Austin et al.:
GENETIC EVIDENCE FOR TWO INTRODUCTIONS OF THE
FORMOSAN SUBTERRANEAN TERMITE,
(ISOPTERA: RHINOTERMITIDAE), TO THE UNITED STATES
Center for Urban and Structural Entomology, Department of Entomology
Texas A&M University, College Station, TX 77843-2143
Department of Entomology, University of Arkansas, Fayetteville, AR 72701
Department of Entomology, University of Florida-Ft. Lauderdale Research and Education Center
3205 College Avenue, Ft. Lauderdale, FL 33314
Dow AgroSciences LLC, 9330 Zionsville Road, Indianapolis, IN 46268
Exotic introductions of Formosan Subterranean Termite (FST) to the United States from
Asia have had significant economic consequences. Multiple introductions through marine
transport have been proposed, but identification of these routes has yet to reveal more than
one lineage in the continental U.S. DNA sequencing of a 640-bp cytochrome oxidase II (COII)
mitochondrial DNA (mtDNA) marker to 60 disjunct populations, revealed two independent
lineages spanning the continental U.S., Hawaii, Japan, and China. Limited genetic variation
was observed with this marker. Group I constitutes a largely Asian clade, while Group II is
comprised of both Asian and southern U.S. populations. This is the first study which has doc-
umented 2 distinct lineages to continental United States and Hawaii.
DNA sequence, genetic variation, molecular diagnostics, termite
Las introducciones exóticas de la termita subterránea de Formosa (TSF) de Asia a los Esta-
dos Unidos han tenido consecuencias económicas significativas. Introducciones multiples
por medio del transporte marino han sido propuestas, pero la identificación de estas rutas to-
davia no ha revelada mas que un linaje en los Estados Unidos continental. La secuenciación
de un marcador de 640-bp del citocromo-c-oxidasa II de ADN mitochondrial (mtADN) a 60
poblaciones separadas, revelo dos linajes independientes atravesando los Estados Unidos
continental, Hawaii, Japan y China. El marcador mostró una variación genética limitada. El
grupo I constituye un clado principalmente asiático, mientras el grupo II consiste de pobla-
ciones asiáticas y del sur de los Estados Unidos. Este es el primer estudio que documenta los
dos linajes distintas en los Estados Unidos y Hawaii.
Formosan subterranean termite (FST)
Shiraki (Isoptera: Rhinoter-
mitidae), has long been suspected to have origi-
nated from Formosa (the Island of Taiwan), but
endemic to mainland China due to the identifica-
tion of a termitophile from there (Kistner 1985).
FST has been reported from 14 southern prov-
inces in China with a northern limit of 33°28’ N
and a western limit of 104°35’E (Gao et al. 1982;
He & Chen 1981; Lin 1986) (Fig. 1). Introductions
of this exotic pest have been documented around
the world following closely with trade routes ex-
tending to the United States and beyond (Chho-
tani 1985). Historical shipping trade between the
east and west over the past 450 years (Welsh
1996; Lim 1997), and the likely introduction(s) of
FST to the continental U.S. after World War II (La
Fage 1987), have made tracking introduction
points difficult. Trading centers in Guangdong
Province (e.g., Macau, Guangzhou, Shenzhen,
and Hong Kong), Fujian Province (e.g., Puyuan)
and Shanghai Province, China, and Taiwan have
provided likely ports of origin for FST (See Prov-
ince Map, Fig 1). Gay (1967) suggests that intro-
ductions of FST into Guam, Midway Island, the
Marshall Islands, and the Hawaiian islands are
most likely due to shipping trade.
FST is believed to have been introduced to
Japan almost 300 years ago (Mori 1987; Su &
Tamashiro 1987; Wang & Grace 1999; Vargo et al.
2003), and has been hypothesized to have been in-
troduced to Hawaii almost 100 years ago (Su &
Tamishiro 1987). The history of FST introduc-
tions to the continental United States is more am-
89(2) June 2006
biguous because of likely misidentifications. For
example, early samples of
ton, Texas, during the 1950s were identified as
Snyder, but were later positively iden-
Presently, FST is distributed across the south-
east United States (Spink 1967; Howell et al.
1987; La Fage 1987; Su & Tamashiro 1987; Appel
& Sponsler 1989; Chambers et al. 1998; Su &
Scheffrahn 1998a; Cabrera et al. 2000; Haw-
thorne et al. 2000; Howell et al. 2000; Su & Schef-
frahn 2000; Hu et al. 2001; Scheffrahn et al. 2001;
Jenkins et al. 2002), and disjunct populations in
southern California (Atkinson et al. 1993;
Haagsma et al. 1995) are thought to have origi-
nated from Hawaii. Without doubt, their contin-
ued presence and growing distribution(s) have
been exacerbated by commerce and trade prac-
tices within the United States (Cabrera 2000;
Jenkins et al. 2002; Glenn et al. 2003), and by the
general lack of education and research funding di-
rected towards this problem until recently (Oper-
ation Full Stop, a FST interdiction research unit
located in New Orleans, Louisiana was initiated
by the United States Department of Agriculture,
Agricultural Research Service in 1998).
Several studies applying genetic or biochemi-
cal interpretations of FST populations have at-
tempted to identify introduction routes of FST.
However, while multiple entry points appear
likely, the lack of genetic variation in this inva-
sive species has made identification of these
routes difficult to achieve. Studies applying cutic-
ular hydrocarbons (Haverty et al. 1990), alloz-
ymes (Korman & Pashley 1991; Strong & Grace
1993; Broughton & Grace 1994; Wang & Grace
2000), mitochondrial DNA (mtDNA) (Jenkins et
al. 2002), and microsatellite DNA (Vargo & Hend-
erson 2000; Husseneder & Grace 2000; 2001a, b;
Husseneder et al. 2002) have been reported, but
current literature has not conclusively estab-
lished the origins of alternative routes to the
United States. These studies have implicated that
more than one introduction route existed, but
Fig. 1. Provincial Map of China based on Wang et al. (2002). Shaded provinces reflect areas with known Copto-
termes formosanus infestations.
Austin et al.:
they have not corroborated their suppositions
with the inclusion of additional FST populations
which might elucidate this observation.
Presumably, this could be attributed to the
overall lack of genetic diversity of FST globally. In
introduced populations, the lack of clear colony
boundaries and the potential for considerable
mixing of individuals among colonies may lead to
the formation of colonies which could extend over
large areas making colonial identity difficult, an
observation observed in unicolonial ant species
al. 2000, 2001). Alternatively, it may be that the
natural dispersal of FST alates is more signifi-
cant than previous recorded distances (Messen-
ger & Mullins 2005), an explanation proposed for
the low mitochondrial DNA (mtDNA) divergence
among sites spanning across states such as Geor-
gia (Jenkins et al. 2002). However, human-aided
dispersal of FST would be equally plausible as a
contribution to low mtDNA divergence. Some ar-
gue that the lack of genetic diversity in FST could
be due to genetic bottlenecks (Strong & Grace
1993; Broughton & Grace 1994) with limited
founder effect. Others suggest the possibility of
significant inbreeding due to neotenic involve-
ment (Wang & Grace 1995). For this to be accept-
able, one must assume that there would be some
inbreeding depression or fixation.
Herein, we report that while multiple intro-
ductions of FST (to the United States) are pre-
sumed, limited genetic variation in this species
restricts the clarification of exactly where these
exotic introductions originated from when using
some molecular markers. We provide evidence of
2 distinct lineages, occurring in the continental
United States and in the Hawaiian Islands, with
identical lineages from China.
) (Tsutsui et
all known continental United States where FST
has been reported, the Hawaiian Islands, Japan,
Hong Kong, and China (Table 1). Morphological
identification of specimens used in this study
were performed by applying the keys of Schef-
frahn et al. (1994), and verified with a FST molec-
ular diagnostic method (Szalanski et al. 2004).
Voucher specimens, preserved in 100% ethanol,
are maintained at the Arthropod Museum, De-
partment of Entomology, University of Arkansas,
Fayetteville, AR, the University of Florida-Ft.
Lauderdale Research and Education Center, Ft.
Lauderdale, FL, and the Center for Urban and
Structural Entomology, Department of Entomol-
ogy, Texas A&M University, College Station, TX.
Alcohol preserved specimens were allowed to
dry on filter paper, and DNA was extracted from
individual worker, or soldier heads by using the
Puregene DNA isolation kit D-5000A (Gentra,
were collected from
Minneapolis, MN). Extracted DNA was resus-
pended in 50 µL of Tris:EDTA and stored at
-20°C. Polymerase chain reaction (PCR) was con-
ducted with the primers TL2-J-3037 (5-ATGGCA-
GATTAGTGCAATGG-3) designed by Liu and
Beckenbach (1992) and described by Simon et al.
(1994) and Miura et al. (1998), and primer TK-N-
3785 (5-GTTTAAGAGACCAGTACTTG-3) from
Simon et al. (1994). These primers amplify a 3’
portion of the mtDNA COI gene, tRNA-Leu, and a
5’ section of the COII gene. PCR reactions were
conducted with 1 µL of the extracted DNA (Sza-
lanski et al. 2000), with a profile consisting of 35
cycles of 94°C for 45 s, 46°C for 45 s, and 72°C for
60 s. Amplified DNA from individual termites
was purified and concentrated by using Microcon-
PCR Filter Units (Millipore, Bedford, MA).
Samples were sent to The University of Arkan-
sas Medical School DNA Sequencing Facility (Lit-
tle Rock, AR) for direct sequencing in both direc-
tions with an ABI Prism 377 DNA sequencer (Fos-
ter City, CA). To facilitate genetic comparison
with existing GenBank DNA sequences, 113 bp
from the 5’ end of the sequence was removed, and
the remaining 667 bp was used. GenBank acces-
sion numbers for the FST haplotypes found in
this study are AY453588 and DQ386170. DNA se-
quences were aligned with BioEdit version 5.09
(Hall 1999) and Clustal W (Thompson et al. 1994).
The distance matrix option of PAUP* 4.0b10
(Swofford 2001) was used to calculate genetic dis-
tances according to the Kimura 2-parameter
model (Kimura 1980) of sequence evolution.
Introduction of exotic termites to the United
States is an ongoing problem that is invariably
sustained by modern trade and limited or non-ex-
istent quarantine regulations.
Native populations (in China) of FST should
possess greater genetic diversity. For this reason,
focusing on the nature of genetic variation in pop-
ulations from China and neighboring Asian coun-
tries (Vargo et al. 2003) is a logical starting point
when evaluating the nature of introduced popula-
tions to the United States (Husseneder et al.
2002) and its territories. In the present study we
evaluated native populations of FST from Guang-
dong, Shanghai, and Fujian provinces (Hong
Kong, Puyuan, Guangzhou, and Xhinhui) in
China. However, only two distinct COII haplo-
types were observed.
outgroups, Haplotype group I contains locations
from Hong Kong, Japan AB109529, Hsin-Hui
(presently known as Xhinhui), China (from Jen-
kins et al. 2002), Puyuan and Guangzhou, China,
Oahu, HI, Nagasaki, Japan, and Ft. Worth, TX
[presumably this sample was collected from
89(2) June 2006
Grapevine, TX, because the only known occur-
rences of FST in Tarrant County, TX, occur in the
Northeast portion of this county (pers. Comm.
Mike Merchant)]. Group II contains several FST
populations from disjunct locations: Hong Kong,
North Carolina, South Carolina (Jenkins et al.
2002), Georgia, Florida, Alabama (Jenkins et al.
2002), Mississippi, Louisiana, Texas, Oahu and
Maui, HI (Figs. 2 and 3). Representative taxa from
group I were slightly more divergent based on
Maximum likelihood analysis (Fig. 3). Inclusion of
FST sequence data from Jenkins et al. (2002), des-
ignated by their respective haplotype descriptions
(A through H), also fall within the two groups pre-
sented herein (Table 2, Figs. 2 and 4).
Fei and Henderson (2003) noted that incipient
colony establishment was somewhat more restric-
tive for outbred primary reproductives, owing dis-
crepancies to environmental adaptive resource
differences from two disjunct populations from
Louisiana. Furthermore, Coaton & Sheasby
(1976), and Lenz & Barrett (1982) suggest that
dominant use of neotenics for colony growth in
may be a successful strategy to in-
LocationCountryN Hap Source
Jenkins et al. 2002
Jenkins et al. 2002
Jenkins et al. 2002
Jenkins et al. 2002
Jenkins et al. 2002
Jenkins et al. 2002
Jenkins et al. 2002
Jenkins et al. 2002
Ft. Worth, TX
Forest City, NC
Marco Island, FL
Florida City, FL
Temple Terrace, FL
Palm Beach, FL
Pompano Beach, FL
San Antonio, TX
Stennis Sp Ctr, MS
New Orleans, LA
Lake Charles, LA
New Orleans, LA
St. Rose, LA
New Orleans, LA
Austin et al.:
Fig. 2. Maximum Parsimony Analysis of
open and closed circles reflect the different mtDNA COII lineages of
comparison and clarification of geographic location in Figures 3 and 4.
lineages in North America. For consistency,
, while the numbers are used for
vade new environments. If this adaptive strategy
is true for
tion may be the result and would account for some
of the limited population viscosity observed to
date. Habitat fragmentation and anthropogenic
disturbances significantly reduce population vis-
cosity. More comprehensive studies of FST may
not reveal significant genetic diversity. For FST,
reduced genetic variation does not necessarily
mean reduced fitness or vigor, but may simply im-
ply that there is greater reproductive plasticity.
For example, Hyashi et al. (2004) demonstrated
facultative parthenogenic reproduction. This
would be a significant establishment capability
for termites like FST when introduced to non-en-
demic locations such as the United States.
There have been numerous emigrations of peo-
ple to Hong Kong throughout history. Major migra-
tions of Chinese settlers from mainland China to
Hong Kong have been recorded as early as the
Song Dynasty (960-1279) (Welsh 1996). After the
end of World War II and the communist takeover of
mainland China in 1949, hundreds of thousands of
people emigrated from China to Hong Kong (Welsh
1996). In fact, locations such as Xhinhui, a treaty
port in 1904, was an important outlet for Chinese
emigrants to the United States (Anonymous 2004).
, reduced genetic varia-
(in Japan) can utilize
The introduction of FST to the U.S. likely occurred
several times, perhaps more than ten different oc-
casions (RHS, personal communication). Given
this fact, it is remarkable that the established link
between the U.S. and China has never been sub-
stantiated for more than one FST lineage.
Populations of FST from Japan appear only in
one of the presented clades (Group I, Fig. 2), and
further sampling from more locations (in Japan)
may provide additional information on whether
Japan could have contributed more significantly
to FST introductions to Hawaii or the continental
United States. Group I (Fig. 2) is largely com-
prised of samples from Asian/Pacific locations but
has one sample (Ft. Worth, TX) that was collected
in the continental U.S. (Fig. 3). This is significant
because it implicates a second introduction route
to the continental U.S. that has never been iden-
tified in previous studies. Group II, is comprised
of FST samples from nearly all known southeast-
ern states (Alabama, Florida, Georgia, Louisiana,
Mississippi, North Carolina, South Carolina),
Texas, Hawaii, and several FST from China. Both
clades are well-supported by strong bootstrap
support (>80%) by both parsimony and Liklihood
analyses (Figs. 1 and 3).
Although FST distributions have been more
recently updated (Wang et al. 2002), the lack of a
Fig. 3. Introduction routes of Coptotermes formosanus from Asia to North America. Dashed arrow pointing to-
wards Southern California suggests the introduction from Hawaii based on anecdotal information that has not been
corroborated in genetic studies to date.
Austin et al.:
geographic explanation for a second lineage intro-
duced to the United States remains unclear
(Wang & Grace 2000). Sequence data obtained
from GenBank, from Jenkins et al. (2002), pro-
vides a second haplotype match in the continental
United States (haplotype E from Ft. Worth, TX)
that represents the first documented case corrob-
orating multiple lineages from presumably multi-
ple introductions (at least two in the present
study). These two distinct haplotypes share one
commonality—both groups have representatives
with identical haplotypes (lineages) from Hong
Kong, Japan, Hawaii, and the continental United
States (Fig 3).
There were numerous FST samples where re-
peated attempts to amplify sufficient DNA for se-
quencing of the mtDNA COII gene were not suc-
cessful (e.g., FST from San Diego, California and
Tai Chuong, Taiwan). These results were not sur-
prising, as we have routinely observed ~60% effi-
ciency when using the COII marker with FST.
However, amplification of the 16S rRNA for these
samples was successful. We routinely observe
>90% efficiency for this marker with FST. While
the utility of the 16S marker is excellent for phy-
logenetic studies of the genus
unpublished), for molecular diagnostic methods
(Szalanski et al. 2004), or other rhinotermitids
(Szalanski et al. 2004; Austin 2004a; 2004b), it
does not provide the degree of genetic variation
suitable to discern the two distinct FST haplo-
types observed in this study. The slightly larger
COII amplicon (640 bp versus 428 bp of 16S
rRNA) provides only a small increase in resolu-
tion between FST populations, even though it
works well for other Rhinotermitidae (Austin et
al. 2002, 2004c). Our laboratory experience with
FST suggests that in general, it is more difficult
to extract high quality DNA from Coptotermes for
genetic studies when compared to other rhinoter-
mitids, a problem that may be more common than
reported. Additional problems may include the
presence of unknown inhibitors, method of sam-
ple preservation (some preservation methods are
known to provide poorer quality DNA for genetic
studies (Post et al. 1993; Reiss et al. 1995;
et al. 1996)
or the age of samples provided.
While the idea that multiple introductions to
the United States have been proposed, alternate
introduction routes have never been substanti-
ated in literature. This study provides a glimpse
of some of the difficulties encountered working
with FST. Most notably, it would appear that the
low genetic variation detected with our COII
marker in this species does not equate to reduced
fitness or establishment capability.
Populations of nearly all species, social or other-
wise, exhibit at least some degree of genetic differ-
entiation among geographic locales (Ehrlich &
Raven 1969). Herein, we present two distinct COII
haplotypes of FST in the continental United States
(one based on our own samples evaluated, and a
second from Jenkins et al. (2002)). However, our
results appear to contradict the degree of variation
described by Jenkins et al. (2002). They describe 8
different COII haplotypes (maternal lineages)
from 14 geographic locations across the southeast
United States, Hawaii, and China. Applying the
COII marker to 60 geographic locations (Table 1)
we only identified 2 haplotypes—one in Japan, two
in Hawaii, the continental United States, and
China, respectively. Noting that many of the vari-
able sites in Jenkins et al. (2002) occur at positions
651 through 685 of their slightly larger COII am-
plicon (total size of the amplicon was 685), it is un-
clear where the discrepancies occurred. One possi-
bility may be due to sequence error that could only
be detected by comparison with greater taxon sam-
pling. Other possibilities may be due from im-
proper sequence alignment or mispriming of tem-
plate DNA during PCR. We elected to include all
taxa from Jenkins et al. (2002) into our sequence
dataset (COII lineages A through H), which may
have provided an advantage due to our larger
number of locations sampled. As with animal pop-
ulations, additional genetic structure normally is
to be expected over increasing spatial scales,
where populations can show additional differenti-
Hap8 11 19 3233 46176 211 222297333 427643
Jenkins et al. (2002).
89(2) June 2006
Fig. 4. Maximum Likelihood analysis
lineages in North America.
Austin et al.:
ation due to spatial habitat structure and isolation
by distance (Avise 2004). However, our results
seem to refute this generalization for FST, a fact
probably attributed to its establishment ability in
fragmented urban ecosystems and their indirect
interactions with humans.
The preponderance of FST research appears to
support our findings. Haverty et al. (1990) found
no differences in qualitative cuticular hydrocar-
bon profiles among four FST populations in the
U.S. Korman & Pashley (1991) concluded that
populations from Florida and New Orleans are in
the same group and are very closely related to
each other, a finding also corroborated within the
present study (Fig. 3). Strong & Grace (1993) con-
cluded that low genetic and phenotypic variabil-
ity in introduced FST populations to Hawaii could
have been from a single event. Broughton &
Grace (1994) observed that only 9 of 16 different
restriction enzymes cut mtDNA zero or once.
Vargo et al. (2003) was unable to detect signifi-
cant isolation by distance among colonies at the
spatial scale studied (0.7-70 km) from 2 disjunct
populations of FST in Japan, nor from popula-
tions in New Orleans, LA and Oahu, HI. This sug-
gests a general lack of strong population viscosity
in introduced populations of FST. The finding also
seems to be contrary to Jenkins et al. (2002),
whose FST samples ranged in distance from 6-37
km in Atlanta, GA. Wang & Grace (2000), apply-
ing enzymatic polymorphisms, concluded that at
least two introductions to the United States have
occurred, but the second clade in their study
lacked sufficient samples from China to deter-
mine the origin of a second route.
More recently, the utility of mtDNA markers
for identifying where exotically introduced
(Szalanski et al. 2004),
(Scheffrahn et al. 2004) and
(RHS, unpublished) to the United
States is being investigated. The principal caveat
with studies of this nature is that significant rep-
resentation of taxa is essential, particularly when
dealing with species of limited genetic variation
like FST. A secondary caveat is that tremendous
skill in identifying termites morphologically is es-
sential to ensure the validity of a genetic study
based on known, identified samples. Because FST
was likely misidentified when it was first ob-
served in the continental United States, little at-
tention was given, and subsequent populations
have developed over the years. This was one of the
reasons behind developing molecular diagnostics
for this species (Szalanski et al. 2004), and a need
to genetically review some species to corroborate
their original identifications (Scheffrahn et al.
2004). As population-level studies for FST from
various locations across the world continue to ac-
cumulate (see Vargo et al. 2003), perhaps a better
understanding of local factors which contribute to
the low genetic diversity observed in FST will be-
come more apparent. Given the 300 years of
known occurrence in Japan (Vargo 2003) and the
lack of genetic variation in China, it is unlikely
we will observe significant variation in this spe-
cies within the U.S. Random genetic drift is un-
likely to occur at a rate that we will detect any-
time soon. Perhaps more intuitively, we should
not assert our scientific prejudices about the na-
ture of reduced genetic variation in FST (causing
some reduction in fitness), or Isoptera in general,
until we more exhaustively investigate their ba-
sic biology and reproductive systems.
We thank R. Davis, M. Merchant, G. Henderson,
K. Grace, J. Nixon, L. Yudin, J. Lopez, K. L. Mosg,
J. Chapman, S. Cabellero, J. Chase, B. McCullock,
O. Miyashita, E. Phillips, P. Ban, M. Weinberg, J. Stotts,
N.-Y. Su, E. Vargo, P. Fitzgerald, M. K. Rust, D. Mura-
vanda, J. Darlington, L. Ethridge, and J. Woodrow for
collecting termite samples. Research was supported in
part by the University of Arkansas, Arkansas Agricul-
tural Experiment Station, the University of Florida
Research Foundation, the Center for Urban and Struc-
tural Entomology, Texas A&M University, and a grant
from USDA-ARS Agreement No. 58-6435-3-0045.
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