances.

14

N. KÔMOTO

rDNAs to analyze insect phylogeny determined that
Polyneoptera was paraphyletic, or at least failed to support
monophyly. For example, Kjer (2004) compared all polyneopteranorders, except Zoraptera and Mantophasmatodea, using 18S
rDNA, and the resulting tree neither supported nor rejected themonophyly of Polyneoptera, while Yoshizawa and Johnson (2005)
included Zoraptera and determined that Polyneoptera isparaphyletic. The phylogenetic tree made up of 18S rDNA,
however, showed that Zoraptera had an extraordinarily long
branch. Further, a study comparing all 11 polyneopteran orders
based on the 28S rDNA sequences also showed Polyneoptera to
be paraphyletic (Wang et al. 2013). In this tree, however,
Polyneoptera and Holometabola formed a clade, which isinconsistent with the general idea that Holometabola is closer toParaneoptera than to Polyneoptera.
Molecular phylogenies of insects have also been
determined using the mitochondrial genome. Carapelli et al.
(2007) used all 13 protein-coding genes of the mitochondrial
genome to reconstruct phylogenetic trees of Pancrustacea. In
these trees, Polyneoptera–including Blattodea, Grylloblattodea,
Mantodea, Mantophasmatodea, Orthoptera, Phasmatodea, andPlecoptera–was polyphyletic or paraphyletic. However, it ispossible that this does not reflect true evolutionary history
because Hexapoda and Crustacea are reciprocallyparaphyletic, perhaps affected by the high evolutionary rate of
the mitochondrial genome.
Recently, protein-coding nuclear genes have been used
in insect molecular phylogenetics. Ishiwata et al. (2011) used
three new nuclear genes (DPD1, RPB1, and RPB2), all ofwhich are relatively large, contain many variable sites, and do
not have paralogs. The authors reconstructed thephylogenetic trees of the three genes from all insect orders,
including the 11 polyneopteran orders, and found Polyneoptera
to be monophyletic. Sasaki et al. (2013) included Entognatha
and similarly concluded that Polyneoptera is monophyletic.
Sequencing methods are progressing rapidly andtranscriptome and/or genome data have become available forphylogenomic analysis. Simon et al. (2012) analyzed
transcriptomic data of insects, including Blattodea, Isoptera,
Orthoptera, Dermaptera, Plecoptera, and Zoraptera, andfound that these polyneopteran taxa form a monophyleticclade. To improve the robustness of molecular phylogenies,
studies must increase the number of taxa and/or the size ofdata sets, while avoiding rogue taxa, such as those with long
branches and paralogous genes.
3. Interordinal relationships of Polyneoptera
In addition to the debated monophyly of Polyneoptera,other phylogenetic relationships of polyneopteran orders
have been controversial because of a lack of appropriate
morphological characters, stemming from deep branching. To
overcome the constraint of morphological classification,
molecular phylogenetic approaches have been applied to theinterordinal phylogenies of Polyneoptera using nuclear genes(Whiting et al., 2003; Yoshizawa and Johnson, 2005; Ishiwata etal., 2011). The mitochondrial genome was also used toreconstruct the phylogenetic relationship of polyneopteranorders, except Zoraptera and Dermaptera (Tomita et al., 2011;
Kômoto et al., 2012). We recently added a partial sequence ofthe mitochondrial genome from these two orders to compare
the phylogenetic relationships of all 11 polyneopteran orders(Fig. 1 depicts preliminary data). Another way of performing
phylogenetic analysis, combining morphological charactersand molecular data, is termed ʻtotal evidence analysisʼ
(Wheeler et al., 2001; Terry and Whiting, 2005; Kjer et al.,2006). However, this method should be interpreted carefully
because the addition of morphological characters can bias theresulting trees, spoiling the significance of molecular data as
an alternative and neutral way.
Dictyoptera, consisting of the orders Isoptera, Blattodea,
and Mantodea, is one of the most robust monophyletic clades
within Polyneoptera, which is supported by various studies(Kristensen, 1981; Engel and Grimaldi, 2005). Molecularphylogenies of mitochondrial genome also support themonophyly of Dictyoptera (Tomita et al., 2011; Kômoto et al.,2012; Fig. 1), and show that Isoptera was included in Blattodea,
which became a paraphyletic group. The monophyly of
Dictyoptera has also been supported by 18S rDNA or three
nuclear genes (Yoshizawa and Johnson, 2005; Ishiwata et al.,2011). The paraphyly of Blattodea has also been determinedby a comprehensive analysis of Dictyoptera based on two
mitochondrial (12S rDNA and COII) and three nuclear genes(18S, rDNA, 28S rDNA and histone H3) (Inward et al., 2007).
A mitochondrial genome phylogeny shows a close
relationship between Phasmatodea and Embioptera, which
form a monophyletic clade; Eukinolabia was named by Terryand Whiting (2005) (Kômoto et al., 2012; Fig. 1). Note that theparaphyletic status of Phasmatodea will be discussed in thenext section. Many morphological studies do not support thisrelationship. For example, Crampton (1926) grouped
Phasmatodea with Dermaptera and Orthoptera, andEmbioptera with Plecoptera, based on the structure of thehead and its appendages. A close relationship between
Embioptera and Zoraptera was also proposed (Engel andGrimaldi, 2000; Yoshizawa, 2011). Recently, Bradler (2009)
performed a phylogenetic analysis using morphological traits
and proposed a sister group relationship between
Phasmatodea and Embioptera. Jintsu et al. (2010) came to thesame conclusion based on egg structure. Recent molecularanalyses of nuclear genes and those of transcriptome data
support the monophyly of Eukinolabia (Whiting et al., 2003;
Ishiwata et al., 2011; Letsch et al., 2012). Morphologicalcomparisons have often grouped Phasmatodea with
Orthoptera (Crampton, 1926; Engel and Grimaldi, 2000;
Yoshizawa, 2011), but according to a mitochondrial genome
phylogeny, these two orders diverged early in polyneopteranevolution (Kômoto et al., 2012; Fig. 1). The monophyly of
Orthoptera has been consistently supported by various
molecular phylogenetic analyses (Fenn et al., 2008; Ishiwata etal, 2011; Kômoto et al., 2012)

MOLECULAR PHYLOGENY OF POLYNEOPTERA

15

Fig. 1 A schematic diagram of a polyneopteran phylogeny based on partial mitochondrial genomic data.

When Mantophasmatodea was first described as a new
insect order, morphological analysis suggested that it was
related to Grylloblattodea and Phasmatodea (Klass et al.
2002). A mitochondrial genome phylogeny also shows that
Mantophasmatodea, Grylloblattodea and Eukinolabia(Phasmatodea + Embioptera) form a sister clade to
Dictyoptera (Kômoto et al., 2012; Fig. 1). The branching orderof Mantophasmatodea and Grylloblattodea, however, is notstable in molecular phylogenetics. Other mitochondrial
genome phylogenies also preferred this branching order(Cameron et al., 2006; Plazzi et al., 2011; Tomita et al., 2011),
but the application of three protein-coding nuclear genes led
to a monophyletic clade: Xenonomia, consisting of
Mantophasmatodea and Grylloblattodea (Ishiwata et al., 2011).
The monophyly of Xenonomia has not necessarily been
supported by molecular analyses: 18S rDNA comparisons
under the alignment with CLUSTAL did not support themonophyly of Xenonomia, while 28S rDNA data did (Terryand Whiting, 2005). To confirm the relationship between
Mantophasmatodea and Grylloblattodea, it will be necessary
to increase the number of taxa whose mitochondrial genome
is fully sequenced.
The positions of the orders Plecoptera, Dermaptera, andZoraptera are difficult to resolve in mitochondrial genome
phylogenies because they generally branch at the base of
Polyneoptera (Kômoto et al., 2012; Fig. 1). Without
Dermaptera and Zoraptera, mitochondrial genome
phylogenies placed Plecoptera in the position of sister toOrthoptera (Tomita et al., 2011; Kômoto et al., 2012). The
addition of a partial sequence of the mitochondrial genome ofZoraptera and Dermaptera changed the position of Plecoptera
and defined it as sister to Dictyoptera + Xenonomia +Eukinolabia, the branch opposite of Orthoptera (Fig. 1). Wan
et al. (2012) sequenced the full mitochondrial genome of adermapteran species and constructed phylogenetic trees
showing the sister relationship between Dermaptera andPlecoptera branching from other polyneopteran orders,
except Zoraptera which is absent in their trees. Our
preliminary data placed Zoraptera sister to the otherpolyneopteran orders, and showed trifurcate branching of
Dermaptera, Orthoptera and the others (Fig. 1). Ishiwata et al.
(2011) was not able to define the branching orders of
Plecoptera, Dermaptera, and Zoraptera in Polyneoptera, butmany morphological studies have placed Zoraptera close to
Embioptera (Engel and Grimaldi, 2000; Yoshizawa, 2011;
Mashimo et al., 2014). To elaborate on these molecularphylogenies using the mitochondrial genome, it is important
to increase the number of taxa, especially within Zoraptera
and Plecoptera.
4. Phasmatodea phylogeny
Phasmatodea is a polyneopteran order whose
synapomorphies are a short mesonotum, the first abdominal
segment that is fused with the metanotum, five tarsomeres,
two prothoracic exocrine glands, etc. (Zompro, 2004). Its
prominent adaptation for crypsis, e.g. resembling twigs orleaves, can easily result in morphological convergence, whichmakes it difficult to resolve intraordinal relationships.
The phylogenetic position of Timema is problematic in
Phasmatodea systematics. Timema has been thought of as aʻbasalʼ taxon of Phasmatodea because the first abdominal
segment is not fused with metanotum, the tarsomeres aretrimeric, and so on (Zompro, 2004). The egg structure ofTimema species indicates its close relationship with
Embioptera, supporting the idea that Embioptera andPhasmatodea form a monophyletic clade, Eukinolabia(Zompro, 2004; Jintsu et al., 2010). Molecular phylogenetic
analyses on nuclear genes have shown that Timema is sisterto the remaining phasmatodean taxa (Whiting et al., 2003). On
the other hand, our mitochondrial data showed that
Euphasmatodea and Embioptera form a sister clade toTimema, suggesting the paraphyly of Phasmatodea (Kômoto

16

N. KÔMOTO

Fig. 2 A schematic diagram of a phasmatodean phylogeny based on the full sequence of the mitochondrial genome. Modified from Tomita
et al. (2011).

et al., 2012; Fig. 1). However, the tree topology should beinterpreted carefully because of the long branch of Embioptera(Kômoto et al., 2012); long branches of some taxa can cause
distortion of the phylogenetic trees (Philippe et al., 2011). To
overcome long branch attraction (LBA), we attempted
different evolutionary models or increasing the number oftaxa, all resulting in a failure to avoid the long branch (data notshown). Phylogenomic approaches may help in theunderstanding of the branching order of these taxa. We tried a
preliminary analysis of Eukinolabia based on recently
available EST data of Timema, Phyllium, and Embioptera(Comeault et al., 2012; Letsch et al., 2012), and results showedthat Timema and Phyllium form a clade sister to Embioptera,consistent with the monophyly of Phasmatodea (data notshown).
Another issue to be re-evaluated is the intraordinalclassification of Phasmatodea. Phasmatodea has been divided
into two groups, Areolatae and Anareolatae, defined by thepresence and absence, respectively, of an impression on the
tip of the tibiae called the area apicalis (Brunner von
Wattenwyl and Redtenbacher, 1906–1908). Although this basic
classification has been accepted for many years (Bradley andGalil, 1977; Günther, 1953), the dichotomic classification has
been questioned recently. Cladistic analyses based onmorphological traits have suggested that both Areolatae andAnareolatae are polyphyletic (Tilgner, 2002; Bradler, 2009),
supported by our molecular phylogenetic studies based on the
mitochondrial genome (Kômoto et al., 2011; Tomita et al.,2011; Fig. 2). Phylogenetic analyses based on the nuclear
genes, 18S rDNA, 28S rDNA and histone H3, have also
concluded that the two groups are polyphyletic (Whiting et al.,2003). Another hypothesis is that area apicalis is a

pleisiomorphy that has been lost independently multiple
times throughout phasmatodean evolution, supported by thepresence of a similar impressed area in Embioptera and theegg morphology of Phasmatodea (Zompro, 2004). The area
apicalis, however, is not suitable for phasmatodean
classification.
Families and lower taxa in phasmatodean taxonomy havealso been challenged. Anareolatae is known to consist of two
families: Diapheromeridae and Phasmatidae, but the
subfamily Lonchodinae was proposed to be moved from
Diapheromeridae to Phasmatidae based on male genital
structures (Hennemann and Conle, 2008). Four of six families
and 9 of 19 subfamilies, including Lonchodinae, described by
Bradley and Galil (1977), were shown to be polyphyletic basedon comprehensive cladistic analyses of morphological andbehavioral traits (Bradler, 2009). The tree topology of
mitochondrial phylogenies also differs from conventional
systematics (Kômoto et al., 2011, 2012; Tomita et al., 2011; Fig.
2). For example, Diapheromeridae and Phasmatidae areparaphyletic and polyphyletic, respectively. Two genera
within Lonchodinae, Phraortes and Neohirasea, are separated
in distantly related branches. Neohirasea is sister to Micadina,which belongs to the paraphyletic subfamily Necrosciinae.
Ramulus is also a paraphyletic group, which forms amonophyletic clade with Entoria. Molecular phylogenetics
based on nuclear genes also contradicts conventionaltaxonomy, showing similar results to mitochondrial analyses(Whiting et al., 2003). For example, both Diapheromeridae andPhasmatidae are polyphyletic, and Neohirasea is sister to
Necrosciinae species. In the meantime, it is better to be
cautious when considering the surprising hypothesis thatwings were recovered independently several times from

17

MOLECULAR PHYLOGENY OF POLYNEOPTERA

apterous phasmatodean lineages (Whiting et al., 2003). It
should be noted that wing loss and recovery cannot beweighed equally in parsimonious analysis (Stone and French,
2003; Zompro, 2004). The direct optimization method, inwhich sequence alignment and tree searches are conductedsimultaneously, may also cause artificial alignment (Simmons,
2004; Ogden and Rosenberg, 2007; Yoshizawa, 2010).

suggest that hexapods and crustaceans are mutually paraphyletic.
Proceedings of the Royal Society B, 272, 1295–1304.
Crampton, G. C. (1926) The affinities of Grylloblatta indicated by astudy of the head and its appendages. Psyche, 33, 78–85.
Engel, M. S. and D. A. Grimaldi (2000) A winged Zorotypus in Mioceneamber from the Dominican Republic (Zoraptera: Zorotypidae),with discussion on relationships of and within the order. Acta
Geologica Hispanica, 35, 149–164.

5. Conclusion
This review has shown that the mitochondrial genome isa useful tool for determining polyneopteran phylogeny,
especially in intraordinal relationships. It should be applied
carefully, however, to ancient divergence such as theinterordinal phylogeny of Polyneoptera. In particular,
extremely different substitution rates or base compositions
can lead to misinterpretation of evolutionary history. The
position of Embioptera is expected to be verified based onother nuclear genes and phylogenomics with increased
number of taxa. The intraordinal systematics of Phasmatodea
need to be reexamined by molecular phylogenies. We will use
the mitochondrial genome of more phasmatodean species todetermine further important information which, united withmorphological classification, may resolve phasmatodean
evolution.

Fenn, J. D., H. Song, S. L. Cameron and M. F. Whiting (2008) A
preliminary mitochondrial genome phylogeny of Orthoptera(Insecta) and approaches to maximizing phylogenetic signal
found within mitochondrial genome data. Molecular Phylogenetics
and Evolution, 49, 59–68.
Gissi, C., F. Iannelli and G. Pesole (2008) Evolution of themitochondrial genome of Metazoa as exemplified by comparisonof congeneric species. Heredity, 101, 301–320.
Grimaldi, D. A. and M. S. Engel (2005) Evolution of the Insects.
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Günther, K. (1953) Über die taxonomische Gliederung und die
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Verbreitung

derInsektenordnungderPhasmatodea, Beiträge zur Entomologie, 3, 541–562.
Hennemann, F. H. and O. V. Conle (2008) Revision of oriental
phasmatodea: the tribe Pharnaciini Günther, 1953, including thedescription of the worldʼs longest insect, and a survey of thefamily Phasmatidae Gray, 1835 with keys to the subfamilies andAcknowledgments: I am grateful to Dr. Tomita for his
critical advice on this review. I also thank Prof. Machida, Dr.
Jintsu, and Mr. Mashimo for providing insect samples.

tribes (Phasmatodea: “Anareolatae”: Phasmatidae), Zootaxa,
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