ArticlePDF Available

Reanalysis of the phylogenetic relationships of the Pentatomomorpha (Hemiptera: Heteroptera) based on ribosomal, Hox and mitochondrial genes

Authors:

Abstract and Figures

Pentatomomorpha is one of the most biodiverse infraorders among the true bugs (Hemiptera: Heteroptera). Phylogenetic relationships among the superfamilies within this infraorder have been uncertain, especially for the Eutrichophora. The previous studies were based on morphological characters, or just mitochondrial or nuclear genes, or only partial 18S rDNA and COI. In this study, we used maximum likelihood (ML) and Bayesian inference (BI) based on massive molecular datasets (18S rDNA, 28S rDNA, Hox and mitochondrial genes totaling 21 loci and 12,538 characters) to infer a robust phylogeny for this terrestrial group. Results strongly support the monophyly of all superfamilies; the superfamily status of Aradoidea and the following relationships: (Aradoidea + (Pentatomoidea + (Coreoidea + (Lygaeoidea + Pyrrhocoroidea)))) in Pentatomomorpha, and (Coreoidea + (Lygaeoidea + Pyrrhocoroidea)) in Eutrichophora. Our results suggest that sampling greater numbers of genes is an effective tool for resolving phylogenetic problems.
Content may be subject to copyright.
Entomotaxonomia (2016) 38(2): 81–91, DOI: 10.11680/entomotax.2016021, ISSN 2095–8609 81
Reanalysis of the phylogenetic relationships of the
Pentatomomorpha (Hemiptera: Heteroptera) based on
ribosomal, Hox and mitochondrial genes
Min LI1,2,3, Yanhui WANG1, Qiang XIE1, Xiaoxuan TIAN1,4, Teng LI1, Hufang
ZHANG3, Wenjun BU1
1. College of Life Sciences, Nankai University, Tianjin 300071, China
2. Department of Biology, Taiyuan Normal University, Taiyuan, Shanxi 030031, China
3. College of Agriculture, Shanxi Agricultural University, Taigu, Shanxi 030801, China
4. Tianjin State Key Laboratory of Modern Chinese Medicine, Tianjin University of Traditional Chinese
Medicine, Tianjin 300193, China
Abstract: Pentatomomorpha is one of the most biodiverse infraorders among the true bugs (Hemiptera:
Heteroptera). Phylogenetic relationships among the superfamilies within this infraorder have been uncertain,
especially for the Eutrichophora. The previous studies were based on morphological characters, or just
mitochondrial or nuclear genes, or only partial 18S rDNA and COI. In this study, we used maximum likelihood
(ML) and Bayesian inference (BI) based on massive molecular datasets (18S rDNA, 28S rDNA, Hox and
mitochondrial genes totaling 21 loci and 12,538 characters) to infer a robust phylogeny for this terrestrial group.
Results strongly support the monophyly of all superfamilies; the superfamily status of Aradoidea and the
following relationships: (Aradoidea + (Pentatomoidea + (Coreoidea + (Lygaeoidea + Pyrrhocoroidea)))) in
Pentatomomorpha, and (Coreoidea + (Lygaeoidea + Pyrrhocoroidea)) in Eutrichophora. Our results suggest that
sampling greater numbers of genes is an effective tool for resolving phylogenetic problems.
Key words: taxonomy; Eutrichophora; molecular phylogenetics; molecular datasets
基于核糖体、Hox 和线粒体基因对蝽次目系统发育关系的重新分析(半翅目:异翅亚目)
李敏 1,2, 3,王艳会 1,谢强 1,田晓轩 1,4 ,李腾 1,张虎芳 3,卜文俊 1
1. 南开大学生命科学学院,天津 3000712. 太原师范学院生物系,山西 太原 0300313. 山西农业
大学农学院,山西 太谷 0308014. 天津中医药大学天津市现代中药重点实验室-省部共建国家重点实
验室(培育),天津 300193
摘要:蝽次目是蝽类昆虫(半翅目:异翅亚目)中物种多样性最为丰富的次目之一,其总科之间的系统
发育关系尚未确定,尤其对于真毛点类。以往对于蝽次目系统发育关系的研究基于形态数据,或仅基于
线粒体或核基因,或为 18S rDNA COI 基因片段。本研究选取了大量分子数据(18S rDNA28S
rDNAHox 和线粒体基因,共 21 个基因位点,12538 bp,利用最大似然法和贝叶斯方法推断蝽次目总
科间的系统发育关系。研究结果支持各总科的单系性,扁蝽总科的总科级地位,蝽次目各总科系统发育
关系(扁蝽总科 +(蝽总科 +(缘蝽总科 +(长蝽总科 + 红蝽总科))和真毛点类系统发育关系(缘
蝽总科 +(长蝽总科 + 红蝽总科)。研究表明选取多个基因作为分子标记为解决系统发育问题的有
Received 23 March 2016. Published 25 June 2016. Published online 21 June 2016.
Corresponding author, E-mail: wenjunbu@nankai.edu.cn
82 LI et al. Reanalysis of the phylogenetic relationships of Pentatomorpha
效途径。
关键词:分类;真毛点类;分子系统发育;分子数据集
Introduction
Pentatomomorpha (Hemiptera: Heteroptera) includes some of the largest terrestrial bugs.
This group causes economic damage to many species of crops because its members are chiefly
phytophagous (Schuh & Slater 1995). Pentatomomorphan bugs comprise more than 14,000
species (Weirauch & Schuh 2011). This large number of species has been variously grouped
into four (Schaefer 1964), five (Štys 1961; Schaefer 1993; Schuh & Slater 1995), six (Henry
1997), or seven (Schuh 1986; Henry & Froeschner 1988) superfamilies (Table 1) and 39
families (Schuh & Slater 1995; Henry 1997; Rider 2015). The superfamily Aradoidea was
raised to the infraorder Aradomorpha by Sweet (1996, 2006) based on morphological evidence,
together with ecological, fossil and biogeographical evidence, but this viewpoint was treated
as invalid in Cassis and Schuh (2010).
Table 1. Previous classification systems of Pentatomomorpha
Schaefer 1964 Štys 1961 Schaefer 1993
Schuh & Slater
1995
Schuh1986
Henry &
Froeschner 1988
Henry 1997
Aradoidea Aradoidea Aradoidea Aradoidea Aradoidea
Pentatomoidea Pentatomoidea Pentatomoidea Pentatomoidea Pentatomoidea
Coreoidea Coreoidea Coreoidea Coreoidea Coreoidea
Pyrrhocoroidea Pyrrhocoroidea Pyrrhocoroidea
Lygaeoidea Lygaeoidea Lygaeoidea
Piesmatoidea Piesmatoidea Piesmatoidea
Idiostoloidea Idiostoloidea Idiostoloidea
Phylogenetic relationships proposed previously at the superfamily level within
Pentatomomorpha are summarized in Fig. 1. The works of Henry (1997) (Fig. 1A) and Yao et
al. (2012) (Fig. 1E) were based on morphological characters. Li et al. (2005) (Fig. 1B)
analyzed the phylogeny of Pentatomomorpha using molecular sequence data (partial 18S
rDNA and COI mtDNA) for the first time, and supported the monophyly of Pentatomomorpha,
a sister-group relationship of Aradoidea and Trichophora, and a clade comprising Lygaeoidea,
Coreoidea, and Pyrrhocoroidea. Later, several other works based on molecular sequences were
published (Hua et al. 2008; Tian et al. 2011; Yuan et al. 2015). Of these, Hua et al. (2008 )
(Fig. 1C) and Yuan et al. (2015) (Fig. 1D) were both mitochondrial genome sequences-based
analyses, but reached different relationships for the Eutrichophora, a concept proposed in Xie
et al. (2005). In Tian et al. (2011) (Fig. 1D), 26 pentatomomorphan and four cimicomorphan
putative families and six Hox gene fragments were analyzed, and the relationship (Aradoidea
+ (Pentatomoidea + (Lygaeoidea + (Coreoidea + Pyrrhocoroidea)))) was supported.
Until now, the monophyly of Pentatomomorpha, and the close relationship between
Pentatomoidea and Eutrichophora have been generally accepted (Henry 1997; Xie et al. 2005;
Li et al. 2005; Hua et al. 2008; Tian et al. 2011; Yao et al. 2012; Yuan et al. 2015). The
phylogenetic relationships within the Pentatomomorpha, however, have not reached full
Entomotaxonomia (2016) 38(2): 81–93 83
agreement. The unsolved problems are: 1) the monophyly of the superfamilies (Xie et al. 2005;
Li et al. 2005); 2) whether Aradoidea should be treated as superfamily Aradoidea or infraorder
Aradomorpha (Sweet 1996, 2006); and 3) the phylogenetic relationships among the
superfamilies, especially in the Eutrichophora (Fig. 1).
Previous phylogenetic studies were mostly based on morphological characters, fossils or
several single source genes. Lack of a sufficient number of features, errors in accessing
homology among features of various organisms, and convergent evolutionary changes can
affect the accuracy of phylogenetic inference (Boore & Brown 1999). Multiple genes with
increased sequence lengths are favorable for accurate phylogenetic analyses (Wortley et al.
2005; Kawahara et al. 2011; Corl & Ellegren 2013). Sequences used to construct phylogenetic
trees of Pentatomomorpha were less than 1.5 kb (Li et al. 2005), or just from nuclear (Tian et
al. 2011) or mitochondria (Hua et al. 2008; Yuan et al. 2015). In this study, we took advantage
of nucleotide and genomic sequencing projects to assemble a data set of 21 genes and 37
species. Based on this data set, a preliminary phylogenetic framework of Pentatomomorpha is
proposed and the status of Aradoidea is analyzed.
Figure 1. Proposed phylogenetic hypotheses within the Pentatomomorpha. A. Henry (1997); B. Li et al.
(2005); C. Hua et al. (2008); D. Tian et al. (2011), Yuan et al. (2015); E. Yao et al. (2012).
Material and methods
Taxa sampling. Taxa were chosen to represent the major lineages according to the
classification of Schuh and Slater (1995), Henry (1997) and Rider (2015). The terminal taxa
were decided according to Campbell and Lapointe (2009). In total, 37 species were sampled,
of which 28 species were ingroups. Two gerromorphans, two nepomorphans, two
leptopodomorphans and three cimicomorphans were selected as successive outgroups (Table 2).
Gene sampling. A total of 15 fragments of Hox genes of Ptilomera tigrina Uhlen, 1860,
Microvelia douglasi Scott, 1874, Tingis ampliata (Herrich-Schaeffer, 1838) and Anthocoris
thibetanus Poppius, 1909 were initially sequenced in this study. All of the other Hox genes, all
84 LI et al. Reanalysis of the phylogenetic relationships of Pentatomorpha
18S rDNA and 28S rDNA sequences, and most mitochondrial genome genes were generated
by authors of the previously published studies (Hua et al. 2008; Tian et al. 2011; Li et al. 2012;
Wang et al. 2015) (Table 2).
Laboratory procedure and primers. The laboratory procedures were the same as those
described in Li et al. (2012). Our newly amplified five Hox gene exons are: the 5’ end of
abd-A, 3’end of Dfd, 5’ end of Dfd, 5’ end of Ubx and 3’ end of pb, with sequence lengths
ranging from 450 to 1,000 bp. Universal degenerate primers were used in this study. Some are
from Tian et al. (2011) and Li et al. (2012); some were newly designed as shown in Table 3.
Table 3. Universal degenerate primers used in this study
Upper primer (5’-3) Lower primer (5’-3)
5’ end of abd-A Tian et al. 2011
3’ end of Dfd
Tian et al. 2011
5’ end of Dfd
Tian et al. 2011
5’ end of Ubx
Li et al. 2012
3’ end of pb
Tian et al. 2011
3’ end of pb for
Gerromorpha
GTRAA RGTYT GGTTY CAAAA YCG TAGTA YTCSG GCGYR AAGTC GTT
5’ end of abd-A
for Gerromorpha
TACCANCCNCAAATGCTGCC
TGTCWGGCATWGGTTGKGAAG
Sequences of 18S rDNA, 28S rDNA, Hox and 13 protein coding genes of mitochondrial
genomes were aligned by Muscle, embedded within MEGA 6.06 (Tamura et al. 2013) under
the default conditions of the program. The alignments of 18S rDNA and 28S rDNA were
adjusted according to the secondary structure models of heteropteran 18S rRNA and 28S
rRNA (Xie et al. 2009; Wang et al. 2013), and length-variable regions of both genes were
eliminated before phylogenetic reconstructing (Wang et al. 2015). The six Hox genes were
also manually corrected according Tian et al. (2011). Finally, 18S rDNA (1937 bp)28S rDNA
(4163 bp), six Hox genes (2708 aa) and 13 mitochondrial protein coding genes (PCGs) (3730
aa) were selected as molecular markers. All of the four data sets (18S rDNA, 28S rDNA, Hox
and mt-genomes) were concatenated in DAMBE V5.3.48 (Xia 2013).
Phylogenetic analyses were conducted utilizing maximum likelihood (ML) and Bayesian
inference (BI). Best-fitting substitution models were selected by Modeltest 3.7 (Posada &
Crandall 1998) and Treefinder (Jobb 2011) for the nrDNAs and amino acids, respectively. ML
analyses were conducted using RAxML 8.0.12 in PThreads version (Stamatakis 2014). The
most appropriate substitution model was GTR+G+I for 18S rDNA and 28S rDNA, mtArt + G
+ I for ATP6, COI, COII, COIII and ND4L, mtZOA + G + I for ATP8, CYTB, ND1, ND2,
ND3, ND4, ND5, ND6 and 5’ end of Scr, Dayhoff + G + I for 5’ end of abd-A and 3’ end of
Dfd, JTT + G + I for 5’ end of Dfd and 5’ end of Ubx, MIX [Dayhoff, BLOSUM, JTT, LG,
PMB, VT, WAG, mtREV, mtMam, mtArt, mtZOA, cpREV, rtREV, betHIV, witHIV, FLU] + G
+ I for 3’ end of pb. The best ML tree was calculated by RAxML with 100 runs, followed by
2000 bootstrap replicates. The consensus tree was built based on the best ML tree and the
bootstrap tree.
Bayesian analyses were conducted using MrBayes 3.2.5 (Ronquist et al. 2012) on CPUs
with the gaps in the matrices treated as missing. The GTR substitution model for 18S rDNA
Entomotaxonomia (2016) 38(2): 81–93 85
and 28S rDNA, and the mixed substitution model for the amino acids were used under a
gamma distribution (+G) with a proportion of invariable sites (+I) to account for among-site
rate variation. Four chains were used and the datasets were run for 5,000,000 generations until
the average standard deviation of split frequencies between the two-parallel Markov chain
Monte Carlo runs dropped below 0.01. Trees were sampled every 1000th cycle, with a burn-in
of 25% of sampled trees.
Phylogenetic results
Two trees generated through two methods (ML and BI) recovered an identical topology
for the higher-level nodes (Figs. 2, 3). The monophyly of all superfamilies except Aradoidea of
Pentatomomorpha was supported. Aradoidea was the sister group of the remaining
pentatomomorphan taxa, and then Pentatomoidea came out. The relationships among
Eutrichophora were as follows: (Coreoidea + (Lygaeoidea + Pyrrhocoroidea)). The suggested
relationships among the nine outgroups and Pentatomomorpha in this paper were (Gerridae +
Veliidae + (Nepomorpha + (Leptopodomorpha + (Cimicomorpha + Pentatomomorpha)))).
Figure 2. ML phylogram inferred from the combined data. Bootstrap support values are indicated at each node
(> 50%).
Two trees generated through two methods (ML and BI) recovered an identical topology
for the higher-level nodes (Figs. 2, 3). The monophyly of all superfamilies except Aradoidea of
Pentatomomorpha was supported. Aradoidea was the sister group of the remaining
86 LI et al. Reanalysis of the phylogenetic relationships of Pentatomorpha
pentatomomorphan taxa, and then Pentatomoidea came out. The relationships among
Eutrichophora were as follows: (Coreoidea + (Lygaeoidea + Pyrrhocoroidea)). The suggested
relationships among the nine outgroups and Pentatomomorpha in this paper were (Gerridae +
Veliidae + (Nepomorpha + (Leptopodomorpha + (Cimicomorpha + Pentatomomorpha)))).
ML tree (Fig. 2). Branch support for the monophyly of all the superfamilies in
Trichophora was robust (BP = 100%), as well as for the basal branch, and clade (Coreoidea +
(Lygaeoidea + Pyrrhocoroidea)). The support indices of clades (Pentatomoidea + (Coreoidea +
(Lygaeoidea + Pyrrhocoroidea))) and (Lygaeoidea + Pyrrhocoroidea) were 91% and 55%,
respectively.
Figure 3. BI phylogram inferred from the combined data. Bayesian posterior probabilities values are indicated
at each node (> 50%).
BI tree (Fig. 3). Bayesian topologies were identical to those recovered in the ML tree (Fig.
2). The posterior probability values supporting the monophyly of all superfamilies and the
relationships among the superfamilies were all 100%. In addition, inter-family relationships
were also well-resolved.
Discussion
Pentatomomorpha is recognized as a monophyletic group by most researchers. Our
results were in accordance with this opinion with high support values in ML and Bayesian
trees.
The monophyly of Pentatomoidea and the sister relationship of Pentatomoidea and the
other Trichophora were strongly supported in both analyses (BP > 90%; PP = 1.00), views that
corroborate almost all of the recent studies (Henry 1997; Li et al. 2005; Hua et al. 2008; Yao et
al. 2012; Yuan et al., 2015). Although only one representative was chosen for Aradoidea, no
Entomotaxonomia (2016) 38(2): 81–93 87
one has questioned its monophyly up to now. So the monophyly of Aradoidea is also accepted
in this research.
The superfamily Aradoidea was raised to the infraorder Aradimorpha by Sweet (1996,
2006) based on morphological, ecological, fossil and biogeographical evidences. In the
mitochondrial genome analyses of Hua et al. (2008), they found a unique gene rearrangement
in Aradoidea as its autapomorphy. However, Aradoidea was consistently placed as an
independent branch of Pentatomomopha in our research. The sister relationship of Aradoidea
and Trichophora (Leston 1958; Henry 1997; Li et al. 2005; Hua et al. 2008; Yao et al. 2012;
Yu a n et al. 2015) was further confirmed in this research.
As for the monophyly and relationships of the other three superfamilies i.e. Coreoidea,
Lygaeoidea and Pyrrhocoroidea, there were different views: Henry (1997) gave the topology
((Coreoidea + Pyrrhocoroidea) + Lygaeoidea) based on morphological characters. Li et al.
(2005) recognized them as a paraphyletic group based on partial 18S rDNA and COI
sequences; Xie et al. (2005) performed a Bayesian analysis using 18S rDNA and reported the
hypothesis of (Pyrrhocoroidea + (Coreoidea + Lygaeoidea)); Hua et al. (2008) used mitochondrial
genomes as molecular markers and obtained the same results as Xie et al. (2005). Tian et al.
(2011) analyzed six Hox genes and found the same relationship as Henry (1997). Yao et al.
(2012) clarified that the remainder of the Trichophora (except for Pentatomoidea) should be
assigned to 5 superfamilies (Coreoidea, Pyrrhocoroidea, Idiostoloidea, Lygaeoidea, and
Piesmatoidea) based on a combination of fossil and extant morphological characters, but
didn’t give the relationships among them. Phylogenetic analyses based on mitogenomic data
of Yuan et al. (2015) supported a phylogenetic relationship of (Lygaeoidea + (Pyrrhocoroidea
+ Coreoidea)), the same result found by Henry (1997) and Tian et al. (2011).
In this study, the relationship ((Coreoidea + (Lygaeoidea + Pyrrhocoroidea)) was
demonstrated. The three superfamilies are united by four synapomorphies with high
consistency indices: presence of an m-chromosome, typically (ground plan) three trichobothria
on at least some of the abdominal segments, 3-lobed (or more) salivary glands, and loss of
dorsal abdominal scent gland in nymphs between tergites 3/4. Further, several studies have
suggested that the incomplete abdominal sutures found in some taxa (e.g., Physopeltinae
[Largidae] and some Pyrrhocoridae) link these bugs with the Rhyparochrominae in the
Lygaeoidea (Henry 1997).
For the relationship among outgroups, (Nepomorpha + (Leptopodomorpha +
(Cimicomorpha + Pentatomomorpha))) was supported and this is in congruence with results of
previous analyses of morphological data (Schuh 1979) and molecular data (Wang et al. 2015).
In this paper, we focused primarily on the higher taxa of Pentatomomorpha. Inclusion of
wider sampling to establish the relationships among lower taxa would be the expected next
step.
Acknowledgements
We thank anonymous referees for their useful comments and suggestions. This research
was supported by the National Natural Science Foundation of China (31372240, 31501840,
31440078), the Postdoctoral Science Foundation of China (134845) and the Taiyuan Normal
University Training Program of Innovation and Entrepreneurship for Undergraduates (CXCY1610).
88 LI et al. Reanalysis of the phylogenetic relationships of Pentatomorpha
References
Boore JL & Brown WM. 1999. Big trees from little genomes: mitochondrial gene order as a phylogenetic tool.
Current Opinion in Genetics & Development, 8(6): 668–674.
Campbell V & Lapointe FJ. 2009. The use and validity of composite taxa in phylogenetic analysis. Systematic
Biology, 58(6): 560–572.
Cassis G & Schuh RT. 2010. Systematic methods, fossils, and relationships within Heteroptera (Insecta).
Cladistics, 26(3): 262–280.
Corl A & Ellegren H. 2013. Sampling strategies for species of trees: the effects on phylogenetic inference of
the number of genes, number of individuals, and whether loci are mitochondrial, sex-linked, or autosomal.
Molecular Phylogenetics and Evolution, 67(2): 358–366.
Henry TJ & Froeschner RC. 1988. Catalog of the Heteroptera, or true bugs, of Canada and the Continental
United States. E. J. Brill, Leiden, the Netherlands, 958 pp.
Henry TJ. 1997. Phylogenetic analysis of family groups within the infraorder Pentatomomorpha (Hemiptera:
Heteroptera), with emphasis on the Lygaeoidea. Annals of the Entomological Society of America, 90(3):
275–301.
Hua J, Li M, Dong P, Cui Y, Qiang X & Bu WJ. 2008. Comparative and phylogenomic studies on the
mitochondrial genomes of Pentatomomorpha (Insecta: Hemiptera: Heteroptera). BMC Genomics, 9: 610.
doi:10.1186/1471-2164-9-610.
Jobb G. 2011. TREEFINDER version of March 2011. Munich, Germany. http://www.treefinder.de/ (Accessed
on 18 March 2011).
Kawahara AY, Ohshima I, Kawakita A, Regier JC, Mitter C, Cummings MP, Davis DR, Wagner DL, Prins JD
& Lopez-Vaamonde C. 2011. Increased gene sampling strengthens support for higher-level groups within
leaf-mining moths and relatives (Lepidoptera: Gracillariidae). BMC Evolutionary Biology, 11: 182.
doi:10.1186/1471-2148-11-182.
Leston D. 1958. Chromosome number and the systematics of Pentatomomorpha (Hemiptera). Proceedings of
the 10th International Congress Entomology, 2: 911–918.
Li HM, Deng RQ, Wang JW, Chen ZY, Jia FL & Wang XZ. 2005. A preliminary phylogeny of the
Pentatomomorpha (Hemiptera: Heteroptera) based on nuclear 18S rDNA and mitochondrial DNA
sequences. Molecular Phylogenetics and Evolution, 37(2): 313–326.
Li M, Wang J, Tian XX, Xie Qiang, Liu HX & Bu WJ. 2012. Phylogeny of the true water bugs
(Hemiptera-Heteroptera: Nepomorpha) based on four Hox genes. Entomotaxonomia, 34(1): 35–44.
Posada D & Crandall KA. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics, 14(9):
817–818.
Rider DA. 2015. Pentatomoidea home page. Available from: https://www.ndsu.edu/ndsu/rider/Pentatomoidea/.
(Accessed on 15 February 2016)
Ronquist F, Teslenko M, vander Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA &
Huelsenbeck JP. 2012. MrBayes3.2: efficient Bayesian phylogenetic inference and model choice across
a large model space. Systematic Biology, 61(3): 539–542.
Schaefer CW. 1964. The morphology and higher classification of the Coreoidea (Hemiptera-Heteroptera):
Parts I and II. Annals of the Entomological Society of America, 57: 670–684.
Schaefer CW. 1993. The Pentatomomorpha (Hemiptera: Heteroptera): an annotated outline of its systematic
history. European Journal of Entomology, 90: 105–122.
Schuh RT. 1979. Evolutionary trends in Heteroptera. Part II. Mouthpart-structures and feeding strategies, by R.
H. Cobben. Systematic Zoology, 28: 653–656.
Schuh RT. 1986. The influence of cladistics on heteropteran classification. Annual Review of Entomology,
Entomotaxonomia (2016) 38(2): 81–93 89
31(31): 67–93.
Schuh RT & Slater JA. 1995. True bugs of the world (Hemiptera: Heteroptera): classification and natural
history. Cornell University Press, Ithaca, United States, 336 pp.
Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.
Bioinformatics, 30: 1312–1313.
Štys P. 1961. Morphology of the abdomen and female ectodermal genitalia of the trichophorus Heteroptera
and bearing on their classification. Proceedings of the 11th International Congress of Entomology, 1:
37–43.
Sweet MH. 1996. Comparative external morphology of the pregenital abdomen of the Hemiptera. In: Schaefer CW
(Ed.), Studies on Hemiptera phylogeny. Lanham, Maryland, pp. 119–158.
Sweet MH. 2006. Justification for the Aradimorpha as an infraorder of the suborder Heteroptera (Hemiptera,
Prosorrhyncha) with special reference to the pregenital abdominal structure. Denisia, 19: 225–248.
Swofford DL. 2003. PAUP* 4 0b10: Phylogenetic Analysis Using Parsimony (*and other methods). Sinauer
Associates, Sunderland, Massachusetts.
Tamura K, Stecher G, Peterson D, Filipski A & Kumar S. 2013. MEGA6: molecular evolutionary genetics
analysis Version 6.0. Molecular Biology and Evolution, 30: 2725–2729.
Thompson JD, Higgins DG & Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive
multiple sequence alignment through sequence weighting, position-specific gap penalties and weight
matrix choice. Nucleic Acids Research, 22(22): 4673–4680.
Tian XX, Xie Q, Li M, Gao CQ, Cui Y, Xi L & Bu WJ. 2011. Phylogeny of pentatomomorphan bugs
(Hemiptera-Heteroptera: Pentatomomorpha) based on six Hox gene fragments. Zootaxa, 2888: 57–68.
Wang YH, Engel MS, Rafael JA, Dang K, Wu H, Wang Y, Xie Q & Bu WJ. 2013. A unique box in 28S rRNA
is shared by the enigmatic insect orders Zoraptera and Dictyoptera. PLoS ONE, 8(1): e53679.
doi:10.1371/journal.pone.0053679.
Wang YH, Cui Y, Rédei DA, Baňař P, Xie Q, Štys P, Damgaard J, Chen PP, Yi WB, Wang Y, Dang K, Li CR &
Bu WJ. 2015. Phylogenetic divergences of the true bugs (Insecta: Hemiptera: Heteroptera), with
emphasis on the aquatic lineages: the last piece of the aquatic insect jigsaw originated in the Late
Permian/Early Triassic. Cladistics, 4663(1): 404–407.
Weirauch C & Schuh RT. 2011. Systematics and evolution of Heteroptera: 25 years of progress. Annual
Review of Entomology, 56: 487–510.
Wortley AH, Rudall PJ, Harris DJ & Scotland RW. 2005. How much data are needed to resolve a difficult
phylogeny? Case study in Lamiales. Systematic Biology, 54(5): 697–709.
Xia X. 2013. DAMBE5: A comprehensive software package for data analysis in molecular biology and
evolution. Molecular Biology and Evolution, 30: 1720–1728.
Xie Q, Bu WJ & Zheng LY. 2005. The Bayesian phylogenetic analysis of the 18S rRNA sequences from the
main lineages of Trichophora (Insecta: Heteroptera: Pentatomomorpha). Molecular Phylogenetics and
Evolution, 34(2): 448–451.
Xie Q, Tian XX, Qin Y & Bu WJ. 2009. Phylogenetic comparison of local length plasticity of the small
subunit of nuclear rDNAs among all Hexapoda orders and the impact of hyper-length-variation on
alignment. Molecular Phylogenetics and Evolution, 50: 310–316.
Yao YZ, Ren D, Rider DA & Cai WZ. 2012. Phylogeny of the infraorder Pentatomomorpha based on fossil
and extant morphology, with description of a new fossil family from China. PLoS ONE, 7(5): e37289.
doi:10.1371/journal.pone.0037289.
Yuan ML, Zhang QL, Guo ZL, Wang J & Shen YY. 2015. The complete mitochondrial genome of Corizus
tetraspilus (Hemiptera: Rhopalidae) and phylogenetic analysis of Pentatomomorpha. PLoS ONE, 10(6):
e0129003. doi: 10.1371/journal.pone.0129003.
90 LI et al. Reanalysis of the phylogenetic relationships of Pentatomorpha
Table 2 Taxa and Genes Used in this Analysis
Infraorder-level Family-level Species Accession
number of
18SrDNA
Accession
number of
28SrDNA
Species
Gerromorpha Gerroidea:Gerridae
P
tilomera tigrina KJ461233 JF719825 Ptilomera tigrina
Gerromorpha Gerroidea:Veliidae Microvelia douglasi KJ461281 KJ461178 Entomovelia sp.
Nepomorpha Nepoidea:Nepidae Ranatra chinensis KJ461186 JF719824
L
accotrephes robustus
Nepomorpha Ochteroidea:Ochteridae Ochterus marginatus KJ461251 KJ461315 Ochterus marginatus
Leptopodomorpha Saldoidea:Saldidae Saldula saltatoria KJ461170 KJ461213 Saldula arsenjevi
Leptopodomorpha Leptopodoidea:Leptopodidae Valleriola buenoi KJ461310 KJ461290
L
eptopus sp.
Cimicomorpha Naboidea:Nabidae
A
lloeorhynchus sp. KJ461245 KJ461293
A
lloeorhynchus bakeri
Cimicomorpha Miroidea:Tingidae Corythucha ciliata KJ461201 KJ461175 Corythucha ciliata
Cimicomorpha Cimicoidea:Anthocoridae
A
nthocoris pilosus KJ461226 KJ461268 Orius niger
Pentatomomorpha Aradoidea:Aradidae Mezira sp. KJ461285 KJ461189
N
euroctenus parus
Pentatomomorpha Pyrrhocoroidea:Largidae
P
hysopelta gutta gutta KJ461164 KJ461255 Physopelta gutta
Pentatomomorpha Pyrrhocoroidea:Pyrrhocoridae
ysdercus cingulatus KJ461263 KJ461235
D
ysdercus cingulatus
Pentatomomorpha Pyrrhocoroidea:Pyrrhocoridae Macrocheraia grandis KJ461199 KJ461172
/
Pentatomomorpha Lygaeoidea:Lygaeidae
A
rocatus melanocephalus KJ461273 KJ461308 Kleidocerys resedae
Pentatomomorpha Lygaeoidea:Lygaeidae Sinorsillus piliferus KJ461269 KJ461194
Pentatomomorpha Lygaeoidea:Artheneidae
A
rtheneis intricata KJ461299 KJ461203
/
Pentatomomorpha Lygaeoidea:Blissidae Cavelerius excavatus KJ461294 KJ461237
/
Pentatomomorpha Lygaeoidea:Cymidae Cymus koreanus KJ461232 KJ461312
/
Pentatomomorpha Lygaeoidea:Geocoridae Geocoris ater KJ461218 KJ461309 Geocoris pallidipennis
Pentatomomorpha Lygaeoidea:Piesmatidae
P
iesma maculatum KJ461171 KJ461169
/
Pentatomomorpha Lygaeoidea:Rhyparochromidae
N
eolethaeus assamensis KJ461280 KJ461225
Pentatomomorpha Coreoidea:Rhopalidae Stictopleurus punctatonervosus KJ461217 KJ461286
/
Pentatomomorpha Coreoidea:Alydidae Megalotomus ornaticeps KJ461221 KJ461236 Stictopleurus subviridis
Pentatomomorpha Coreoidea:Alydidae Riptortus pedestris AB725684 AB725684
/
Pentatomomorpha Coreoidea:Coreidae Cletus punctiger KJ461173 KJ461219 Riptortus pedestris
Pentatomomorpha Coreoidea:Stenocephalidae
D
icranocephalus alticolus KJ461228 KJ461267 Hydaropsis longirostris
Pentatomomorpha Pentatomoidea:Tessaratomidae Eurostus validus KJ461181 JF719828
/
Pentatomomorpha Pentatomoidea:Pentatomidae Rhaphigaster nebulosa X89495 EU426880 Eusthenes cupreus
Pentatomomorpha Pentatomoidea:Pentatomidae Eurydema maracandica JX997807 JX997806 Halyomorpha halys
Pentatomomorpha Pentatomoidea:Acanthosomatidae Elasmucha laeviventris KJ461262 KJ461208 Eurydema gebleri
Pentatomomorpha Pentatomoidea:Scutelleridae Cantao ocellatus KJ461182 KJ461230
/
Pentatomomorpha Pentatomoidea:Cydnidae Fromundus pygmaeus KJ461296 KJ461209
/
Pentatomomorpha Pentatomoidea:Plataspidae Coptosoma bifarium KJ461259 KJ461239 Macroscytus gibbulus
Pentatomomorpha Pentatomoidea:Plataspidae
P
aracopta maculata KJ535895 KJ535890 Coptosoma bifaria
Pentatomomorpha Pentatomoidea:Urostylididae Urochela luteovaria KJ461205 KJ461306 Megacopta cribraria
Pentatomomorpha
Pentatomomorpha
Pentatomoidea:Urostylididae
Pentatomoidea:Urostylididae
Tessaromerus licenti
Urostylis chinai
KJ461291
KJ461275
KJ461300
KJ461287
Urochela quadrinotata
/
Entomotaxonomia (2016) 38(2): 81–93 91
Continued Table 2 on the right
Accession
number of Mt
genomes
Species Accession
number of
5'end abd-A
3'end Dfd 5'end Dfd 3'end pb 5'end Scr 5'end Ubx
KP400583 Ptilomera tigrina 0 0 0 0
/
/
KP400582 Microvelia douglasi 0
/
0 0
/
/
NC_012817 Ranatra chinensis JQ409392 JQ409405 JQ409432 JQ409445
/
JQ409419
NC_012820 Ochterus marginatus JQ409394 JQ409407 JQ409434 JQ409447
/
JQ409421
NC_012463 Saldula pallipes JQ409389 JQ409402 JQ409429 JQ409442
/
JQ409416
FJ456946 Valleriola sp. JQ409390 JQ409403 JQ409430 JQ409443
/
JQ409417
NC_016432 Gorpis annulatus FJ851727 FJ851754 FJ851784 FJ851810 FJ851840 FJ851870
KC756280 Tingis ampliata 0 0 0 0
/
0
EU427341
A
nthocoris thibetanus 0 0 0
/
FJ851839 FJ851868
NC_012459 Carventus hainanensis FJ851698 FJ851729 FJ851756 FJ851785 FJ851811 FJ851842
NC_012432 Physopelta quadriguttata FJ851712 FJ851739 FJ851769 FJ851798 FJ851825 FJ851856
NC_012421 Pyrrhopeplus posthumus FJ851711 FJ851738 FJ851768 FJ851797 FJ851824 FJ851855
/
/
/
/
/
/
/
/
KJ584365
L
ygaeus equestris FJ851700 FJ851731 FJ851758 FJ851787 FJ851813 FJ851844
Oncopeltus fasciatus FJ851728 FJ851755 / / FJ851841 FJ851871
/
A
rtheneis intricata FJ851705 FJ851734 FJ851762 FJ851792 FJ851818 FJ851849
/
D
imorphopterus spinolae FJ851703 FJ851733 FJ851760 FJ851790 FJ851816 FJ851847
/ Cymus koreanus FJ851701 / / FJ851788 FJ851814 FJ851845
NC_012424 Geocoris pallidipennis FJ851704 / FJ851761 FJ851791 FJ851817 FJ851848
/ Piesma josifovi FJ851710 FJ851737 FJ851767 / FJ851823 FJ851854
/
D
ieuches femoralis FJ851707 / FJ851764 FJ851794 FJ851820 FJ851851
NC_012888
A
eschyntelus chinensis FJ851715 FJ851742 FJ851772 FJ851801 FJ851828 FJ851859
/
/
/
/
/
/
/
/
NC_012462 Riptortus pedestris FJ851713 FJ851740 FJ851770 FJ851799 FJ851826 FJ851857
NC_012456
A
canthocoris scabe
r
FJ851714 FJ851741 FJ851771 FJ851800 FJ851827 FJ851858
/
/
/
/
/
/
/
/
NC_022449 Eurostus validus FJ851722 FJ851749 FJ851779 FJ851808 FJ851835 FJ851866
NC_013272
N
ezara viridula FJ851723 FJ851750 FJ851780 FJ851809 FJ851836 FJ851867
KP207595
/
/
/
/
/
/
/
/
A
canthosoma crassicauda FJ851717 FJ851744 FJ851774 FJ851803 FJ851830 FJ851861
/ Poecilocoris lewisi FJ851720 FJ851747 FJ851777 FJ851806 FJ851833 FJ851864
NC_012457
A
ethus indicus FJ851718 FJ851745 FJ851775 FJ851804 FJ851831 FJ851862
NC_012449
/
/
/
/
/
/
/
NC_015342 Megacopta cribraria FJ851719 FJ851746 FJ851776 FJ851805 FJ851832 FJ851863
JQ743678 Urochela distincta FJ851716 FJ851743 FJ851773 FJ851802 FJ851829 FJ851860
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
Note: Sequences marked with 0 were newly amplified in this research and the accession numbers will
be supplied after assigned by the GenBank staff.
... Coreoidea includes five extant families, Alydidae, Coreidae, Rhopalidae, Stenocephalidae, and Hyocephalidae (Schuh & Weirauch, 2020). The phylogeny of Coreoidea was investigated in several studies which most excluding Stenocephalidae and Hyocephalidae and multiple phylogenetic hypotheses was proposed for this group Henry, 1997;Hua et al., 2008;Li, 1996;Li et al., 2016;Liu et al., 2019;Tian et al., 2011;Weirauch et al., 2018;Zhao et al., 2018). The close relationship between Alydidae and Coreidae has been supported by several phylogenetic studies (e.g., Henry, 1997;Hua et al., 2008;Li et al., 2016;Xie et al.,2005;Yuan et al., 2015). ...
... The phylogeny of Coreoidea was investigated in several studies which most excluding Stenocephalidae and Hyocephalidae and multiple phylogenetic hypotheses was proposed for this group Henry, 1997;Hua et al., 2008;Li, 1996;Li et al., 2016;Liu et al., 2019;Tian et al., 2011;Weirauch et al., 2018;Zhao et al., 2018). The close relationship between Alydidae and Coreidae has been supported by several phylogenetic studies (e.g., Henry, 1997;Hua et al., 2008;Li et al., 2016;Xie et al.,2005;Yuan et al., 2015). Currently, Coreidae has four recognized subfamilies (Coreinae, Hydarinae, Meropachyinae and Pseudophloeinae) and Alydidae has two recognized subfamilies (Alydinae and Micrelytrinae) (Schuh & Weirauch, 2020). ...
... Considering the limited molecular data and taxa sample here, we also have to pay attention to other proposed hypothesis for the relationship. Stenocephalidae and Hyocephalidae, rather than Rhopalidae, were found to be more closely to Alydidae + Coreidae in some studies (e.g., Henry, 1997;Li et al., 2016;Weirauch et al., 2018). According to the cladistic analysis by Li, 1996, Pseudophloeinae and Hydarinae were formed sister group with sampled ingroup Rhopalidae + (Alydidae + Coreidae) in turn. ...
Article
Full-text available
Coreoidea (Insecta: Hemiptera: Heteroptera) is a widely distributed and agriculturally important bugs. However, the phylogeny of Coreoidea lacked consensus on higher-level relationships and several studies by comparative morphological characters and molecular data suggested the non-monophyly of two families: Coreidae and Alydidae. The mitochondrial genome (mitogenome) has long been thought to be a significant marker to understand phylogenetic relationships, but the mitogenome in Alydidae is scarce to date. In the present study, we gathered the mitogenomes of 28 species from four families of Coreoidea excluding Hyocephalidae (Alydidae, Coreidae, Rhopalidae, and Stenocephalidae), including four newly sequenced mitogenomes of Alydidae, and conducted mitogenomic organization and phylogenetic studies. We used maximum likelihood and Bayesian inference methods to infer the higher-level phylogeny from the perspective of mitogenomes, primarily to investigate the phylogenetic relationship betweeen Coreidae and Alydidae. We add evidence that neither Alydidae nor Coreidae are monophyletic based on mitogenomes. Newly sequenced mitogenomes of Alydidae have traditional gene structure and gene rearrangement was not found. Alydinae was always recovered as closely related to Pseudophloeinae of the coreid subfamily with high support. The placement of the coreid subfamily Hydarinae and alydid subfamily Micrelytrinae are unstable depending on approach used. In terms of the length and nucleotide composition of the protein coding genes in mitogenomes, Pseudophloeinae and Hydarinae of coreid were more similar to Alydidae. The unsettled classification issues of Coreidae and Alydidae by mitogenomes were demonstrated in this work, indicating that further study is needed.
... A series of phylogenetic analyses based on morphological and molecular data of Pentatomomorpha demonstrated broad agreement regarding the position of Aradoidea as the basal lineage of Pentatomomorpha, in other words, the sister group of Trichophora (Idiostoloidea þ Lygaeoidea þ Coreoidea þ Pyrrhocoroidea þ Pentatomoidea). Similarly, the sister group relationship of Pentatomoidea and Eutrichophora (Idiostoloidea þ Lygaeoidea þ Coreoidea þ Pyrrhocoroidea) was unequivocally recognized by a series of phylogenetic analysis (Henry, 1997;Li et al., 2005;Xie et al., 2005;Hua et al., 2008;Yao et al., 2012;Yuan et al., 2015;Li et al., 2016;Li et al., 2017;Liu et al., 2019;Weirauch et al., 2019). However, there are still some contrasting views about the phylogenetic relationships within Eutrichophora. ...
Article
A new genus Megaoptocoris gen. nov. and two new species of the fossil coreoid family Yuripopovinidae, Megaoptocoris punctatus sp. nov., and M. similis sp. nov. are described based on two well-preserved specimens from mid-Cretaceous Burmese amber from northern Myanmar. The new genus is similar to Yuripopovina Azar et al., 2011, the type genus of Yuripopovinidae, and also has unique morphological characters such as large eyes and parts of the pronotal margin laminate. The main diagnostic characters of Yuripopovinidae are discussed, and the emended diagnosis is proposed.
... The evaporatorium in Lygaeoidea is quite small, situated on the metapleuron and the posterior part of mesopleuron, but largely extended in Berytidae and Colobathristidae (Henry, 1997a,b). Unfortunately, polarisation of the characters is impossible at the moment due to highly conflicting phylogenetic hypotheses available for Lygaeoidea (Henry, 1997a;Li et al., 2005Li et al., , 2016Li et al., , 2017Tian et al., 2011;Yuan et al., 2015;Song et al., 2016;Johnson et al., 2018;Liu et al., 2018Liu et al., , 2019Zhao et al., 2018Zhao et al., , 2019Weirauch et al., 2019). ...
Article
Pyrrhocoroidea represents an important group of true bugs (Insecta: Hemiptera: Heteroptera) which includes fire bugs, cotton stainers and other taxa widely used in experimental studies or known as pests. However, the morphology and phylogeny of Pyrrhocoroidea have been only poorly studied so far. Here, structures of the external scent efferent system of the metathoracic scent glands are examined in 64 out of 71 currently valid genera of Pyrrhocoroidea and scanning electron micrographs are provided for most taxa. Several characters are revealed which define each of the three higher taxa within Pyrrhocoroidea: Larginae (small auriculate peritreme lacking manubrium and median furrow; metathoracic spiracle never surrounded by evaporatorium), Physopeltinae (large, widely open ostiole; large peritremal disc with manubrium [new term], lacking median furrow; mace-like mycoid filter processes of equal shape and size on both anterior and posterior margins of metathoracic spiracle), and Pyrrhocoridae (elongate auriculate peritreme with deep median furrow). Within Pyrrhocoridae, three main types (A, B and C) of the external scent efferent system are distinguished, differring in the amount of reductions. The findings are interpreted in the context of phylogenetic hypotheses available for Pyrrhocoroidea and their close relatives, Coreoidea and Lygaeoidea. An updated identification key to the families and subfamilies of Pyrrhocoroidea applicable for both sexes is provided.
... The fact remains that, in spite of their spermathecal differences, Coreidae and Alydidae are consistently united as sister taxa in various recent phylogenetic analyses mainly focused on pentatomomorphan lineages, regardless of whether they are based on morphological characters or molecular sequences (Henry 1997;Xie et al. 2005;Hua et al. 2008;Tian et al. 2011;Yao et al. 2012;Wang et al. 2016;Li et al. 2016;Li et al. 2017). However, in his cladistic analysis of the tribal rank taxa of Coreidae, Li (1997) found that the subfamilies Hydarinae and Pseudophloeinae are the most basal lineages: Hydarinae sister-group of the 21 tribes examined (Coreinae and Meropachyinae); Pseudophloeinae sister-group of the clade comprising Coreinae and Meropachyinae + Hydarinae. ...
Article
Full-text available
The morphology of the spermatheca is described in 109 species of 86 genera representing all four currently recognised subfamilies of Coreidae, covering the undivided Hydarinae, both tribes of Pseudophloeinae, all three tribes of Meropachyinae and 27 of the 32 tribes of Coreinae. Three types of spermatheca are recognised. Type I is bipartite, consisting only of a simple tube differentiated into distal seminal receptacle and proximal spermathecal duct and lacks the intermediate part present in most Pentatomomorpha, in which it serves as muscular pump. Type II is also bipartite but more elaborate in form with the receptacle generally distinctly wider than the duct. Type III is tripartite, with receptacle, duct and an often complex intermediate part. Four subtypes are recognised within type III. Type I is found only in Hydarinae and type II only in Pseudophloeinae. Type III is found in both Coreinae and Meropachyinae. Subtype IIIA (“Coreus-group”) unites many tribes from the Eastern Hemisphere and only one (Spartocerini) from the Western Hemisphere. Subtypes IIIB (“Nematopus-group”) and IIID (“Anisoscelis-group”) are confined to taxa from the Western Hemisphere and subtype IIIC (“Chariesterus-group”) is found in tribes from both hemispheres. The polarity of several characters of the intermediate part and some of the spermathecal duct is evaluated, suggesting autapomorphies or apomorphies potentially relevant to the classification of Coreidae at the sufamilial and tribal levels. Characters of the intermediate part strongly indicate that the separation of Meropachyinae and Coreinae as currently constituted cannot be substantiated. The tribes Anisoscelini, Colpurini, Daladerini and Hyselonotini are heterogeneous, each exhibiting two subtypes of spermatheca, and probably polyphyletic. Two tribes, Cloresmini and Colpurini, requiring further investigation remain unplaced. This study demonstrates the great importance of characters of the spermatheca, in particular its intermediate part, for research into the phylogeny and taxonomy of Pentatomomorpha.
... As shown above, based on the study of 108 species representing 101 genera in 27 families of Pentatomomorpha, it is clear that the external opening of the metathoracic spiracle and the associated filter apparatus exhibits considerable variability ( Fig. 7 and Table A1). Considering that the phylogenetic relationships within the Pentatomomorpha, and in particular the Eutrichophora and Lygaeoidea is unsatisfactory (Henry, 1997;Xie et al., 2005;Hua et al., 2008;Tian et al., 2011;Li et al., 2012;Li et al., 2016;Li et al., 2017;Zhao et al., 2018;Wang et al., 2016Wang et al., , 2019Liu et al., 2019;Weirauch et al., 2019;Hemala et al., 2020), we selected as a framework for our phylogenetic considerations the detailed hypothesis of Henry (1997), which was based on morphological characters of members of 15 families of Lygaeoidea, thus making it the most comprehensive of the other studies cited above. We mapped the character states of the metathoracic spiracles on Henry's (1997) cladogram (Fig. 7). ...
Article
Spiracles are the openings in the exoskeleton of insects through which air enters into the respiratory system that is formed by a series of tubes called tracheae. They are primarily located on the abdomen, but can also occur on the thorax, including the metathorax. An insect metathoracic spiracle is usually composed of an external opening and a more internal filter apparatus. We propose new terminology for these structures, and we explore the value in their use in taxonomic and phylogenetic studies within the true bug infraorder Pentatomomorpha, with emphasis on the superfamily Lygaeoidea (Insecta: Hemiptera: Heteroptera). These structures were studied using scanning electron microscopy. Two types of metathoracic spiracle external openings were recognized: a narrow opening (type N), which is slit-like; and a wide opening (type W), with internal fine structures located between the mesothoracic and metathoracic margins of the interpleural suture clearly visible. The filter apparatus in the Pentatomomorpha consists of modified mushroom bodies of the metathoracic scent gland evaporatorium, for which the term mycoid filter processes is proposed. Eight different types of mycoid filter processes, and an unmodified microsculpture type (a type with usual cuticular microsculpture and filter setae) can be found on the anterior or posterior margins of the metathoracic spiracle. We believe the wide opening (type W) to be the plesiomorphic character state in the Pentatomomorpha, with multiple, independent transformations leading to the narrow opening in Lygaeoidea. Considerable variability in the structure of the spiracle opening (in Lygaeoidea), and in the structure of the mycoid filter processes (in Pentatomomorpha) was detected. Overall, we found the morphology of these structures to be of limited value concerning the taxonomy or for determining phylogenetic relationships of the higher taxa (families) of Pentatomomorpha, but they may be useful as additional evidence for taxonomic and phylogenetic studies at the generic and perhaps the tribal levels.
... Neither the topology of the consensus tree nor any of the individual equally parsimonous trees reflect the currently accepted paradigm of the phylogenetic history of Pentatomomorpha (discussed by Henry, 1997;Xie et al., 2005;Yuan et al., 2015;Li et al., 2016Li et al., , 2017Wang et al., 2016;Liu et al., 2019). The reason of this is that the ovipositor morphology does not necessary correlate the phylogenetic position of the pentatomomorphan subclades. ...
Article
The ovipositor morphology of Trichophora (Hemiptera: Heteroptera) is revisited. Skeletomuscular structure of the ovipositor of selected species and outgroups is documented. Homologies of the structures are established, different homology hypotheses of previous authors are discussed and rejected. The groundplan of the trichophoran ovipositor is reconstructed, apomorphic conditions of each part of the ovipositor are documented. A standard nomenclature is proposed for muscles associated with the ovipositor and extrinsic muscles of the female inner ectodermal genital tracts. Character transformations of the ovipositor are reconstructed via cladistic analysis. The concepts of "lanceolate ovipositor" and "plate-like ovipositor", frequently used in the literature, are discussed; it is concluded that no unambiguous definition of them is possible on a morphological basis, these terms refer merely to evolutionary grades rather than strictly distinct character states. "Plate-like ovipositors" evolved at least four times within Trichophora; they exhibit considerable differences among and within these clades. It is demonstrated that the "M- or W-shaped sclerites" of Pyrrhocoridae and Urostylididae are not homologous: in Pyrrhocoridae they are expansions of the mesal face of the posterior portion of valvifers IX, whilst the superficially similar structures in Urostylididae are infoldings of the ventral rim of the mesal portion of laterotergites IX.
... High level relationships among Pentatomomorpha have been well demonstrated by morphological and molecular phylogenetic evidence, as follows: Aradoidea þ Trichophora (Pentatomoidea þ Eutrichophora (Coreoidea þ Lygaeoidea þ Pyrrhocoroidea)) . However, the phylogenetics of the three superfamilies of Eutrichophora (Coreoidea sensu lato) is inconsistent in recent molecular studies (Yuan et al., 2015;Li et al., 2016;Liu et al., 2019), and so their relationships remain not well resolved. ...
Article
The extinct family Yuripopovinidae Azar et al., 2011 was erected based on a true bug fossil in Lower Cretaceous amber of central Lebanon. Recently, a unique yuripopovinid Reticulatitergum hui Du et al. (2019), with an areolate body and strongly dilated antennal segment IV, was reported from mid-Cretaceous Kachin amber of northern Myanmar. Herein, the second yuripopovinid genus and species from this amber biota, Caulisoculus electrus gen. et sp. nov., is described and illustrated. The new taxon bears bizarre long eyestalks, which is an unusual morphological trait amongst true bugs. The two specialized yuripopovinid genera (Caulisoculus gen. nov. and Reticulatitergum) suggest that this extinct pentatomomorph lineage was with high disparity in Kachin amber biota.
Article
More than 95% of phytophagous true bug (Hemiptera: Heteroptera) species belong to four superfamilies: Miroidea (Cimicomorpha), Pentatomoidea, Coreoidea, and Lygaeoidea (all Pentatomomorpha). These iconic groups of highly diverse, overwhelmingly phytophagous insects include several economically prominent agricultural and silvicultural pest species, though their evolutionary history has not yet been well resolved. In particular, superfamily- and family-level phylogenetic relationships of these four lineages have remained controversial, and the divergence times of some crucial nodes for phytophagous true bugs have hitherto been little known, which hampers a better understanding of the evolutionary processes and patterns of phytophagous insects. In the present study, we used 150 species and concatenated nuclear and mitochondrial protein-coding genes and rRNA genes to infer the phylogenetic relationships within the Terheteroptera (Cimicomorpha + Pentatomomorpha) and estimated their divergence times. Our results support the monophyly of Cimicomorpha, Pentatomomorpha, Miroidea, Pentatomoidea, Pyrrhocoroidea, Coreoidea, and Lygaeoidea. The phylogenetic relationships across phytophagous lineages are largely congruent at deep nodes across the analyses based on different datasets and tree-reconstructing methods with just a few exceptions. Estimated divergence times and ancestral state reconstructions for feeding habit indicate that phytophagous true bugs explosively radiated in the Early Cretaceous-shortly after the angiosperm radiation-with the subsequent diversification of the most speciose clades (Mirinae, Pentatomidae, Coreinae, and Rhyparochromidae) in the Late Cretaceous.
Article
Recent phylogenomic analyses within the insect superfamily Coreoidea (Hemiptera: Heteroptera) have begun to challenge previous phylogenetic hypotheses of the Coreidae and Alydidae based on more traditional cladistic and non-cladistic studies. Phylogenomic studies have found the coreid subfamilies Hydarinae and Pseudophloeinae to be more closely related to a potentially paraphyletic Alydidae (an “AHP” clade) in contrast with traditional cladistic studies. However, taxon sampling within these higher-level groups has remained sparse in current phylogenetic analyses, and the taxonomic positions and monophyly of some of these taxa continue to be unclear. Here, we expand upon previous phylogenomic studies using ultraconserved element loci by increasing taxon sampling within the AHP clade. Using concatenation and summary coalescent approaches, we specifically tested previous support for an AHP clade, the paraphyly of Alydidae, the phylogenetic position of Hydarinae, and the monophyly of the two tribes of Pseudophloeinae. Our results robustly support an AHP clade and resolved the position of Hydarinae as the sister group to a clade consisting of a paraphyletic Alydidae and Pseudophloeinae, regardless of analytical method and locus/gene tree filtering strategies we employed. We also found support for the monophyly of the pseudophloeine tribes Clavigrallini and Pseudophloeini, but generic relationships within each of these tribes varied across analyses. We discuss past non-cladistic morphological studies that have suggested the potential for an AHP clade in light of our results, and we highlight further systematic work needed to discern the AHP clade as a morphologically diagnosable group for future re-classification of the Alydidae and Coreidae.
Article
Full-text available
The fifth yuripopovinid specimen from mid-Cretaceous Kachin amber is described and illustrated, and Caulisoculus monlyae Zhuo et Chen, sp. nov. is erected based upon this new specimen. Caulisoculus monlyae sp. nov. can be easily distinguished from its two congeners by possessing eyestalks almost perpendicular to vertex, compound eyes nearly spherical, hemelytra with corium slightly sclerotized and darkly pigmented, and membrane with three large subparallel cells. Our new find suggests that the extinct true bug family Yuripopovinidae was highly diversified in the late Mesozoic.
Article
Full-text available
Pentatomomorpha is one of the most diversified infraorders of the true bugs (Insecta: Hemiptera: Heteroptera). The phylogenetic relationships among superfamilies within this infraorder are still in dispute. In this study, 31 species representing 26 pentatomomorphan and four cimicomorphan putative families were chosen, and six Hox gene fragments with as many as 4 kilobases for each representative were analyzed to reconstruct the phylogeny of the Pentatomomorpha. The (Homeotic) Hox gene family is a group of nuclear genes, which is considered to determine animal segmentation. The combined nucleotide and amino acid sequences were used separately as two data matrices, and analyzed by employing maximum likelihood and Bayesian methods. Results strongly support the monophyly of Trichophora and the superfamilies Pentatomoidea, Lygaeoidea, Coreoidea, and Pyrrhocoroidea. The relationship of (Aradoidea + (Pentatomoidea + (Lygaeoidea + (Coreoidea + Pyrrhocoroidea)))) was mostly congruent with previous results based on the morphological data. Our results suggested that the Hox genes could be used as novel molecular markers for phylogenetic research on the Pentatomomorpha and other insects.
Article
Full-text available
Heteroptera are among the most diverse hemimetabolous insects. Seven infraorders have been recognized within this suborder of Hemiptera. Apart from the well-established sister-group relationship between Cimicomorpha and Pentatomomorpha (= Terheteroptera), the two terminal lineages, the relationships among the other five infraorders are still controversial, of which three (Gerromorpha, Nepomorpha and Leptopodomorpha) are intimately connected to aquatic environments. However, the various and often conflicting available phylogeny hypotheses do not offer a clear background for a connection between diversification and palaeoenvironments. In this study, a molecular data set representing 79 taxa and 10 149 homologous sites is used to infer the phylogenetic relationships within Heteroptera. Bayesian inference, maximum-likelihood and maximum parsimony analyses were employed. The results of phylogenetic inferences largely confirm the widely accepted phylogenetic context. Estimation of the divergence time based on the phylogenetic results revealed that Gerromorpha, Nepomorpha and Leptopodomorpha originated successively during the period from the Late Permian to Early Triassic (269–246 Ma). This timescale is consistent with the origin and radiation time of various aquatic holometabolans. Our results indicate that the aquatic and semi-aquatic true bugs evolved under environmental conditions of high air temperature and humidity in an evolutionary scenario similar to that of the aquatic holometabolans.
Article
Full-text available
Insect mitochondrial genome (mitogenome) are the most extensively used genetic information for molecular evolution, phylogenetics and population genetics. Pentatomomorpha (>14,000 species) is the second largest infraorder of Heteroptera and of great economic importance. To better understand the diversity and phylogeny within Pentatomomorpha, we sequenced and annotated the complete mitogenome of Corizus tetraspilus (Hemiptera: Rhopalidae), an important pest of alfalfa in China. We analyzed the main features of the C . tetraspilus mitogenome, and provided a comparative analysis with four other Coreoidea species. Our results reveal that gene content, gene arrangement, nucleotide composition, codon usage, rRNA structures and sequences of mitochondrial transcription termination factor are conserved in Coreoidea. Comparative analysis shows that different protein-coding genes have been subject to different evolutionary rates correlated with the G+C content. All the transfer RNA genes found in Coreoidea have the typical clover leaf secondary structure, except for trnS1 (AGN) which lacks the dihydrouridine (DHU) arm and possesses a unusual anticodon stem (9 bp vs. the normal 5 bp). The control regions (CRs) among Coreoidea are highly variable in size, of which the CR of C . tetraspilus is the smallest (440 bp), making the C . tetraspilus mitogenome the smallest (14,989 bp) within all completely sequenced Coreoidea mitogenomes. No conserved motifs are found in the CRs of Coreoidea. In addition, the A+T content (60.68%) of the CR of C . tetraspilus is much lower than that of the entire mitogenome (74.88%), and is lowest among Coreoidea. Phylogenetic analyses based on mitogenomic data support the monophyly of each superfamily within Pentatomomorpha, and recognize a phylogenetic relationship of (Aradoidea + (Pentatomoidea + (Lygaeoidea + (Pyrrhocoroidea + Coreoidea)))).
Book
— We studied sequence variation in 16S rDNA in 204 individuals from 37 populations of the land snail Candidula unifasciata (Poiret 1801) across the core species range in France, Switzerland, and Germany. Phylogeographic, nested clade, and coalescence analyses were used to elucidate the species evolutionary history. The study revealed the presence of two major evolutionary lineages that evolved in separate refuges in southeast France as result of previous fragmentation during the Pleistocene. Applying a recent extension of the nested clade analysis (Templeton 2001), we inferred that range expansions along river valleys in independent corridors to the north led eventually to a secondary contact zone of the major clades around the Geneva Basin. There is evidence supporting the idea that the formation of the secondary contact zone and the colonization of Germany might be postglacial events. The phylogeographic history inferred for C. unifasciata differs from general biogeographic patterns of postglacial colonization previously identified for other taxa, and it might represent a common model for species with restricted dispersal.