Journal of Integrative Agriculture 2019, 18(4): 748–757

Available online at www.sciencedirect.com

ScienceDirect

REVIEW

Invasion genetics of alien insect pests in China: Research progress

and future prospects

CHU Dong, QU Wan-mei, GUO Lei

Key Lab of Integrated Crop Pest Management of Shandong Province/College of Plant Health and Medicine, Qingdao Agricultural
University, Qingdao 266109, P.R.China

Abstract
An unwelcome side effect of the globalization of the world’s economy and dramatic increase in human mobility and trade
has been a marked increase in species invasions that have posed severe threats to the ecological, economic, and/or social
stability of the introduced regions. In this review, we analyzed the application of molecular markers in invasion genetics of
invasive alien insect pests (IAIPs) in China based on a bibliometric survey. Our report discusses the considerable progress
that has been made during the past two decades in understanding the invasion genetics of IAIPs in China. We reviewed the
major findings in the main topics including the effects of origin and routes of invasion on genetic structure, spatial and temporal
genetic changes, factors contributing to the genetic changes of IAIPs, and genetic mechanisms involved in IAIPs’ invasions.
On the other hand, some of these research areas remain relatively unexplored in China, especially those pertaining to spatial
and temporal genetic changes of IAIPs and genetic mechanisms of IAIPs’ invasions. Finally, the future research prospects
of IAIPs in China are discussed. We hope this review will stimulate an interest in and provide an increased understanding
of the field of invasion genetics of IAIPs in China, and provide a basis for future research in this area.

Keywords: biological invasion, invasive alien insect pests (IAIPs), China, invasion genetics, genetic variation

publication of The Ecology of Invasion by Animals and Plants

1. Introduction
With the globalization of the world’s economy and drastic
increase of human activities, species invasions have
posed severe threats to the ecological, economic, and/
or social stability of the introduced regions. Since the
Received 21 June, 2017 Accepted 28 November, 2017
Correspondence CHU Dong, Mobile: +86-15192495196, E-mail:
chinachudong@qau.edu.cn
© 2019 CAAS. Published by Elsevier Ltd. This is an open
access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).
doi: 10.1016/S2095-3119(17)61858-6
written by Elton (Elton 1958), the research on biological
invasions (mainly in the study of invasion ecology) has
increased tremendously, especially during the past 30 years,
providing a sound foundation for preventing and controlling
the invading species. Compared to invasion ecology,
considerably less research has been directed at invasion
genetics, although the publication of The Genetics of
Colonizing Species by Baker and Stebbins (1965) launched
the study of this field in 1965. The term “invasion genetics”
appeared toward the end of the 1990’s, and has since been
frequently used in the titles of various publications (Barrett
2015). According to Colautti et al. (2005), invasion genetics is
‘the application of genetic techniques to investigate biological
invasions’. Recently, Barrett ( 2015) further explained it as
“the study of the historical, ecological and demographic
 CHU Dong et al. Journal of Integrative Agriculture 2019, 18(4): 748–757
processes responsible for the patterns of genetic diversity
in populations and their influence on invasion success and
contemporary evolution during biological invasion”.
As the largest agricultural producer, China is the most
susceptible to experiencing the greatest monetary losses
from species invasions (Paini et al. 2016). To date, 560
alien invasive species have been recorded in China; among
these 125 have been identified as invasive alien insect pests
(IAIPs) (Wan and Yang 2016). Although the past three
decades have seen substantial progress made in the field
of invasion ecology in this country (Wan and Yang 2016),
little information is currently available on invasion genetics
(e.g., Chu et al. 2007c; Bin et al. 2014; Wan et al. 2015),
though the term “invasion genetics” has been increasingly
used in the titles of papers published in recent years (e.g.,
Cao 2016). Several reviews have discussed the molecular
makers applied in some IAIPs (Zhang et al. 2011; Quan
et al. 2012; Sun et al. 2012; Ding et al. 2014; Wang et al.
2014). The research that has been published on invasion
genetics of IAIPs in China is widely dispersed and has yet
to be comprehensively reviewed.
Based on our bibliometric survey, the number of
publications involving research in the IAIPs
in China had increased to 125 by the end of 2015 (Wan
and Yang 2016). Our survey (as of June 1, 2017) showed
that at least 66 pest species have been investigated with
various molecular markers in approximately 150 publications
since 2001 with the majority of these appearing after 2010
(Appendix A), demonstrating that the past 10 years have
been especially productive in research involving invasion
genetics of IAIPs in China. Altogether, eight orders have
been studied; of these, Coleoptera, Hemiptera, and Diptera
have been the major orders, totalling 32, 26, and 17% of
the species, respectively (Appendix A).
The majority of the research has focused on the
identification of the IAIPs and/or means of differentiation the
introduced species from other species in order to provide
rapid and accurate methods or techniques for monitoring of
the IAIPs (e.g., Chen et al. 2002, 2009; Qiu et al. 2003; Chu
et al. 2008a; He et al. 2011; He 2012; Xu et al. 2013; Jiang
2015, 2016). The major topics in this research area in China
have included the effects of origin and routes of invasion on
genetic structure, spatial and temporal genetic changes,
factors contributing to the genetic changes of IAIPs, and
genetic mechanisms involved in the IAIPs’ invasion (Table 1).
2. Effects of origins and routes on IAIPs’
genetic structure
2.1. Invasion origins
The invasion origins have been analyzed for only a few IAIPs
749
such as Bemisia tabaci Q (also known as B. tabaci biotype Q
or putative species B. tabaci MED), Liriomyza huidobrensis
and Liriomyza trifolii. B. tabaci Q can be differentiated into
several subclades based on the mtCOI gene. It has been
shown that all of the Q populations in China originate from
just a single subclade, which differs from those in the United
States where two subclades were discovered (Chu et al.
2012b). By comparing Mediterranean populations and
the Chinese populations of B. tabaci Q, Chu et al. (2011)
determined that the Chinese Q population originated from
the western Mediterranean region, possibly in Morocco
and/or Spain rather than the eastern Mediterranean region,
displaying the bias in the geographic origin of the invasion
as demonstrated in many other invasive species (Lee and
Gelembiuk 2008). The analysis using mtCOII of the genetic
structure of L. huidobrensis populations in six provinces
of China and 10 populations in eight overseas countries
demonstrated that the Asian and European populations
might have originated in South America (Wang 2010). The
Chinese populations of L. trifolii, except the ones from
Guangxi, are thought to have come from Taiwan of China,
or Europe, while the origin of the Guangxi population could
not be determined (Wang 2010). These results suggest that
the IAIPs populations generally have genetic differentiation
in their regions of origin, and thus the origins of the IAIPs
may be closely associated with the genetic structure and/
or diversity of the introduced populations.
2.2. Invasion routes
The invasion patterns of a few IAIPs in China have been
studied, e.g., B. tabaci B (also known as B. tabaci biotype B or
putative species B. tabaci MEAM1), B. tabaci Q, Solenopsis
invicta, Trialeurodes vaporariorum, and Eriosoma lanigerum.
The B. tabaci B populations collected in China in 2003, are
thought to be the progeny of multiple primary introductions
from the source region (i.e., Israel) or represent secondary
spread from another invaded region. Based on the analysis
of microsatellite markers, Chinese B. tabaci B was found to
have greater genetic diversity than B. tabaci B from Spain,
Australia, or the USA, indicating that the Chinese form might
have more than one source (Chu et al. 2012c). Similarly,
the potential invasion route of Chinese B. tabaci Q has
also been analyzed based on microsatellite loci (Chu et al.
2013) and mtCOI haplotypes (Li et al. 2017). Shao (2008)
analyzed six Chinese populations of S. invicta by using six
microsatellite loci markers, with the result showing that their
distributions were probably the result of multiple invasions.
T. vaporariorum was introduced into China more than
60 years ago. Using seven microsatellite loci, Gao et al.
(2014) analyzed the genetic diversity and population structure
of 17 collections of this insect from nine provinces. Their
750
Table 1 The invasive alien insect pests (IAIPs) in China involved in invasion genetics
Effects of origin Spatial and
Order and species of IAIPs
genetic structure changes
Isoptera
Reticulitermes speratus
Thysanoptera
Frankliniella occidentalis
Hemiptera
Aleurodicus disperses
Bemisia tabaci (includes
B. tabaci B and B. tabaci Q
putative species)
Trialeurodes vaporariorum
Dysmicoccus brevipes
Dysmicoccus neobrevipes
Matsucoccus matsumurae
Phenacoccus solenopsis
Viteus vitifoliae
(Daktulosphaira vitifoliae)
Eriosoma lanigerum
Coleoptera
Cylas formicarius
Dendroctonus valens
Heterobostrychus aequalis
Leptinotarsa decemlineata
Lissorhoptrus oryzophilus
Rhyzopertha dominica
Rhynchophorus ferrugineus
Diptera
Bactrocera dorsalis
Liriomyza huidobrensis
Liriomyza trifolii
Obolodiplosis robiniae
Lepidoptera
Cydia pomonella
CHU Dong et al. Journal of Integrative Agriculture 2019, 18(4): 748–757
Topic
Factors
and routes of temporal contributing Genetic features References (molecular marker used)1)
invasion on genetic to the genetic with invasiveness
changes
▲ Deng et al. 2016 (COII)
▲ ▲ ▲ ▲ Qiao 2012 (COI); Yang et al. 2012 (SSR,
COI); Duan et al. 2013a (SSR),
2013b (COI)
▲ Yu 2012 (COI, ITS1); Yu et al. 2013
(COI, ITS1)
▲ ▲ ▲ ▲ Luo et al. 2002 (COI); Qiu et al. 2003
(COI); Chu et al. 2006, 2007b, 2008a,
2010 (COI); Chu et al. 2007a (RAPD);
Chu et al. 2008b (ISSR); Teng et al.
2010 (SCAR, COI); Chu et al. 2011 (COI,
SSR); Pan et al. 2011 (COI); Rao et al.
2011 (COI); Shen et al. 2011 (COI); Chu
et al. 2012a (SCAR); Chu et al. 2012b
(PCR-RFLP); Chu et al. 2012c, 2013,
2014 (SSR); Shi 2012 (COI, Cytb );
Li et al. 2017 (COI)
▲ Gao et al. 2014 (SSR)
▲ He 2012 (18S, 28S, COI); He et al. 2012
(COI); He et al. 2014 (ITS1, ITS2);
He et al. 2015 (COI)
▲ He 2012 (18S, 28S, COI); He et al. 2014
(ITS1, ITS2)
▲ Yang et al. 2013 (RAPD)
▲ Chu et al. 2009 (COI);
Wu et al. 2015 (COI)
▲ ▲ Sun et al. 2009 (COI)
▲ Wu 2009 (SSR); Zhou et al. 2015 (SSR)
▲ Yu et al. 2011 (ITS1)
▲ Yin et al. 2012 (COI)
▲ Shu 2010 (RAPD, COI)
▲ ▲ Liu Q et al. 2016 (SSR, RAPD)
▲ Liu X et al. 2016 (ISSR); Wang Q L et al.
2016 (RAPD); Li et al. 2017 (AFLP)
▲ Song 2011 (AFLP, COI)
▲ ▲ Wang 2014 (COI, SSR)
▲ Wan et al. 2010 (SSR);
Wang X W et al. 2016 (COI)
▲ ▲ Wang 2010 (COII)
▲ ▲ Wang 2010 (ITS2, COI, COII);
▲ Shang et al. 2015 (COI); Yao et al. 2015
(SSR); Shang 2016 (COI, SSR); Shang
et al. 2016 (SSR);
▲ ▲ Dong 2010 (COI); Men 2012 (SSR); Men
et al. 2012 (SSR); Li 2013 (COI, COII,
Cytb); Li et al. 2013 (COI); Men 2013
(SSR); Li 2015 (COI, COII);
Zhang et al. 2015 (SSR)
(Continued on next page)
 CHU Dong et al. Journal of Integrative Agriculture 2019, 18(4): 748–757 751

Table 1 (Continued from preceding page)

Topic
Effects of origin Spatial and Factors
Order and species of IAIPs and routes of temporal contributing Genetic features References (molecular marker used)1)
invasion on genetic to the genetic with invasiveness
genetic structure changes changes
Hyphantria cunea ▲ ▲ Du 2009 (SSR); Kan et al. 2009 (RAPD);
Gao et al. 2010 (SSR); Du et al. 2012
(SSR); Liu 2012 (AFLP); Liu et al. 2012
(AFLP); Cao 2016 (SSR)
Pectinophora gossypiella ▲ Liu et al. 2006 (SSR); Liu et al. 2008
(SSR); Liu et al. 2010 (nad4, COII)
Hymenoptera
Apis mellifera ▲ Zhang et al. 2011 (AFLP)
Solenopsis invicta ▲ ▲ He et al. 2006 (COI); Shao 2008 (SSR);
Huang et al. 2014 (SSR);
Zhang and Hou 2014 (COI)
1)
▲represents references are involved in the topic.
2)
COI, COII, Cytb, and nad, mitochondrial genes; SSR, simple sequence repeat or microsatellite locus; ITS, rDNA inter-transcript spacer
region; RAPD, random amplified polymorphic DNA; ISSR, inter-simple sequence repeat; SCAR, sequence characterized amplified region;
PCR-RFLP, polymerase chain reaction-restriction fragment length polymorphism; AFLP, amplified fragment length polymorphism.

results demonstrated these populations exhibited significant
genetic differentiation, suggesting possible multiple
introductions of this insect into China. Similarly, E. lanigerum
was first detected in only three provinces (Shandong,
Liaoning, and Yunnan) during the 1910s to 1930s. Since
the 1990s, however, the aphid has spread to many other
areas of China. Using eight microsatellite loci, Zhou et al.
(2015) showed that the recently established E. lanigerum
populations in Xinjiang might not have originated from the
“supercolony” in northern China, indicating that this species
might also have multiple sources. These results suggest
that the IAIPs populations in the introduced regions often
have multiple introductions or sources.
3. Temporal and spatial changes of spe-
cies or genetic composition of IAIPs
The temporal and spatial changes of species composition of
IAIPs’ populations have been investigated in alien B. tabaci.
The putative species of B. tabaci complex, B. tabaci Q and
B. tabaci B, can be reliably differentiated using the mtCOI
gene (Luo et al. 2002; Chu et al. 2006). Since first being
detected in China in 2003, B. tabaci Q has gradually
displaced the previously well-established populations of
B. tabaci B and has now become the dominant whitefly in
most regions of the country (Chu et al. 2007b, 2010; Teng
et al. 2010; Pan et al. 2011; Rao et al. 2011; Shen et al.
2011). Based on the meta-analysis of available records,
the initial phase (such as the introduction, colonization and
establishment) of Q was in ca. 2003, the displacement of
B by Q occurred mainly during the years 2004–2007, and
since 2008, Q has become the dominant species throughout
its range in China (Chu et al. 2012a).
The temporal and spatial changes of genetic composition
in IAIPs’ populations have been investigated in the
introduced species, Frankliniella occidentalis and B. tabaci
Q. The monitoring of F. occidentalis in Shandong Province
demonstrated that this IAIP could readily disperse and
colonize a wide geographic range within a few years. In
China, F. occidentalis, which was first discovered as an
introduced species in Beijing in 2003 (Zhang et al. 2003), is
composed of two mitochondrial clades, WFT-G and WFT-L
(Rugman–Jones et al. 2010). Using the mtCOI gene, Yang
et al. (2013) noted that both types of F. occidentalis could be
detected across China. Similarly, Duan et al. (2013b) found
that both types of F. occidentalis were present in Shandong
Province, China and that WFT-G was the dominant type.
Monitoring of the genetic structure of B. tabaci Q populations
in Shandong Province using microsatellite data showed that
there was a rapid change of genetic composition in the field
populations between 2006–2012 (Chu et al. 2014).
Research focusing on the temporal and spatial genetic
changes of IAIPs’ populations plays an important role in
the discovery of IAIPs. This is especially true in cryptic
invasions, which involve introduced species that are
indistinguishable or difficult to separate from the native
species or earlier introduced species in the introduced
regions (Geller et al. 1997; Chu et al. 2012c).
4. Factors contributing to genetic changes
Previous studies have demonstrated that many factors may
be involved in the genetic changes of IAIPs, including the
bottleneck effect, founder effect, bridgehead effect, multiple
752 CHU Dong et al. Journal of Integrative Agriculture 2019, 18(4): 748–757
introductions, genetic turnover, gene flow, and hybridization.
4.1. Bottleneck effect or founder effect
Generally, an alien species will experience bottleneck or
founder effects, which can limit the success of their invasion.
These effects on the invading species may disappear after
an extended period of time or after multiple generations.
The IAIPs, especially newly established IAIPs, are ideal
subjects for studies involving the effects caused by the initial
introduction on the genetics of alien species. For example, in
analyzing the mitochondrial COI gene and 10 microsatellites
of 14 F. occidentalis populations, Yang et al. (2013)
revealed that seven of the 14 populations had a statistically
significant excess of heterozygotes under the infinite
allele model (IAM), although the test was not significant
for all populations under the TPM (two-phase model) and
stepwise mutation model (SMM). These results suggest that
these populations may have undergone a recent genetic
bottleneck due to a small founding population or a limited
number of introductions. While the genetic diversity based
on analyses of microsatellite loci markers suggests that
substantial gene flow among F. occidentalis populations
may possibly have minimized the bottleneck effects (Duan
et al. 2013a). Based on three mitochondrial genes (COI,
COII, and Cytb), Cydia pomonella populations from Xinjiang
and Gansu were shown to have undergone founder effects,
while the population from Heilongjiang had a relatively high
genetic diversity, most likely from multiple introductions (Li
et al. 2013). However, according to Men (2012), based on
analyses of microsatellite loci markers, all these introduced
populations have not experienced bottleneck effects.
4.2. Bridgehead effect and secondary introductions
Using mitochondrial and microsatellite markers in
combination, Duan et al. (2013a) analyzed the genetic
diversity of 15 populations of F. occidentalis from Shandong,
three populations from Yunnan, two populations from Beijing,
as well as two populations from California - in western North
America where the species is thought to have originated.
This study suggested that the Shandong populations
might be derived from a secondary incursion originating
in Yunnan, which may play an important role as the
bridgehead population (Yang et al. 2013). T. vaporariorum
populations collected from the provinces of Jilin, Ningxia,
Guizhou, and Qinghai appear to represent secondary
introductions originating from other Chinese provinces
(Gao et al. 2014). Using eight microsatellite loci, Zhou et al.
(2015) analyzed the genetic diversity and genetic structure
of 24 E. lanigerum populations in 10 provinces. The results
suggest that the populations in northern China may have
been introduced from Shandong or Liaoning provinces; the
populations in Yunnan consisted of an early-established
population and a population introduced secondarily
from Shandong or neighboring areas, indicating that the
population in Yunnan had at least two sources.
4.3. Gene flow and hybridization
Extensive gene flow has been revealed in many IAIPs such
as B. tabaci Q, T. vaporariorum, and E. lanigerum (Gao et al.
2013, Zhou et al. 2015). Both Yang et al. (2013) and Duan
et al. (2013a) stated that the two mitochondrial clades of
F. occidentalis, WFT-G and WFT-L, may have introgressive
hybridization, because the two genetic clades cannot be
differentiated based on nuclear genes (microsatellite loci)
or other mitochondrial genes (i.e., 28S rDNA gene).
5. Associations of genetic features with
invasiveness of IAIPs
The “genetic paradox” often found in species invasions has
been extensively studied. Introduced populations of alien
species generally have low genetic diversity because of
the bottleneck effects or founder effects, which negatively
affect their adaptation to new environments in the introduced
regions. However, many alien species have been very
successful and thus the phenomenon is regarded as a
genetic paradox. Meta-analysis has shown that the genetic
diversity of most invasive species does not decrease
dramatically in novel environments, which may result from
multiple introductions, continuous introduction, or high
propagation pressure. On the other hand, a decrease in
genetic diversity can also be conductive to the successful
invasion of some alien species such as the Argentine ant
(Linepithema humile) in North America (Tsutsui et al. 2001).
In China, research on the relationship between
invasiveness and genetic diversity of IAIPs is limited. The
mitochondrial and nuclear genetic diversity of B. tabaci Q and
F. occidentalis have been compared between populations
found in China and their regions of origin. One study found
that the mitochondrial diversity of B. tabaci Q populations in
China was lower compared to populations from its presumed
geographic origin, whereas microsatellite allele diversity
did not experience such a decline (Chu et al. 2011). Duan
et al. (2013a) found that the mitochondrial diversity in some
populations of F. occidentalis from Shandong had decreased
drastically, whereas the diversity of their nuclear alleles had
not been affected. These analyses demonstrated that the
nuclear diversity of some IAIPs in China may tend to remain
at a high level while the mitochondrial diversity decreases
drastically, suggesting that a loss in mitochondrial diversity
does not necessarily imply that nuclear allelic diversity
 CHU Dong et al. Journal of Integrative Agriculture 2019, 18(4): 748–757
will also decline. These findings may help to explain the
apparent paradox between the concept of reduced genetic
variation limiting adaptation to new environments and the
observed low genetic diversity in successful invaders (Chu
et al. 2011).
Therefore, the nuclear genetic diversity may provide
a better indication of the adaptability of an alien species
than mitochondrial genetic diversity. The paper by Chu
et al. (2012c) demonstrating that the invasive B. tabaci Q
populations have a greater nuclear genetic diversity than
the B populations, may explain why the former has spread
as rapidly as it has and succeeded in displaced the latter
in most of its range in China (Chu et al. 2012c). Another
factor to consider is that overwintering greenhouses can
allow for rapid increases in the nuclear genetic diversity of
the Q population, and thereby increasing its adaptive ability
to local environments (Chu et al. 2014).
6. Future prospects
Invasion genetics not only provides novel insight into
understanding genetic change and its potential influencing
factors, but also is applicable to successful management
of the IAIPs. For example, the B. tabaci Q species is
morphologically indistinguishable from the previously
established B. tabaci B, but differs in many biological
traits (Guo et al. 2013) including the host range, virus
transmission, insecticide resistance, and susceptibility to
a number of its natural enemies (Muňiz 2000; Muňiz and
Nombela 2001; Wang et al. 2011). B. tabaci Q is more
prone than B. tabaci B to having a higher and/or constant
insecticide resistance. This is especially true in regard
to neonictinoid insecticides (Nauen et al. 2002; Luo et al.
2010). Similarly, F. occidentalis WFT-G and WFT-L also
differ in many biological traits such as their fecundity, host
adaptability, and insecticide resistance (Rugman-Jones
et al. 2010). Thus, the advantage of being aware of a cryptic
invasion of sibling species or subclades of IAIPs would be
extremely helpful in adopting control measures including
the selection of insecticides, biocontrol agents, or variety
of crop plants.
Although the past 20 years have produced significant
strides in the field of invasion genetics of IAIPs in China,
more research will be necessary in the future, especially in
the area of spatial and temporal genetic changes of IAIPs
and in elucidating the genetic mechanisms involved in
IAIPs’ invasion.
First, empirical investigations and theoretical research in
the area of invasion genetics remain poorly explored. It is
important to select several economically important IAIPs in
the near future and subject them to a systemic, continuous
analysis or field investigation. Concurrently, international
753
collaboration will also be needed to decipher the invasion
mechanism by comparing the genetics of native and
introduced populations. This process will provide a deep
and robust insight into the genetics of biological invasions.
Second, in addition to exploration of the nuclear markers
such as the extensively used microsatellite loci (Li et al.
2015), many newly developed techniques including the next
generation sequencing technique (NGS), genomics, and
RNAi techniques will be increasingly utilized in the coming
decades. This will not only be helpful to the development of
invasion genetics, but also in the development of sustainable
management approaches of alien insects based on genetic
manipulation.
Finally, in respect to research strategies, many
researchers argue that the strategy of manipulative
experiments should be employed to study invasion genetics
(Bock et al. 2015). This advice should be heeded by the
affected researchers in China. The field of invasion genetics
of IAIPs can also effectively utilize information generated
by biocontrol researchers (Zhang et al. 2014; Zhou et al.
2014), whose data, including the number of individuals,
release time, and locations, are often recorded in detail.
The detailed information can not only help in determining the
ecological processes, but also help determine the process
rate. In addition, the genetics of migrating insects (Li et al.
2016) may also be applicable in revealing the potential
ecological factors involved in the genetic dynamics in a
region, which would greatly benefit our understanding of
the genetic mechanisms of insect invasions.
Acknowledgements
This research was supported by the National Key Research
and Development Program of China (2016YFC1201200),
the National Natural Science Foundation of China
(31572064) and the Taishan Mountain Scholar Constructive
Engineering Foundation of Shandong, China.
Appendix associated with this paper can be available on
http://www.ChinaAgriSci.com/V2/En/appendix.htm
References
Baker H G, Stebbins G L. 1965. The Genetics of Colonizing
Species. Academic Press, New York.
Barrett S C. 2015. Foundations of invasion genetics, the Baker
and Stebbins legacy. Molecular Ecology, 24, 1927–1941.
Bin S Y, Wu Z Z, Zhang H, Lin J T. 2014. Application of
molecular markers in studies of insect invasion. Acta
Entomologica Sinica, 57, 1094–1104. (in Chinese)
Bock D G, Caseys C, Cousens R D, Hahn M A, Heredia S M,
Hubner S, Turner K G, Whitney K D, Rieseberg L H. 2015.
What we still don’t know about invasion genetics. Molecular
754 CHU Dong et al. Journal of Integrative Agriculture 2019, 18(4): 748–757
Ecology, 24, 2277–2297
Cao L J. 2016. Invasion genetics of fall webworm (Hyhantryia
cunea) in China based on microsatellite markers. Ph D
thesis, Beijing Forestry University, China. (in Chinese)
Chen P, Wen S Y, Zeng L. 2002. Study on using PCR-RFLP
technique to identify L. astiyae and L. bryoniae. Wuyi
Science Journal, 10, 60–64. (in Chinese)
Chen P, Wen S Y, Zeng L. 2009. The molecular identification
of five species of Liriomyza (Diptera Agromyzidae) by PCR-
RFLP. Plant Quarantine, 5, 22–24. (in Chinese)
Chu D, Chen G F, Xu B Y, Wu Q J, Zhang Y J. 2007a. RAPD
analysis of population genetic structure of Bemisia tabaci
biotype B and biotype Q. Acta Entomologica Sinica, 50,
264–270. (in Chinese)
Chu D, Gao C S, De Barro P, Zhang Y J, Wan F H. 2011.
Investigation of the genetic diversity of an invasive whitefly
in China using both mitochondrial and nuclear DNA markers.
Bulletin of Entomological Research, 101, 467–475.
Chu D, Guo D, Pan H P, Zhang Z L, Wan F H. 2012a.
Cryptic invasion of alien species, types and effects. Acta
Entomologica Sinica, 55, 218–225. (in Chinese)
Chu D, Guo D, Tao Y L, Jiang D F, Li J, Zhang Y J. 2014.
Evidence for rapid spatiotemporal changes in genetic
structure of an alien whitefly during initial invasion. Scientific
Reports, 4, 4396.
Chu D, Hu X S, Gao C S, Zhao H Y, Nichols R L, Li X C. 2012b.
Use of mitochondrial cytochrome oxidase I polymerase
chain reaction-restriction fragment length polymorphism
for identifying subclades of Bemisia tabaci Mediterranean
group. Journal of Economic Entomology, 105, 242–251.
Chu D, Jiang T, Liu G X, Jiang D F, Tao Y L, Fan Z X, Zhou H
X, Bi Y P. 2007b. Biotype status and distribution of Bemisia
tabaci (Hemiptera, Aleyrodidae) in Shandong Province of
China based on mitochondrial DNA markers. Environmental
Entomology, 36, 1290–1295.
Chu D, Li X C, Zhang Y J. 2012c. Microsatellite analyses reveal
the sources and genetic diversity of the first-introduced
Q-biotype population and the well-established B-biotype
populations of Bemisia tabaci in China. Acta Entomologica
Sinica, 55, 1377–1386. (in Chinese)
Chu D, Liu G X, Fan Z X, Tao Y L, Zhang Y J. 2007c. Genetic
differentiation of different geographical populations of
Bemisia tabaci (Gennadius) complex. Agricultural Sciences
in China, 6, 696–705.
Chu D, Pan H P, Li X C, Guo D, Tao Y L, Liu B M, Zhang Y
J. 2013. Spatial genetic heterogeneity in populations of a
newly invasive whitefly in China revealed by a nation-wide
field survey, PLoS ONE, 8, e79997.
Chu D, Wan F H, Tao Y L, Liu G X, Fan Z X, Bi Y P. 2008a.
Genetic differentiation of Bemisia tabaci (Hemiptera,
Aleyrodidae) biotype Q based on mitochondrial DNA
markers. Insect Science, 15, 115–123.
Chu D, Wan F H, Xu B Y, Wu Q J, Zhang Y J. 2008b.
Comparative analysis of population genetic structure in
Bemisia tabaci (Gennadius) biotypes B and Q based on
ISSR marker. Agricultural Sciences in China, 7, 101–105.
Chu D, Wan F H, Zhang Y J, Brown JK. 2010. Change in
the biotype composition of Bemisia tabaci in Shandong
Province of China from 2005 to 2008. Environmental
Entomology, 39, 1028–1036.
Chu D, Zhang Y J, Brown J K, Cong B, Xu B Y, Wu Q J, Zhu
G R. 2006. The introduction of the exotic Q biotype of
Bemisia tabaci (Gennadius) from the Mediterranean region
into China on ornamental crops. Florida Entomologist, 89,
168–174.
Colautti R I, Manca M, Viljanen M, Ketelaars H A M, Burgi H,
MacIsaac H J, Heath D D. 2005. Invasion genetics of the
Eurasian spiny waterflea: evidence for bottlenecks and
gene flow using microsatellites. Molecular Ecology, 14,
1869–1879.
Deng F, Liu Y S, Pang Z P, Ping Z M, Wang J G. 2016. Genetic
differentiation of Reticulitermes speratus in East Asia.
Sichuan Journal of Zoology, 3, 361–390. (in Chinese)
Ding J J, Yu M, Liu Z W, Quan Y B, Pang Z P, Ping Z M,
Wang J G. 2014. Advance of molecular identification in the
genus Coptotermes (Isoptera, Rhinotermitidae). Journal of
Environmental Entomology, 2, 225–232. (in Chinese)
Dong K. 2010. Genetic difference analysis on geographic
populations of Cydia pomonella L. and molecular method for
larvae rapid identification based on COI gene. MSc thesis,
Northwest A&F University, China. (in Chinese)
Du J. 2009. Studies on genetic diversity and differentiation in fall
webworm (Hyphantria cunea) population and its influence
factors. MSc thesis, Agricultural University of Hebei, China.
(in Chinese)
Du J, Zhang Y M, Zhang E L, Wang J. 2012. Genetic
differentiation of fall webworm (Hyphantria cunea)
populations in Hebei Province. Journal of Anhui Agricultural
Sciences, 6, 3347–3348. (in Chinese)
Duan H S, Yu Y, Zhang A S, Guo D, Tao Y L, Chu D. 2013a.
Genetic diversity and inferences on potential source areas
for the introduced western flower thrips, Frankliniella
occidentalis in Shandong, China based on mitochondrial
and microsatellite markers. Florida Entomologist, 96,
963–972.
Duan H S, Yu Y, Zhang A S, Guo D, Tao Y L, Chu D. 2013b.
Sudden widespread distribution of western flower thrips
in Shandong Province, China. Florida Entomologist, 96,
933–940.
Elton C S. 1958. The Ecology of Invasions by Animals and
Plants. Methuen, London.
Gao B J, Du J, Gao S H, Liu J X. 2010. Genetic diversity
and differentiations of fall webworm (Hyphantria cunea)
populations. Scientia Silvae Sinicae, 8, 120–124. (in
Chinese)
Gao R R, Zhang W P, Zhang R M, Zhou H X, Pan H P, Tao Y
L, Zhang Y J, Brown J K, Chu D. 2014. Population structure
of the greenhouse whitefly, Trialeurodes vaporariorum
(Westwood), an invasive species from the Americas,
60 years after invading China. International Journal of
Molecular Science, 15, 13388–13402.
Geller J B, Walton E D, Grosholz E D, Ruiz G M. 1997. Cryptic
invasions of the crab Carcinus detected by molecular
phylogeography. Molecular Ecology, 6, 901–906.
Guo Q, Tao Y L, Chu D. 2013. Characterization and comparative
profiling of miRNAs in invasive Bemisia tabaci (Gennadius)
 CHU Dong et al. Journal of Integrative Agriculture 2019, 18(4): 748–757
B and Q. PLoS ONE, 8, e59884.
He X F, Lu Y Y, Zhang W Q, Zeng L. 2006. Three haplotypes
found in populations of the red imported fire ant invading
China. Acta Entomologica Sinica, 6, 1046–1049. (in
Chinese)
He Y B. 2012. Molecular Identification, Genetic structure and
control strategy of pink pineapple mealybug, Dysmicoccus
brevipes (Cockerell). Ph D thesis, Southwest University,
China. (in Chinese)
He Y B, Liu Y H, Zhan R L, Xu Z F, Sun G M, Zhao Y L, Li
G P, Chang J M. 2014. The occurrence of two species of
pineapple mealybugs (Dysmicoccus spp.) (Hemiptera:
Pseudococcidae) in China and their genetic relationship
based on rDNA ITS sequences. Caryologia, 67, 36–44.
He Y B, Wan X W, Liu Y H, Sun G M, Zhan R L. 2012.
Mitochondrial COI from Dysmicoccus brevipes (Hemiptera:
Pseudococcidae) suggests cryptic lineage and pinpoints the
source of the introduction to China. Florida Entomologist,
95, 183–191.
He Y B, Wang X W, Zhan R L, Sun G M, Liu Y H, Xu Z F, Zhao
Y L. 2011. Genetic relationship of 12 species of mealybugs
(Hemiptera, Pseudococcidae) based on DNA sequences.
Chinese Journal of Tropical Crops, 12, 2324–2330. (in
Chinese)
He Y B, Zhan R L, Sun G M, Wu J B, Zhao Y L. 2015.
Phylogeography of pink pineapple mealybugs, Dysmicoccus
brevipes (Cockerell) reveals the history of pineapple
introduction and cultivation in China. Genetics and
Molecular Research, 14, 9890–9897.
Huang Y W, He X F, Lu Y Y, Zeng L, Cheng D F. 2014.
Population genetic structure of Solenopsis invicta Buren
in China based on microsatellite. Journal of Biosafety, 2,
131–138. (in Chinese)
Jiang F. 2015. Technique system for molecular identification of
quarantine fruit flies in China. Ph D thesis, China Agricultural
University, China. (in Chinese)
Kan G S, Li X, Ding J Y. 2009. RAPD analysis on genetic
differentiation of Hyphantria cunea populations. Chinese
Journal of Ecology, 10, 2032–2036. (in Chinese)
Lee C E, Gelembiuk G W. 2008. Evolutionary origin of invasive
populations. Evolutionary Applications, 1, 427–448.
Li H, Lang K L, Fu H B, Shen C P, Wan F H, Chu D. 2015.
Analysis of expressed sequence tags (ESTs) from a
normalized cdna library and isolation of EST-SSRs from
the invasive cotton mealybug, Phenacoccus solenopsis.
Insect Science, 22, 761.
Li H R, Pan H P, Tao Y L, Zhang Y J, Chu D. 2017. Population
genetics of an alien whitefly in China, implications for its
dispersal and invasion success. Scientific Reports, 7, 2228.
Li S W, Wei F C, Du J, Yang M F. 2017. Genetic diversity
and spread of Lissorhoptrus oryzophilus (Coleoptera:
Curculionidae) in China, based on amplified fragment
length polymorphism. Journal of Asia-Pacific Entomology,
20, 935–941.
Li X Y, Chu D, Yin Y Q, Zhao X Q, Chen A D, Khay S,
Douangboupha B, Kyaw M M, Kongchuensin M, Ngo V
V, Nguyen C H. 2016. Possible source populations of the
white-backed planthopper in the Greater Mekong Subregion
755
revealed by mitochondrial DNA analysis. Scientific Reports,
6, 39167.
Li Y S. 2015. Population genetic structure of Cydia pomonella L.
(Lepidoptera) and Grapholita molesta Busck. (Lepidoptera)
in China, based on the mitochondrial DNA genes. Ph D
thesis, China Agricultural University, China. (in Chinese)
Li Y T. 2013. Genetic diversity and invasion source of the
codling moth Cydia pomonella (L.) (Lepidoptera, Tortricidae)
population in China inferred from mtDNA gene sequences.
MSc thesis, Northwest A&F University, China. (in Chinese)
Li Y T, Wang K, Zheng Y, Men Q L, Qian L, An Y L, Feng J
N, Zhang Y L, Chen M H. 2013. COI gene analysis based
genetic differentiation of Cydia pomonella (Lepidoptera,
Tortricidae) populations in Hexi Corridor. Journal of
Northwest A&F University, 9, 85–90. (in Chinese)
Liu J. 2012. Genetic diversity analysis by AFLP of Hyphantria
cunea populations in China and the isolation of microsatellite
makers. MSc thesis, Beijing Forestry University, China. (in
Chinese)
Liu J, Li J, Chen M, Luo Y Q, Tao J. 2012. Genetic diversity of
Hyphantria cunea populations in China by AFLP analysis.
Journal of Beijing Forestry University, 4, 107–113. (in
Chinese)
Liu Q, Li Y, Wang D H, Luo R, Shi X J, Huang Y M, Fu Y, Chen
G H. 2016. Research on genetic diversity of the rice water
weevil, Lissorhoptrus oryzophilus Kuschel (Coleoptera,
Curculionidae) based on ISSR markers. Journal of
Environmental Entomology, 1, 102–112. (in Chinese)
Liu Y, Fu K Y, Ahmat Tursun, He J, Guo W C, Zhou J. 2016.
Analysis on genetic diversity of different geographical
population of the Leptinotarsa decemlineata using RAPD
and SSR markers. Xinjiang Agricultural Sciences, 9,
1608–1617. (in Chinese)
Liu Y D, Hou M L, Wu K M. 2010. Genetic variation of
mitochondrial DNA in Chinese populations of Pectinophora
gossypiella (Lepidoptera, Gelechiidae). Environmental
Entomology, 4, 1344–51.
Liu Y D, Wu K M, Guo Y Y. 2006. Isolation and characterization
of polymorphic microsatellite loci from the pink bollworm
Pectinophora gossypiella (Saunders) (Lepidoptera,
Gelechiidae). Molecular Ecology Notes, 3, 847–849.
Liu Y D, Wu K M, Guo Y Y. 2008. Population structure and
introduction history of the pink bollworm, Pectinophora
gossypiella, in China. Entomologia Experimentalis et
Applicata, 2, 160–172.
Luo C, Jones CM, Devine G, Zhang F, Denholm I, Gorman
K. 2010. Insecticide resistance in Bemisia tabaci biotype
Q (Hemiptera, Aleyrodidae) from China. Crop Protection,
29, 429–434.
Luo C, Yao Y, Wang R J, Yan F M, Hu D X, Zhang Z L. 2002.
The use of mitochondrial cytochrome oxidase I (mtCOI)
gene sequences for the identification of biotypes of Bemisia
tabaci (Gennadius) in China. Acta Entomologica Sinica, 45,
759–763. (in Chinese)
Men Q L. 2012. Genetic diversity and structure of codling moth,
the Cydia pomonella (L), populations in China inferred
from microsatellite markers. Ph D thesis, Northwest A&F
University China. (in Chinese)
756 CHU Dong et al. Journal of Integrative Agriculture 2019, 18(4): 748–757
Men Q L, Chen M H, Zhang Y L, Feng J N. 2012. Amplifying
stability and genetic diversity of microsatellite loci in
codling moth Cydia pomonella (Lepidoptera, Tortricidae)
populations in China. Journal of Plant Protection, 4,
341–346. (in Chinese)
Men Q L, Chen M H, Zhang Y L, Feng J N. 2013. Genetic
structure and diversity of a newly invasive species,
the codling moth, Cydia pomonella (L.) (Lepidoptera,
Tortricidae) in China. Biological Invasions, 2, 447–458.
Muňiz M. 2000. Host suitability of two biotypes of Bemisia tabaci
on some common weeds. Entomologia Experimentalis et
Applicata, 95, 63–70.
Muňiz M, Nombela G. 2001. Differential variation in development
of the B- and Q-biotypes of Bemisia tabaci (Homoptera,
Aleyrodidae) on sweet pepper at constant temperatures.
Environmental Entomology, 30, 720–727.
Nauen R, Stumpf N, Elbert A. 2002. Toxicological and
mechanistic studies on neonicotinoid cross resistance
in Q-type Bemisia tabaci (Hemiptera, Aleyrodidae). Pest
Management Science, 58, 868–875.
Paini D R, Sheppard A W, Cook D C, De Barro P J, Worner
S P, Thomas M B. 2016. Global threat to agriculture from
invasive species. Proceedings of the National Academy
of Sciences of the United States of America, 113, 7575.
Pan H P, Chu D, Ge D Q, Wang S L, Wu Q J, Xie W, Jiao X
G, Liu B M, Yang X, Yang N N, Su Q, Xu B Y, Zhang Y J.
2011. Further spread of and domination by Bemisia tabaci
biotype Q on field crops in China. Journal of Economic
Entomology, 104, 978–985.
Qiao W N. 2012. Application of DNA barcoding technology
for species identification of common thrips (Insecta,
Thysanoptera) and spread trending analyse of Frankliniella
occidentalis in China. MSc thesis, Chinese Academy of
Agricultural Sciences, China. (in Chinese)
Qiu B L, Ren S X, Wen S Y, Mandour N S. 2003. Biotype
identification of the populations of Bemisia tabaci
(Homoptera, Aleyrodidae) in China using RAPD-PCR. Acta
Entomologica Sinica, 46, 605–608. (in Chinese)
Quan Y B, Liao L, Zhang W D, Ding J J, Ping Z M, Wang
J G. 2012. Advance of quarantine molecular diagnosis
of subterranean termite genus Coptotermes (Isoptera,
Rhinotermitidae). Journal of Environmental Entomology,
3, 354–362. (in Chinese)
Rao Q, Luo C, Zhang H, Guo X, Devine G J. 2011. Distribution
and dynamics of Bemisia tabaci invasive biotypes in Central
China. Bulletin of Entomological Research, 101, 81–88.
Rugman-Jones P F, Hoddle M S, Stouthamer R. 2010. Nuclear-
mitochondrial barcoding exposes the global pest Western
flower thrips (Thysanoptera, Thripidae) as two sympatric
cryptic species in its native California. Journal of Economic
Entomology, 103, 877–886.
Shang X, Yao Y, Huai W, Zhao W. 2015. Population genetic
differentiation of the black locust gall midge Obolodiplosis
robiniae (Haldeman) (Diptera: Cecidomyiidae): A North
American pest invading Asia. Bulletin of Entomological
Research, 105, 736–742.
Shang X P. 2016. Population genetic structure of an
alien invasive species Obolodiplosis robiniae (Dintera,
Cecidomviidae) in China. MSc thesis, Chinese Academy
of Forestry, China. (in Chinese)
Shang X P, Zhao W X, Huai W X, Yao Y X. 2016. Effects of
sample size on genetic diversity index for population of
Obolodiplosis robiniae in use of microsatellite DNA marker.
Plant Quarantine, 1, 32–35. (in Chinese)
Shao J G. 2008. Analysis of social forms & genetic diversity in
different geographic populations of Solenopsis invicta Buren
in China. MSc thesis, Huazhong Agricultural University,
China. (in Chinese)
Shen Y, Du Y Z, Ren S X, Qiu B L. 2011. Preliminary study of
succession of Bemisia tabaci biotypes in Jiangsu Province,
China. Chinese Journal of Applied Entomology, 48, 16–21.
Shi P X. 2012. Molecular identification of species of whiteflies
and biotypes of Bemisia tabaci in Shanghai. MSc thesis,
Jiangxi Agricultural University, China. (in Chinese)
Shu Q. 2010. Genetic diversity of geographical populations
of Heterobostrychus aequalis (Waterhouse). MSc thesis,
Southwest Forestry University, China. (in Chinese)
Song X H. 2011. Resistance and genetic differentiation of
Rhyzopertha dominica to phosphine at different spatial
scales in China. Ph D thesis, Huazhong Agricultural
University, China. (in Chinese)
Sun Q H, Chen Y C, Wang H B, Downie D A, Zhai H. 2009.
Origin and genetic diversity of grape phylloxera in China.
Acta Entomologica Sinica, 8, 885–894. (in Chinese)
Sun Q H, Du Y P, Wang Z S, Di H. 2012. Research progress on
biotypes and genetic diversity of grape phylloxera. Journal
of Fruit Science, 1, 125–129. (in Chinese)
Teng X, Wan F H, Chu D. 2010. Bemisia tabaci biotype
Q dominates other biotypes across China. Florida
Entomologist, 93, 363–368.
Tsutsui N D, Suarez A V, Holway D A, Case T J. 2001.
Relationships among native and introduced populations of
the Argentine ant (Linepithema humile) and the source of
introduced populations. Molecular Ecology, 10, 2151–2161.
Wan F H, Yang N W. 2016. Invasion and management of
agricultural alien insects in China. Annual Review of
Entomology, 61, 77–98.
Wan X W, Liu Y H, Luo L M, Feng C H, Wang S, Ma L. 2015.
Inference on the invasion history of invasive alien species
based on molecular methods. Acta Ecologica Sinica, 35,
1296–1309. (in Chinese)
Wan X W, Liu Y H, Zhang B, Zhou H D. 2010. Genetic
differentiation among poupulations of the oriental fruit
fly Bactrocera dorsalis (Hendel) in Chongqing based on
microsatellite markers. Scientia Agricultura Sinica, 13,
2688–2696. (in Chinese)
Wang G H. 2014. Population genetic structure analysis of
Rhynchophorus ferrugineus (Olivier) based on microsatellite
loci and mitochondrial COI sequences. MSc thesis, Fujian
Agriculture and Forestry University, China. (in Chinese)
Wang J H, Luo C, Liu T X, Zhang F, Li Y X. 2011. Effects
of Bemisia tabaci (Hemiptera, Aleyrodidae) biotype on
host selection and development of Encarsia sophia
(Hymenoptera, Aphelinidae). Acta Entomologica Sinica,
54, 687–693. (in Chinese)
Wang Q L, Wu J, Xu L J, Pan Y F, Luo D, Li Z H. 2016a.
 CHU Dong et al. Journal of Integrative Agriculture 2019, 18(4): 748–757
Population source analysis of Bactrocera dorsalis (Hendel)
based on complete mitochondria COI sequences in Wuxi.
China Plant Protection, 8, 5–10. (in Chinese)
Wang S Y. 2010. Analysis of mitochondrial genome sequences
and population differeatiation of several invasion leafminers.
Ph D thesis, Chinese Academy of Agricultural Sciences,
China. (in Chinese)
Wang X G, Wang D G, Liao F, Zhao J P, Lin H J, Jiang X,
Jiang Z H, Wang X L. 2014. Review on the classification
of Coptotermes termite and its effect on Chinese plant
quarantine. Plant Quarantine, 6, 8–13.
Wang X W, Fu K Y, Ding X H, Ahmat Tursun, He J, Guo W C.
2016b. Analysis on genetic diversity of the rice water weevil
based on RAPD markers in the ecological regions of oasis
in Xinjiang. Xinjiang Agricultural Sciences, 11, 2069–2076.
(in Chinese)
Wu F Z, Ma J, Hu X N, Zeng L. 2015. Homology difference
analysis of invasive mealybug species Phenacoccus
solenopsis tinsley in southern China with COI gene
sequence variability. Bulletin of Entomological Research,
105, 32–39.
Wu Q. 2009. Genetic structure analyses of woolly apple aphid
(Eriosoma lanigerum Hausmann) population in China
studied using microsatellite markers. MSc thesis, Shandong
Agricultural University, China. (in Chinese)
Wu Y, Li F, Li Z, Cao Y. 2016. Microsatellite markers for
Rhyzopertha dominica (Coleoptera: Bostrichidae). Journal
of Stored Products Research, 69, 282–285.
Xiang Z, Hou Y M. 2014. Invasion history of Solenopsis invicta
(Hymenoptera: Formicidae) in Fujian, China based on
mitochondrial DNA and its implications in development of
a control strategy. Insect Science, 21, 493–498.
Xu L, Lin W, Huang P Y, Zhang W F, Lu X Y, Wang Y, Zheng
Y, Jiao Y, Lou D F, Yu D J. 2016. Rapid detection of
Dysmicoccus neobrevipes and D. brevipes (Hemiptera,
Diaspididae) using TaqMan MGB probe. Plant Quarantine,
4, 38–41. (in Chinese)
Xu L, Yu D J, Chen Z L, Jiao Y, Lou D F, Xiang C Y, Hu Y F,
Wang H Y. 2013. Detection of three important Solenopsis
spp. (Hymenoptera, Formicidae) by real-time qualitative
PCR. Plant Quarantine, 4, 65–68. (in Chinese)
Yao Y, Zhao W, Shang X. 2015. Development of polymorphic
microsatellite markers of Obolodiplosis robiniae (Haldeman)
(Diptera: Cecidomyiidae), a North American pest invading
Asia. Journal of Insect Science, 15, 865–886.
Yang Q, Xie Y P, Fan J H, Shao S F, Wu J, Wang Y S, Zhao C
S, Zhang Y W. 2013. Genetic differentiation of Matsucoccus
matsumurae from three geographic populations in China.
Scientia Silvae Sinicae, 12, 88–96. (in Chinese)
757
Yang X M, Sun J T, Xue X F, Li J B, Hong X Y. 2012. Invasion
genetics of the western flower thrips in China, evidence
for genetic bottleneck, hybridization and bridgehead
effect. PLoS ONE, 7, 165–166.
Yin Y S, Zhang F, Qian L, Zheng S Z, An Y L. 2012. Investigating
the provenance of Dendroctonus using COI gene. Journal
of Biosafety, 3, 201–209. (in Chinese)
Yu H B, Shen J W, Ma J, Ma H J, Chen S L. 2011. The study
on rDNA ITS-1 variation of Cylas formicarius (Coleoptera,
Brentidae) populations and its invasive sources in China.
Chinese Agricultural Science Bulletin, 18, 282–287. (in
Chinese)
Yu W W. 2012. Studies on genetic differentiation of different
populations and mitochondrial and ribosomal genome
of Aleurodicus dispersus (Hemiptera, Aleyrodidae). MSc
thesis, Yangzhou University, China. (in Chinese)
Yu W W, Yang W Y, Du Y Z, Li W D. 2013. Sequence and
phylogenetic analyses of mtDNA-COI and rDNA-ITSl
genes in populations of Aleurodicus dispersus (Hemiptera,
Aleyrodidae) in Hainan, southern China. Acta Entomologica
Sinica, 11, 1324–1334. (in Chinese)
Zhang C X, Zhang X F, Chen Y Z, Cheng Y Z, Liu W Z, Jiang
Y S. 2011. Analysis of genetic diversity in twelve honeybee
populations based on AFLP technique. Scientia Agricultura
Sinica, 18, 3877–3885. (in Chinese)
Zhang D W, Luo J C, Zhou Z X, Wei Y H, Liu Y Y. 2015. Genetic
diversity analysis of different geographical populations of
the codling moth, Cydia pomonella (L.) in Gansu Province.
Plant Protection, 5, 94–99. (in Chinese)
Zhang G F, Meng X Q, Wan F H. 2011. Advances in identification
techniques of the western flower thrips, Frankliniella
occidentalis (Pargande). Journal of Biosafety, 1, 81–88.
Zhang R M, Zhou H X, Guo D, Tao Y L, Wan F H, Wu Q, Chu
D. 2014. Two putative bridgehead populations of Aphelinus
mali (Hymenoptera, Aphelinidae) introduced in China,
Florida Entomologist, 97, 401–405.
Zhang Y J, Wu Q J, Xu B Y, Zhu G R. 2003. Occurrence and
damage in Beijing of an invasive pest - western flower
thrips, Frankliniella occidentalis. Plant Protection, 29,
58–59. (in Chinese)
Zhou H X, Zhang R M, Guo D, Tao Y L, Wan F H, Wu Q, Chu
D. 2014. Analysis of genetic diversity and structure of two
clades of Aphelinus mali (Hymenoptera, Aphelinidae) in
China. Florida Entomologist, 97, 699–706.
Zhou H X, Zhang R M, Guo D, Tao Y L, Wan F H, Wu Q, Chu D.
2015. Invasion genetics of woolly apple aphid (Hemiptera,
Aphididae) in China. Journal of Economic Entomology,
108, 1040–1046.
Executive Editor-in-Chief WAN Fang-hao
Managing editor SUN Lu-juan