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ANRV363-EN54-20 ARI 23 October 2008 13:50
Biology of Subterranean
Termites: Insights from
Molecular Studies of
Reticulitermes and Coptotermes
Edward L. Vargo1and Claudia Husseneder2
1Department of Entomology, North Carolina State University, Raleigh,
North Carolina 27695-7613; email: ed vargo@ncsu.edu
2Department of Entomology, Louisiana State University, Agricultural Center,
Baton Rouge, Louisiana 70803; email: chusseneder@agcenter.lsu.edu
Annu. Rev. Entomol. 2009. 54:379–403
First published online as a Review in Advance on
September 15, 2008
The Annual Review of Entomology is online at
ento.annualreviews.org
This article’s doi:
10.1146/annurev.ento.54.110807.090443
Copyright c
2009 by Annual Reviews.
All rights reserved
0066-4170/09/0107-0379$20.00
Key Words
Rhinotermitidae, population genetics, molecular ecology,
microsatellites, caste determination, breeding structure
Abstract
Molecular genetic techniques have made contributions to studies on
subterranean termites at all levels of biological organization. Most of
this work has focused on Reticulitermes and Coptotermes, two ecologically
and economically important genera. DNA sequence data have signifi-
cantly improved our understanding of the systematics and taxonomy of
these genera. Techniques of molecular biology have provided important
new insights into the process of caste differentiation. Population genetic
markers, primarily microsatellites, have furthered our understanding
of the life history, population biology, community ecology, and inva-
sion biology of subterranean termites. Recent results on the behavioral
ecology of subterranean termites reveal a picture different from long-
held views, especially those concerning colony breeding structures and
foraging ranges. As additional molecular tools and genomic resources
become available, and as more subterranean termite researchers in-
corporate molecular techniques into their approaches, we can expect
accelerating advances in all aspects of the biology of this group.
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INTRODUCTION
Subterranean termites (Rhinotermitidae) are a
large and important group of social insects.
They are the most widely distributed family
of termites, occurring throughout the tropical,
subtropical, and temperate regions of the world
(32). They are especially abundant in temper-
ate areas, where their biomass can approach that
of many tropical termites (15, 39). In addition,
they frequently attack human-made structures,
exerting a major economic impact estimated to
be as high as $11 billion per year in damage and
control costs in the United States alone (119).
Subterranean termites occupy an important
evolutionary position within the Isoptera. Ter-
mites are typically divided into the higher ter-
mites (Termitidae), containing some 80% of all
species, and the lower termites, represented by
the remaining six families. Of the lower ter-
mites, the Rhinotermitidae are the most de-
rived (59). Reticulitermes and Coptotermes are es-
pecially important as transitional taxa between
the lower and higher termites for three rea-
sons. First, new phylogenetic analyses (5, 59,
75) show that the clade containing these genera
is likely the sister group of the Termitidae, indi-
cating that Reticulitermes and Coptotermes share
an especially close affinity with the higher ter-
mites. Second, these two genera contain more
species than any other genus of subterranean
termites and are among the most species-rich
genera of all the lower termites (63). Third, they
exhibit features intermediate between lower
and higher termites (59), such as feeding habits
typical of lower termites, nesting habits inter-
mediate between the single-site nesting of more
basal lower termites (in which colonies use a
single piece of wood as both nesting site and
food source) (116) and the central-site nesting
of higher termites (in which colonies use mul-
tiple sources of food away from the nest site)
(116), as well as the presence of a true worker
caste, a trait primarily associated with higher
termites. Thus, understanding basic features of
the life history, behavior, and ecology of Reti-
culitermes and Coptotermes can provide insights
into the evolution and remarkable radiation of
the higher termites.
Termites have attracted increasing attention
from entomologists. This is especially true of
subterranean termites, where a search of the
worldwide literature shows that between 2000
and the date of this review there have been
more papers published on this group (934) than
during all of the previous century (694). Al-
though aspects of the biology of this group have
been the subjects of many excellent reviews,
these have tended to be regionally and/or taxo-
nomically limited in nature. Some more recent
reviews of this group include summaries of the
biology of Reticulitermes spp. (130) and Coptoter-
mes formosanus (122, 142), the life histories of
termites in general (116), the evolution and de-
velopment of termite castes (109), and the gut
symbionts of wood-feeding termites (16).
Molecular genetic methods are providing
exceptional new insights into the biology of
subterranean termites. In addition to elucidat-
ing such basic processes as development and
caste differentiation, molecular techniques give
us a window into the breeding structure, as well
as colony and population dynamics, that has re-
mained elusive owing to the cryptic nesting and
foraging habits characteristic of these species.
Here, we review some of the progress that has
been made using molecular methods in the ar-
eas of taxonomy, caste differentiation, breeding
structure, behavioral biology, and community
ecology. We focus on Reticulitermes and Cop-
totermes because these genera have been the
subject of more than three-quarters of these
studies, and because these genera contain the
most economically important termites in many
parts of the world, especially temperate and
subtropical regions.
SYSTEMATICS AND
PHYLOGEOGRAPHY OF
RETICULITERMES AND
COPTOTERMES
Taxonomy
Subterranean termites pose many taxonomic
challenges at the species level and above. The
taxonomy of both Reticulitermes and Coptotermes
380 Vargo ·Husseneder
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Table 1 Species status of Reticulitermes in North America
Species Distribution Status Reference(s)
R. flavipes Throughout eastern and central United States Valid (11)
R. arenincola Sandy soils near the Great Lakes Nomen dubium (4)
R. virginicus Throughout eastern and central United States Valid (4)
R. hageni Throughout eastern and central United States Valid, but may be species complex (44)
R. malletei Eastern United States Valid (11)
R. tibialis Western and Midwestern United States Valid, but may be species complex (24, 44)
R. hesperus Western United States Valid, but may be species complex (24, 44)
R. okanaganensis Pacific Northwest Valid (124)
is far from settled. At the present time, these
two genera are by far the largest within the
Rhinotermitidae, with 75 and 71 described
species, respectively, accounting for nearly half
of all subterranean termite species among the
15 recognized genera (63). The large number
of species in these two genera is due largely
to a plethora of new species descriptions that
have appeared in China over the past 60 years
(31). These genera are in need of careful mono-
graphic revisions, with particular emphasis on
Oriental forms.
Existing taxonomic keys are spotty in cover-
age, both in terms of taxonomic breadth and ge-
ographic region, and the characters used to dis-
tinguish species are often too variable to provide
reliable determinations (125). The recent appli-
cation of molecular genetic data, especially in
combination with cuticular hydrocarbon com-
position, morphological characters, and flight
phenologies, has helped clarify the taxonomy
of these genera.
The past five years have seen significant
changes in the taxonomy of Reticulitermes in the
United States, where there are currently seven
recognized species (Table 1). On the basis of
primarily molecular data, these changes include
the probable synonomy of one species (R. aren-
incola is considered to be R. flavipes) (4) and the
addition of two new species: R. malletei (4) in
the eastern United States and R. okanaganen-
sis in the Pacific Northwest (124). From all the
available evidence, there are likely other unde-
scribed species, especially within R. tibialis and
R. hageni, both of which appear to be species
complexes (24, 44).
Compared to the still unsettled situation in
the United States, the taxonomic status of Reti-
culitermes seems well resolved in Europe, where
there are currently seven recognized taxa:
R. balkanensis,R. grassei,R. banyulensis,R. urbis,
R. lucifugus lucifugus,R. l. corsicus, and the in-
troduced R. flavipes (=R. santonensis) (22, 134).
These taxonomic designations have been sup-
ported by a number of studies using DNA
sequence data (13, 81, 82, 134).
What little taxonomic work has been done
on Coptotermes suggests this genus is in seri-
ous need of revision. The widespread and de-
structive C. gestroi was apparently described
as several different species that have recently
been synonymized (66, 144), including C. hav-
ilandi and C. vastator, previously recognized
as invasive pest species. In Australia, where
there are six currently described Coptotermes
species, there are likely several more unrecog-
nized species (74). We can certainly expect to
see many taxonomic changes in this genus in
the future as greater attention is given to this
widespread and economically important taxon.
Molecular Tools for
Species Identification
The application of molecular genetic tech-
niques to clarify species relationships has
provided PCR-based tools for species identifi-
cation. PCR-restriction fragment length poly-
morphism methods have been developed for
distinguishing among Reticulitermes species in
the south-central United States (125) and for
differentiating C. formosanus from other species
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ANRV363-EN54-20 ARI 23 October 2008 13:50
of Coptotermes (126). The advantages of such di-
agnostic methods are (a) they remove much of
the ambiguity of identification based on mor-
phological keys, (b) they can be used with any
caste or developmental stage, and (c) they can be
performed on a single individual. These tech-
niques have allowed for more extensive stud-
ies of species ranges, for detection of species
introduced into locations outside their native
ranges, and for the determination of the rel-
ative abundance of species in particular geo-
graphic areas (7–10, 125). For example, the
relative abundance of Reticulitermes species in
the eastern and central United States has re-
ceived much recent attention. Three species,
R. flavipes,R. virginicus, and R. hageni, are sym-
patric over much of this region (118). In addi-
tion, they often occur together with R. malletei
(4) in the eastern United States, R. tibialis in
the central United States, and the introduced
C. formosanus throughout much of the south-
ern portions of their ranges (120). Studies of
samples collected across the range (7–9, 27, 92,
101) show varying species compositions, with
R. flavipes occurring most commonly, ranging
from 74% to 90% of all samples, and R. vir-
ginicus and R. hageni present at much lower fre-
quencies. The one clear exception to this pat-
tern was a South Carolina coastal site, where
R. hageni was the most common species, occur-
ring at a slightly higher frequency (43%) than
R. flavipes (37%) (141).
Little is known about the determinants of
species diversity in subterranean termite com-
munities, or the factors that contribute to co-
existence of species that are apparently so sim-
ilar in their ecological roles and life histories.
Future studies of relative species abundance,
combined with population genetic characteris-
tics such as gene flow and dispersal, will pro-
vide insights into both environmental factors
and population processes that influence species
richness in subterranean termite communities.
Phylogeography and Diversification
Phylogeography, the study of historical pro-
cesses and their effects on species distributions
(14), has great potential to elucidate the evolu-
tionary relationships among subterranean ter-
mite taxa, the processes leading to speciation,
and the factors determining current distribu-
tions. So far only Reticulitermes spp. in southern
Europe and the Middle East have received at-
tention in this regard (6, 20, 22, 68, 80–82, 85).
Results of these studies suggest that there were
four refugia scattered through southern Europe
and the Middle East during the last glacial max-
imum, each harboring one or more species or
subspecies. The northward expansion and ra-
diation of populations from these refugia fit
reasonably well with the current distributions
of species and subspecies throughout southern
Europe, especially if one assumes that the rate
of mitochondrial DNA evolution in this group
has occurred at 10 times the rate normally as-
sumed for insects, as appears to be the case (80).
Our understanding of the taxonomy and evolu-
tionary history of the Reticulitermes spp. would
benefit from similar analyses in other parts of
the world.
DEVELOPMENT AND
CASTE DIFFERENTIATION
Castes
Termites are unique among the social insects
because they undergo incomplete metamor-
phosis and display a remarkably complex and di-
versified caste polyphenism (109). Within each
mature colony, morphologically differentiated
castes (workers, soldiers, reproductives) and un-
differentiated immatures cooperate in a highly
integrated manner. This functional network of
behaviorally and morphologically specialized
individuals is the cornerstone of the advanced
eusociality characteristic of termites.
The terminology regarding caste, especially
in the lower termites, is complicated and some-
what controversial. Here we follow the nomen-
clature of Thorne (128). There appears to
be considerable variation in the developmen-
tal pathways within the large and diverse fam-
ily Rhinotermitidae (109), but Reticulitermes
and Coptotermes share many similarities in their
382 Vargo ·Husseneder
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caste patterns. In principle, larvae develop into
workers or nymphs. Nymphs develop either
into alates with wings and eyes (imagoes) that
disperse and become primary colony founders,
or they develop into brachypterous (second
form) neotenic reproductives with rudimentary
wings and no eyes that do not disperse but
supplement or replace the reproductives within
the colony. Workers can transform into apter-
ous (third form) neotenic reproductives with
no wings and eyes, remain workers, or become
presoldiers that molt into soldiers. Diagrams
depicting the various developmental pathways
within colonies of subterranean termites have
been presented for Reticulitermes spp. (70, 145),
C. formosanus (106), and C. lacteus (110).
As with other types of polyphenisms, caste
determination is the result of the interaction of
endogenous and exogenous factors during crit-
ical stages in development (96). Although little
progress has been made in identifying exoge-
nous factors involved in caste determination in
termites, morphogenic hormones, primarily ju-
venile hormone ( JH), play a pivotal role in caste
determination (46, 96). With the new tools of
molecular biology, such as expressed sequence
tag (EST) libraries, DNA arrays, quantitative
PCR, and gene silencing via RNA interference,
termite researchers are now able to investigate
the molecular mechanisms modulating the ac-
tion of JH, as well as elucidate the downstream
effects of JH and the genomic network under its
control. In addition, molecular studies are pro-
viding important new insights into gene expres-
sion levels associated with caste-specific mor-
phogenesis in general.
Soldier Differentiation
A number of studies have shown that in both
Reticulitermes and Coptotermes relatively high JH
levels in workers will induce them to molt into
soldiers (33, 84, 100, 113). On the basis of gene
expression profiles and gene silencing experi-
ments (114, 115, 145–147), Zhou et al. (147)
proposed that hexameric proteins play a cen-
tral role in regulating soldier caste determi-
nation by modulating the availability of JH in
the hemolymph. A first approach to determine
how JH action modulates expression of caste-
specific genotypes is to identify genes whose
expression levels change in response to JH ac-
tion during caste differentiation. Zhou et al.
(147) identified various genes associated with
morphogenesis that were up- or downregulated
in response to silencing of a hexamerin gene,
including genes involved in signal transduc-
tion, transcription, translation, and cytoskele-
tal structure. These genes are likely part of the
hexamerin-controlled JH-dependent gene net-
work that regulates soldier differentiation.
Zhou et al. (147) proposed a model in which
JH production is influenced by extrinsic and in-
trinsic factors. According to the model, various
intrinsic factors modulate hexamerin levels that
in turn attenuate the effects of JH. The pos-
sible extrinsic factors affecting JH production
include both environmental and social stim-
uli. Intrinsic factors that may affect JH pro-
duction and/or hexamerin levels are nutritional
status, allatostatins (143), sex, and developmen-
tal stage. The link between caste differentiation
and nutritional status is especially intriguing
given the role of hexamerins as both storage
proteins and putative JH binding proteins that
may regulate caste polyphenism in the euso-
cial wasp Polistes metricus (49), suggesting a
widespread role for hexamerins in social insect
caste determination.
Differentiation of
the Reproductive Caste
Although the process of reproductive caste dif-
ferentiation, either in the form of imagoes or
neotenics, has received less attention than sol-
dier determination, it is likely that many of the
same processes are involved (96). Elliott & Stay
(33) found elevated JH titers in the differenti-
ation of both soldiers and apterous neotenics
from workers in R. flavipes, but individuals ap-
parently destined to become soldiers had higher
JH levels than those developing into neoten-
ics. Although both apterous and brachypter-
ous neotenics readily develop in colonies of
Reticulitermes lacking functional reproductives
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ANRV363-EN54-20 ARI 23 October 2008 13:50
(93, 102, 103), neotenics are not formed in labo-
ratory colonies of C. formosanus devoid of active
reproductives (106). Raina et al. (106) have pro-
posed that nymph development and subsequent
neotenic differentiation in this latter species re-
quire a yet undetermined nymph induction fac-
tor produced by reproductives.
To shed light on the genomic network in-
volved in differentiation of the reproductive
caste, Scharf et al. (115) identified genes that
were differentially expressed in nymphs and re-
productives. A gene coding for a hexamerin
protein showed highest expression in nymphs
and neotenic reproductives and is thus assumed
to play a role in reproductive differentiation
(115), possibly by modulating the availability
of JH in the hemolymph. Following the gen-
eral model of insect development, low JH titers
during critical JH-sensitive periods in develop-
ment almost certainly regulate differentiation
into reproductives in subterranean termites, al-
though the number and timing of these critical
periods are likely to differ between develop-
ment into primary reproductives and develop-
ment into neotenics (96).
Genetic Caste Determination
Differentiation into primary reproductives in
R. speratus, at least in the laboratory, may have a
sex-linked genetic component (45). According
to a proposed model, the production of primary
reproductives occurs exclusively in colonies
headed by neotenics, but so far this has not
been confirmed in field colonies of R. speratus
or other Reticulitermes spp. Existing data on R.
flavipes and R. virginicus do not support genetic
caste determination as an important mechanism
regulating alate production in these species, be-
cause alates are not produced mainly or exclu-
sively by neotenic-headed colonies in the field
(17, 28). Although the possibility of genetic
caste determination in subterranean termites is
intriguing, additional studies are needed to con-
firm that this occurs under field conditions.
Although we still have a very rudimentary
understanding of the genetic and physiological
mechanisms influencing development and caste
determination in subterranean termites, there
have been several important and promising ad-
vances in this field. It is clear that the applica-
tion of molecular tools together with reliable
bioassays have shed new light on the processes
regulating caste polyphenism.
ALATE DISPERSAL AND
COLONY FOUNDATION
In general, colonies of subterranean termites
are founded by monogamous pairs of repro-
ductives following large synchronous mating
flights that occur in response to climatic condi-
tions during species-specific times of the year
(61, 98). After the mating flight, individuals
land on the ground, shed their wings, and begin
the process of searching for partners. Partner-
finding in some subterranean termite species,
including Reticulitermes spp., is facilitated by a
sex pheromone emitted by the female, whereas
in other species, such as C. formosanus, females
do not appear to produce a chemical attractant
(99, 107). After shedding their wings, partners
run in tandem with the female in the lead. As
soon as a suitable nest site is found, pairs move
underground or into wood to mate and repro-
duce. There is high mortality and thus intense
selection during the founding phase.
Partner Selection
There are a number of reasons to believe that
both male and female termites should be se-
lective in their choice of mates. First, termites
mate for life and perform intensive biparental
care. Second, large body size and/or weight can
be advantageous in mate selection, because the
first generation of larvae is entirely dependent
on the fat reserves of the founding pair until for-
agers emerge to provide the young colony with
nutrition (67, 88, 117). Third, genetic charac-
teristics of potential partners, such as genetic
diversity and relatedness, may influence colony
fitness. For example, males of C. formosanus
are more likely to pair with females exhibiting
higher levels of heterozygosity (55). However,
tandem pair formation in C. formosanus appears
384 Vargo ·Husseneder
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to be random with respect to kinship (55), as was
reported for the Japanese subterranean termite,
R. kanmonensis (67), and R. flavipes (28). The lack
of evidence supporting kin discrimination dur-
ing colony founding in subterranean termites is
surprising considering the mounting evidence
of negative effects of inbreeding in many plants
and animals (64) and in subterranean termites
(28, 36, 54), but data on more species, espe-
cially those that undergo short-range dispersal
flights, are needed before we can rule this out
as a mechanism promoting outbreeding in this
group.
Dispersal Distances
One possible mechanism that could promote
outbreeding is long-range dispersal of alates
reducing the likelihood that nestmates en-
counter each other during tandem pair for-
mation. Flight distances appear to vary among
species of subterranean termites, ranging from
a few meters to 1 km or further, and likely have
been underestimated in some cases (61, 98).
Genetic studies of alates from mass swarms of
C. formosanus in New Orleans, Louisiana, sug-
gest alates can fly at least 1 km (57). Dispersal
distance in this species is sufficient to guaran-
tee mixing of up to 29 colonies within a swarm
aggregation in areas of high population den-
sity; under conditions of random mating up to
90% of alate pairings would be among non-
nestmates (57).
Studies of gene flow in Reticulitermes sug-
gest that alate dispersal distances can be suffi-
cient to promote outbreeding in some species,
e.g., R. virginicus (28), yet insufficient in oth-
ers, leading to the probable pairing of related
primary reproductives during colony founding,
e.g., R. hageni (138, 141). In a study of R. flavipes,
some 20% of founding pairs were composed of
likely siblings, but few of these successfully es-
tablished colonies, presumably because of in-
breeding depression during colony foundation
(28). The apparent variation in the tolerance
to the potential effects of inbreeding in closely
related sympatric species merits further inves-
tigation.
Colony breeding
structure: number
and degree of
relatedness of the
reproductive
individuals within
colonies
Simple family
colony: group of
cohabiting individuals
produced by a
monogamous pair of
reproductives, usually
the primary founders
Extended family
colony: group of
cohabiting individuals
produced by multiple
inbred neotenic
reproductives
descended from the
original founding pair
Sex-Biased Alate Production
by Colonies
Another potential mechanism promoting out-
breeding is sex-biased alate production by
colonies, in which individual colonies in-
vest predominantly in alates of one sex (61).
Such bias may occur as a function of colony
breeding structure. Experimentally orphaned
colonies of Australian Coptotermes spp. that were
subsequently headed by inbreeding neotenics
produced almost exclusively males (72, 111).
Genetic analysis of swarming alates of C. for-
mosanus found that male alates in most swarm
aggregations were significantly more inbred
than females (57), a finding consistent with pre-
dominant male production in neotenic-headed
(inbred) colonies. One factor promoting female
alate production in outbred colonies in this
species could be sexual selection favoring het-
erozygous females during mate selection (55),
as mentioned above. In R. virginicus, DeHeer
and Vargo (28) inferred that female alates were
produced primarily in inbred colonies on the
basis of lower levels of heterozygosity compared
to males. The extent of sex-biased alate pro-
duction and its possible role in promoting out-
breeding in subterranean termites deserve fur-
ther study.
COLONY DEVELOPMENT
AND BREEDING STRUCTURE
After establishment by the founding pair,
colony growth is initially slow, reaching a pop-
ulation size after one year of about 30 to 50 in-
dividuals in the case of Reticulitermes spp. (130)
and 20 to 90 in C. formosanus (107, 122). During
this initial phase, the colony is a simple fam-
ily composed of a monogamous pair of repro-
ductives and their offspring. Eventually one or
both of the primary reproductives senesces or
dies, and these are replaced by neotenics, ei-
ther apterous or, more commonly, brachypter-
ous forms that develop from within the colony
(95, 130), producing an extended family colony.
The number of neotenics in these extended
family colonies can vary from a few to several
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ANRV363-EN54-20 ARI 23 October 2008 13:50
dozen, and these colonies can undergo several
generations of inbreeding. In addition to sim-
ple family and extended family colonies, it has
been assumed that colonies often fuse to create
genetically complex groups consisting of mixed
families (21, 87, 132).
Owing to the cryptic nesting habits of this
group, it has been difficult to conduct exten-
sive studies of colony breeding structure. How-
ever, this has changed with the application
of highly sensitive molecular genetic markers
(58), combined with population genetic model-
ing of subterranean termite breeding systems
(17, 132). The main approach to investigat-
ing colony breeding structure is to genotype
groups of foragers at numerous genetic loci us-
ing codominant markers, such as microsatellites
(27, 58, 136). The genotypes of the individuals
are then subjected to pedigree analysis to deter-
mine family structure.
Once the family structure of a colony is de-
termined, more detailed information about the
relatedness of reproductives, degree of inbreed-
ing within the colony, and the numbers of re-
productives within extended family colonies can
be inferred from the coefficients of inbreeding
and relatedness (17, 132). There is significant
variation in all aspects of colony breeding struc-
ture both within and among species (Table 2).
In most cases, colonies are either simple fam-
ilies or extended families, with simple families
more common in many populations.
Simple Family Colonies
Colony breeding structure has now been char-
acterized in populations of six species of Retic-
ulitermes, with four species represented by mul-
tiple populations (Table 2). In most species and
most populations, the majority of colonies—
often 75% or more—are simple families. One
major exception is the European species R. gras-
sei, in which simple families comprised a minor-
ity of colonies in all four populations studied,
with one population containing no simple fami-
lies at all. The other conspicuous exceptions are
(a) populations of R. flavipes in Massachusetts,
at the northern edge of the range of this species
where only about 25% of the colonies were sim-
ple families, and (b) populations of R. flavipes in
France, where this species was introduced and
no simple families have been found.
There is both inter- and intraspecific vari-
ation in the degree to which the kings and
queens heading simple family colonies are re-
lated. Colonies of R. flavipes,R. virginicus, and
R. hesperus appear to be headed by unrelated re-
productives, whereas the reproductives in sim-
ple family colonies of R. hageni and R. malletei
appear to be related (101, 138, 141), most likely
because primary reproductives often pair with
relatives during colony foundation (138). The
European species R. grassei exhibits variation
among populations, with closely related repro-
ductives in one French population and largely
unrelated reproductives in a Portuguese popu-
lation (Table 2).
Studies of Coptotermes have largely con-
cerned introduced populations of C. formosanus,
in which considerable variation in colony
breeding structure has been found (Table 2).
The proportion of simple families varies from
nearly 100% in two Japanese populations (139)
to no simple families present in a population
from the native range in southern China (54).
However, in six of nine C. formosanus popula-
tions studied to date, simple families were more
common than extended families. The degree
of relatedness between the kings and queens
heading simple families varies from essentially
zero in New Orleans to full siblings (r=
0.6) in one Japanese population (53, 139, 140).
In the only other Coptotermes species studied
to date, the Australian mound-building C. lac-
teus, all 39 colonies examined genetically (127)
were simple families headed by slightly related
reproductives.
Extended Family Colonies
Extended families can vary both in the numbers
of neotenics present, from a few to dozens, and
in the number of generations of inbreeding they
have undergone. Of particular importance in
inferring details regarding the breeding struc-
ture of extended families is the coefficient of
386 Vargo ·Husseneder
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Table 2 Summary of colony breeding structures in Reticulitermes spp. and Coptotermes spp. termites as inferred by
microsatellite markers except where noted
Simple families Extended families Mixed families
Species/Population
(N=no. colonies) Percent
Reproductives
relatedaPercent FICb
Inferred no.
neotenics Percent
Overall
FIT Reference(s)
Reticulitermes flavipes
Central North
Carolina
N=319
78.4% – 19.7% –0.209 <10 1.9% 0.052 (27, 101, 135,
136, 138)
Charleston, South
Carolina
N=18
72.2% – 22.2% –0.140 <10 5.6% 0.030 (141)
Eastern
Massachusettsc
N=22
27.3% – 59.1% 0.097 >100 13.6% 0.289 (17)
Central Tennesseec
N=48
NR NR NR 0.260dNR NR 0.680a(108, 132)
Paris, Franced
N=12
0% N/A 100% 0.032 >100 0% 0.386 (30)
Ol´
eron Island,
Francee
N=14
0% N/A 100% –0.001 >100 0% 0.168 (30)
Reticulitermes hageni
Raleigh, North
Carolina
N=15
86.7% ++ 13.3% –0.257 <10 0% 0.357 (101, 138)
Charleston, South
Carolina
N=21
95.2% +4.8% N/A <10 0% 0.140 (141)
Reticulitermes malleteif
Duke Forest, North
Carolina
N=13
53.8% +46.2% –0.257 <10 0% 0.190 (138)
Reticulitermes virginicus
Raleigh, North
Carolina
N=8
75.0% – 25.0% –0.332 <10 0% 0.037 (101, 135)
Charleston, South
Carolina
N=4
100% – 0% N/A N/A 0% –0.04 (141)
Reticulitermes hesperus
Northern California
N=30
73.3% – 26.7% –0.185 <10 0% 0.081 (23)
Reticulitermes grassei
Southwestern
France, population
A
N=24
0% N/A 100% 0.019 >100 0%h0.294 (26)
(Continued )
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Table 2 (Continued )
Simple families Extended families Mixed families
Species/Population
(N=no. colonies) Percent
Reproductives
relatedaPercent FICb
Inferred no.
neotenics Percent
Overall
FIT Reference(s)
Southwestern
France, population
B
N=15
26.7% ++ 73.3% –0.038 10–100 0%h0.306 (26)
Southwestern
France, population
C
N=32
43.7% +56.3% –0.113 <10 0%h0.210 (26)
Central Portugal
N=15
33.3% – 53.4%i–0.310 <10 13.3% –0.020 (97)
Coptotermes lacteus
Southern Australia
N=38
100% +0% N/A N/A 0% NR (127)
Coptotermes formosanus
New Orleans,
Louisianae
N=46
57.0% – 43.0% –0.147 <10 0% 0.159 (53, 56, 140)
Charleston, South
Carolinad
N=25
48.0% +52.0% –0.058 10–100g0% 0.139 (140)
Rutherford County,
North Carolinae
N=8
75.0% +25.0% –0.127 <10 0% 0.239 (140)
Kyushu, Japane
N=20
85.0% +15.0% 0.012 >100 0% 0.161 (139)
Fukue, Japane
N=10
100% ++ 0% N/A N/A 0% 0.461 (139)
Oahu, Hawaiie
N=19
36.8% +63.2% –0.10 <10 0% 0.32 (54)
Guangdong
Province, China
N=12
0% N/A 100% –0.14 <10 0% 0.18 (54)
a–, coefficient of relatedness (r) not significantly different from zero; +,0<r<0.25; ++,r>0.25.
bStrongly negative FIC (<–0.14) suggests low numbers of reproductively active neotenics (fewer than 10), whereas values close to zero suggest many
neotenics (10 to 100).
cAllozyme markers used to infer breeding structure.
dEstimated by Thorne et al. (132).
eIntroduced population.
fOriginally reported as the Duke Forest population of R. hageni.
gLow power to distinguish extended from mixed families.
hAuthors refer to extended families as pleometrotic families.
iMay exhibit a degree of assortative mating in some colonies.
NR, not reported.
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inbreeding in individuals relative to their
colony (FIC), a statistic that is especially sen-
sitive to the numbers of reproductives present
(17, 27, 29, 97, 132).
The FIC values for extended families from
a number of populations are given in Table 2
along with the inferred numbers of functional
neotenics. There was variation among pop-
ulations of the European species, R. gras-
sei, suggesting large numbers of neotenics in
some populations and low numbers in oth-
ers (Table 2). In North American Reticuliter-
mes species, extended families in most popu-
lations contained relatively few reproductives,
and these were likely the direct offspring of
the founding pair (17, 132). These conclusions
are strikingly similar to results from laboratory
colonies in which the reproductive composi-
tion was censused (79). Laboratory studies of
R. flavipes (42, 76) have shown that neoten-
ics may sometimes coexist alongside primary
reproductives. Husseneder et al. (51) found a
primary king together with 25 female neoten-
ics in the African subterranean termite Sche-
dorhinotermes lamanianus, demonstrating that
primary and neotenic reproductives of other
species do sometimes occur alongside each
other in the field.
A couple of populations are worth spe-
cial mention. First, colonies of R. flavipes in
France (previously called R. santonensis) differ
radically from those studied so far in the na-
tive range. Detailed studies of populations in
Paris and northwestern France (30) found only
highly inbred colonies headed by many neoten-
ics (Table 2). These invasive populations will
be discussed in more detail later. Second, an
older study of R. flavipes in central Tennessee
using allozymes (108) reported extremely high
levels of inbreeding (FIT =0.680), almost twice
as high as the next most inbred native popula-
tion (see Table 2). The reasons for the large dis-
crepancy between this population and the many
other populations studied are not known.
In introduced populations of C. formosanus,
the inferred numbers of reproductives in
extended family colonies vary considerably.
FIC:coefficient of
inbreeding in
individuals relative to
their colony
FIT:coefficient of
inbreeding in
individuals relative to
their population
Colonies in populations from New Orleans,
Louisiana; Charleston, South Carolina; and
Rutherford County, North Carolina, had lev-
els of inbreeding indicative of low numbers of
neotenics (<10) (2, 53, 140), whereas colonies
from Japan and Hawaii were more inbred, sug-
gesting higher numbers of reproductives (54,
139). Whether these differences are due to the
inherent genetic structure of introduced popu-
lations or are responses to local ecological con-
ditions is not known. Extensive studies of na-
tive populations of this species from mainland
China are needed to determine how the num-
ber of reproductives in extended family colonies
varies in natural environments and how these
numbers compare with introduced populations.
One sample of 12 colonies from a native popula-
tion in Guangdong Province consisted entirely
of extended families presumably headed by rel-
atively few neotenics (54). The inferred number
of neotenics in these colonies is consistent with
data from nest excavations in China (142), in
which the number of neotenics in colonies was
generally fewer than 20.
Within extended family colonies, genetic
substructuring can occur through a couple of
processes. First, the presence of spatially sepa-
rated groups of reproductives with little or no
interbreeding between them coupled with lim-
ited movement of workers from their natal nest
can lead to genetic differentiation within the
colony. In an expansive colony of C. formosanus,
Husseneder et al. (53) found evidence of sub-
structure among foragers feeding on monitor-
ing stations located 25 to 100 m apart. Similar
results were reported for a colony of the African
subterranean termite S. lamanianus (50). In a
large introduced colony of R. flavipes in France,
foragers occurring further apart were geneti-
cally more differentiated than those occurring
closer together (30).
Another process that can lead to differenti-
ation among foraging groups is kin-biased for-
aging. In S. lamanianus, groups of foragers col-
lected away from the nest were more closely
related than workers taken from the nest cen-
ter (62), which suggests that workers sorted
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Mixed-family colony:
group of cohabiting
individuals produced
by multiple unrelated
reproductives
themselves into kin groups while foraging. It
is not known whether genetic substructuring,
either through kin-biased sorting or as a re-
sult of spatially separated reproductive cen-
ters, is widespread in subterranean termites,
but it is likely to occur mainly in species
with expansive colonies. Studies of several
species, especially North American Reticuliter-
mes, show that colonies are often localized, so
opportunities for genetic substructuring within
colonies of these species are most likely limited
(27, 101, 141).
Geographic Variation
in Breeding Structure
Populations spanning much of the eastern
seaboard of the United States show strong cli-
nal variation in colony breeding structure in
R. flavipes, with a greater proportion of extended
family colonies and higher levels of inbreed-
ing in northern populations (137). Studies of
R. grassei in France and Portugal, although
more limited in scope, indicate a similar trend
in increasing levels of inbreeding from north
to south (Table 2) (26, 97). The apparent geo-
graphic variation in these species suggests that
colony breeding structure is responsive to local
ecological conditions, and that these conditions
vary in a gradual manner along latitudinal gradi-
ents. One of the big challenges in subterranean
termite biology will be to determine the ecolog-
ical factors that shape colony breeding struc-
ture, especially those factors that may select
against inbreeding. Studies in additional subter-
ranean termite species focusing on clinal varia-
tion in colony breeding structure similar to that
found in R. flavipes and R. grassei should prove
particularly fruitful.
Mixed-Family Colonies
and Colony Fusion
Among subterranean termites, mixed-family
colonies in the field have so far only been
demonstrated in R. flavipes (27, 29, 101, 138)
and R. grassei (97). Several mechanisms can
potentially lead to mixed families, but colony
fusion is the only mechanism that has been
documented in subterranean termites (27).
Pleometrotic association of multiple same-sex
reproductives is another means, but to date
this route has been found only in some termi-
tids (3, 43). Results of field (29) and laboratory
(37) studies indicate that the presence of multi-
ple unrelated groups of reproductives in fused
colonies of R. flavipes is generally rather short-
lived; over time reproduction in fused colonies
is usually restricted to individuals from just one
of the original source colonies.
The factors underlying colony fusion are not
clear. Matsuura & Nishida (87) proposed that
colonies with numerous nymphs preparing to
molt into alates would be more likely to accept
individuals from foreign colonies, but this hy-
pothesis has not been rigorously tested in the
field. In a study of mixed-family colonies in
North Carolina and South Carolina, DeHeer
& Vargo (29) showed that individuals origi-
nating from different families had identical or
nearly identical mtDNA haplotypes but were
unrelated at nuclear microsatellite loci. These
results suggest some maternally inherited fac-
tor underlying colony fusion, but the nature
of this factor is not known. Because mixed-
family colonies have low genetic relatedness,
and therefore lower inclusive fitness of colony
members, the factors influencing colony fusion,
including similarities in mtDNA haplotype, are
worthy of further study.
Colony Longevity, Breeding Structure,
and Effects of Inbreeding
The proportions of simple families in a pop-
ulation can provide insights into its age struc-
ture. Assuming that a population has reached a
stable age distribution, the presence of a high
proportion of simple family colonies, as we find
in most Reticulitermes spp. populations studied
to date, suggests that most colonies in these
populations do not survive past the death of
one of the primaries. The life span of pri-
mary reproductives in the field is not known
for any species, but in a laboratory study of
30 R. flavipes colonies, reproductives began to
390 Vargo ·Husseneder
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ANRV363-EN54-20 ARI 23 October 2008 13:50
die after 6 years but some were still alive af-
ter 11 years (78). Long-term demographic stud-
ies are needed to determine how long colonies
live with both primary reproductives present,
and how long they survive once neotenics are
produced.
Because relatively few colonies in many pop-
ulations of subterranean termites do not sur-
vive the death of the primary reproductives,
there may be a cost associated with reproduc-
tion by neotenics. The production of neotenics
appeared early in the evolution of the Isoptera
and is thought to confer many advantages (129).
Principal among these is that neotenic repro-
duction gives workers the option of differentiat-
ing into reproductives in their natal colony and
inheriting existing resources, thereby foregoing
the risks of embarking on mating flights (95,
116, 129). A major consequence of neotenic re-
production is elevated levels of inbreeding. The
possibility of inbreeding depression in subter-
ranean termites has received little attention to
date.
Recent results from dampwood and subter-
ranean termites give somewhat mixed views re-
garding the possible importance of inbreeding
depression in termites. Sibling founding pairs
of the dampwood termite, Zootermopsis angusti-
collis, survived better than pairs in which males
and females were unrelated (112). Similarly,
sibling founding pairs of C. formosanus had
higher survivorship than pairs of unrelated indi-
viduals, but the survivors in the latter group had
higher growth rates (36). Other studies have
shown a cost to inbreeding in termites through
increased susceptibility to some diseases (19)
and reduced survivorship of colonies founded
by related primary reproductives in the field
(28). In addition, some studies report an effect
of inbreeding (77) or numbers of reproductives
(54) on worker size in subterranean termites,
although possible fitness consequences of these
differences are unknown. The costs and benefits
associated with neotenic reproduction should
be addressed in future research, including both
ecological factors related to breeding structure
and potential physiological and behavioral con-
sequences of inbreeding.
Mark-release-
recapture (MRR):
method used to delimit
colony-foraging areas
and sometimes for
estimating colony
population size
Colony Reproduction by Budding
Although it has often been assumed that subter-
ranean termite colonies frequently reproduce
by budding (95, 116, 130, 132), in which a por-
tion of a colony splits off or becomes isolated
from the natal nest and functions as an indepen-
dent colony, results from a number of studies on
several species do not support this view. If com-
mon, budding should lead to high population
viscosity in which colonies located near each
other are genetically more similar than colonies
further apart. Yet, several fine-scale studies of
Reticulitermes species (17, 26, 27, 136, 138, 141)
and C. formosanus (53, 140) have failed to find
such a relationship. However, Husseneder et al.
(50) did find evidence for budding in a pop-
ulation of S. lamanianus, suggesting that this
mode of reproduction may occur in some sub-
terranean termite species.
Parthenogenetic Reproduction
Parthenogenetic reproduction occurs in the
laboratory in R. virginicus (48) and R. sper-
atus (86). In the latter species, the mecha-
nism of parthenogenetic reproduction has been
identified (86). However, to date there are
no clear cases of parthenogenetic colonies re-
ported from field populations of any species, so
the significance of this mode of reproduction
under natural conditions remains uncertain.
COLONY-FORAGING AREA
AND POPULATION DENSITY
The application of the mark-release-recapture
(MRR) technique to connect spatially separated
groups of foragers to the same colony (69)
was an important advance in delimiting colony-
foraging areas and has been used extensively
over the past three decades (122, 130). The use
of molecular markers, such as highly variable
microsatellite markers, offers many advantages
over MRR for assigning workers to colonies, for
determining the limits of colony-foraging areas,
and for determining the numbers of colonies
in an area (101). Chief among the advantages
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Table 3 Foraging ranges of Reticulitermes spp. and Coptotermes spp. as determined by genetic markers
Species Location (N) Linear foraging distance (m)aForaging area (m2) Reference(s)
Reticulitermes flavipes North Carolina (169) 1–26 1–174 (101)
North Carolina (122)b1–85 NR (135, 136, 138)
North Carolina (29) 1–12 1–96 (27)
South Carolina (18)b1NR (141)
Massachusetts (22) 1–76 1–800 (17)
France (26) 1–320 1–90,000 (30)
R. hageni North Carolina (15) 1–11 1–21 (27, 101)
North Carolina (3)b1 1 (138)
South Carolina (21)b1NR (141)
R. malleteicNorth Carolina (13)b1 1 (138)
R. virginicus North Carolina (8) 1–50 1–318 (27, 101)
North Carolina (4)b1–122 NR (135, 138)
South Carolina (4)b1–125 NR (141)
R. hesperusdCalifornia (30) 1–15 NR (23)
R. grassei France (71) 1–70 NR (26)
Portugal (15) 1–10 NR (97)
Coptotermes formosanus Louisiana (13)e40–175 83–1,634 (90, 91)
North Carolina, South
Carolina, Louisiana (115)b
1–144 NR (2, 53, 56, 140)
aColonies found in only one station or feeding site were assumed to have a foraging range of 1 m.
bStudy not specifically designed to map colony foraging areas.
cOriginally reported as the Duke Forest population of R. hageni.
dSpecies was not specified but occurs in area where R. hesperus is common.
eUsed both mark-release-recapture and genetic methods to delimit colony foraging areas.
N, number of colonies studied; NR, not reported.
of using genetic markers are (a) studies can be
done faster with less effort, (b) far fewer foragers
are required for determining colony identity,
and (c) studies can be conducted over a period
of years without losing the ability to identify
colonies. Thus, more colonies can be studied
over a larger area and over a period of months
or years, allowing for extensive long-term stud-
ies of colony dynamics and colony-level effects
of termiticide treatments.
Colony Foraging Area
Here, we summarize what has been learned
about the foraging ranges of Reticulitermes
and Coptotermes since 2001 using genetic
markers (Table 3). The picture has changed
significantly since the last reviews done more
than a decade ago, before the application of
molecular methods (122, 130). For example, it
now appears that small, localized colonies are
the norm for many Reticulitermes species. Con-
spicuous exceptions to small foraging areas in
Reticulitermes spp. are colonies of R. virginicus,
which frequently forage over 100 linear meters
(135, 138, 141), and introduced populations of
R. flavipes in France that can cover thousands
of square meters (30). Similarly, colonies of
C. formosanus in introduced areas are often
expansive, extending >100 linear meters
(90, 140).
It has been generally assumed that the
large worker populations and expansive forag-
ing ranges attained by colonies of some sub-
terranean termite species can only be achieved
by the reproductive output of multiple female
392 Vargo ·Husseneder
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ANRV363-EN54-20 ARI 23 October 2008 13:50
neotenic reproductives (42, 130). Although the
very large colonies of R. flavipes in France,
which are among the largest subterranean ter-
mite colonies known, are headed by numer-
ous neotenics (30), these are introduced pop-
ulations and do not appear to be representative
of natural populations. Studies of natural pop-
ulations of R. flavipes and R. virginicus show that
colonies headed by a single queen (simple fam-
ily) do not differ in the size of their foraging
areas from colonies headed by multiple queens
(extended families) (27, 101, 138, 141), suggest-
ing that colony family structure does not influ-
ence the size of the worker population. Similar
results reported for an introduced population
of C. formosanus suggest that the presence of
multiple queens in colonies does not necessar-
ily allow for larger colony size in this species ei-
ther (53). Support for the lack of larger colony
size in colonies headed by neotenics also comes
from a recent laboratory study by Long et al.
(78). There was no difference in colony size
(either all individuals or numbers of work-
ers) between laboratory-established colonies
containing their original primary reproductive
pairs and colonies headed by neotenics (78).
Population Densities
Data from molecular studies in which individual
colonies are identified are now accumulating,
showing that colony densities can be high in
some areas. A study of forests in central North
Carolina (27) found densities of up to 300 Reti-
culitermes spp. colonies per hectare, consisting
overwhelmingly of R. flavipes; these are among
the highest densities recorded for any termite
species in any ecosystem (73). Colony densities
can be high in urban environments as well. On
residential properties in North Carolina, Par-
man and Vargo (101) found an average popu-
lation density of 62 colonies per hectare, with
a maximum of 185 colonies per hectare, over
90% of which were R. flavipes.
Relative abundance is likely to vary with
habitat and geographic location. In an undis-
turbed site in Massachusetts, near the far north-
ern edge of the range of R. flavipes, Bulmer et al.
(17) found a much lower population density
than that found in North Carolina—only about
seven colonies per hectare. The lower colony
density in this northern population is associated
with a higher frequency of inbred colonies.
Colony density of C. formosanus in a park
in New Orleans was 1.5 colonies per hectare
(53, 90). This is similar to the 1.0 colonies per
hectare for this species reported for a park in
Charleston (140). The lower colony densities
of this species compared with Reticulitermes spp.
are consistent with the larger colonies it forms,
with foraging ranges often exceeding 100 linear
meters (90, 122, 140).
Intraspecific interactions among colonies
undoubtedly play an important role in deter-
mining colony density. Recent studies show
that colonies of R. flavipes and C. formosanus
in relatively undisturbed sites appear to form
territories that are remarkably stable over a pe-
riod of years (27, 90) with little or no infringe-
ment by neighboring colonies. Further evi-
dence supporting territorial interactions comes
from studies in which colonies were removed by
baiting. In areas of relatively high population
density, the territories of eliminated colonies
are quickly invaded by neighboring colonies in
both R. flavipes (135) and C. formosanus (56, 91).
The apparently weak intraspecific agonism
displayed by R. flavipes (18, 104) and by intro-
duced populations of C. formosanus (52, 89, 121)
suggests that some mechanism other than ag-
gressive behavior is responsible for intraspe-
cific territoriality, at least in some cases. This
is in marked contrast to many termite species
that show strong intraspecific agonism (131),
including the African subterranean termite
S. lamanianus (50).
Use of Genetic Markers for Applied
Studies in the Field
The use of molecular markers to identify large
numbers of individual colonies and track them
over time allows for more rigorous field evalu-
ations of insecticide treatments than was pre-
viously possible (35, 56, 135). By comparing
the genotypic profiles of colonies present before
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ANRV363-EN54-20 ARI 23 October 2008 13:50
and after treatment, we can determine whether
termites that reinfest treated areas or bait
stations are remnants of targeted colonies, in-
vading neighboring colonies, or previously un-
detected hidden colonies. For example, stud-
ies of C. formosanus found that foraging areas
of colonies eliminated by baiting with chitinase
inhibitors were often reinvaded, and that the
source of reinfesting termites was either known
neighboring colonies or hidden colonies (56,
91). Similar results were obtained in baiting
studies with Reticulitermes spp. (135). Although
reinfestation after treatment is common in ar-
eas with high colony density, reinfestation rates
decline with repeated treatment (56, 135), indi-
cating such treatments have a population-level
effect, at least on a small scale.
The use of genetic markers in applied studies
also allows us to compare the breeding structure
of colonies present before and after treatment
to determine whether family type or the de-
gree of inbreeding influences treatment success
(56). To date, studies have indicated that breed-
ing structure of colonies does not affect treat-
ment success, because all treated colonies of
both Reticulitermes and Coptotermes were elimi-
nated regardless of family type (56, 135). In one
study, new colonies appearing within treated
areas were primarily simple families, whereas
a disproportionate number of hidden C. for-
mosanus colonies taking over vacated foraging
areas were extended families (56), suggesting
that simple families and extended families dif-
fer in their response to vacated territories.
INVASION BIOLOGY OF
SUBTERRANEAN TERMITES
A number of termites have been introduced and
have become established in new locations, but
in only a few cases can these be considered truly
invasive in the sense that they have significant
ecological and economic impact in their intro-
duced ranges. Termites that have most often
been introduced and have become established
in new areas are drywood termites (Kalotermi-
tidae) and subterranean termites (Rhinotermi-
tidae) (38). Among the subterranean termites,
species of Coptotermes and Reticulitermes are the
most common and the most destructive. The
Formosan subterranean termite, C. formosanus,
is considered among the 100 worst invasive
species (40). Coptotermes gestroi has been intro-
duced into several places around the world (60).
R. flavipes is well established in Europe (11) and
South America (123).
The use of molecular markers can provide
powerful tools for identifying the source pop-
ulations of introduced species (83). DNA se-
quence data established that populations of
R. santonensis in France and South America were
introduced populations of R. flavipes (11, 123),
a native of eastern and central United States. In
addition, R. flavipes has been introduced into
areas of North America north of the native
range (34, 65). The precise locations of pop-
ulations within the United States serving as
the sources of introduced populations have not
been identified. Attempts have been made to
identify the source populations and routes of
introduction of invasive populations of C. for-
mosanus (12) and C. gestroi (60), but small sam-
ple sizes and low variation in the mitochondrial
genes used in these studies render conclusions
from this work tentative at best (94). Studies us-
ing highly variable markers, such as microsatel-
lites, should provide greater power in identify-
ing likely source populations (25, 105) and the
routes of introduction of invasive subterranean
termites.
A major area of inquiry in invasion biology
concerns the factors that make some species
successful invaders. The attributes of success-
ful ant invaders have received considerable at-
tention (47). Among the most prominent fea-
tures of many invasive ants is the breakdown of
colony boundaries resulting in large unicolo-
nial populations that become ecologically dom-
inant within introduced ranges. The behavioral
changes in introduced populations most likely
result from reduced genetic variation associated
with introduction events, resulting in a homog-
enization of the cues used by ants to distinguish
nestmates. This reduced ability to recognize
394 Vargo ·Husseneder
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ANRV363-EN54-20 ARI 23 October 2008 13:50
nestmates in turn leads to fusion of colonies into
large aggregations (133).
Do invasive subterranean termites share any
of the unicolonial characteristics of invasive
ants? The evidence to date shows a mixed pic-
ture. French populations of R. flavipes exhibit
reduced genetic variation compared with native
populations at both microsatellite loci (30, 136,
141) and mitochondrial genes (11). The popu-
lations in France form exclusively large, highly
polygamous extended family colonies (30), and
this appears to be true of populations intro-
duced into North America as well (34, 41). This
is in contrast to colonies in the native range
that tend to be primarily simple families with
localized foraging areas. Thus, there are some
intriguing parallels between these introduced
populations of R. flavipes and those of some in-
vasive ants. It is of interest to know whether
other introduced populations of R. flavipes, such
as those in Chile (123), also form expansive,
highly polygamous colonies.
Studies of introduced populations of
C. formosanus also show reduced genetic
variation compared with native populations
at microsatellite loci (53, 54, 139, 140). De-
spite little or no agonistic behavior among
colonies in the introduced range (52, 89,
121), invasive populations of this species do
not form large, unicolonial societies. Rather,
they form genetically distinct colonies that
are either simple families or secondarily
polygamous (extended) families derived from
simple families. In contrast, the dozen colonies
characterized to date from the native range
were all polygamous (54). Thus, although the
data are still limited, it appears that introduced
populations of C. formosanus are not charac-
terized by higher numbers of reproductives
than native populations. This may not be
true of all Coptotermes spp., however. Three
species of mound-building Coptotermes native
to Australia, C. lacteus,C. acinaciformis, and
C. frenchi, all form almost exclusively simple
families in Australia but colonies in New
Zealand, where they have been introduced,
contain many neotenics (71).
CONCLUSIONS
There is growing interest among scientists in
the biology of subterranean termites. Molec-
ular techniques have begun to make signifi-
cant contributions to nearly all areas of sub-
terranean biology. Progress in some areas, such
as systematics and taxonomy, the molecular ba-
sis of caste differentiation, and colony breeding
structure, will largely depend on continued ap-
plication of molecular methods. In other areas,
such as foraging ecology, population dynam-
ics, and community ecology, molecular tech-
niques can provide important information on
colony identity, allowing for much more de-
tailed and comprehensive studies than would
otherwise be possible. Recent molecular eco-
logical studies are already changing long-held
views about the breeding structure and dynam-
ics of subterranean termite colonies. In addi-
tion, the use of molecular markers is playing
an increasingly important role in applied stud-
ies to assess colony-level effects of termiticide
treatments in the field.
Although molecular techniques will grow
increasingly important in studies of subter-
ranean termite biology and management, the
results generated by these methods will have
greatest utility as part of a multidisciplinary
approach. For example, a more complete
understanding of the mechanisms regulating
caste differentiation will involve integrating
molecular tools with physiological methods,
chemical ecological approaches, and behav-
ioral studies. Molecular genetic markers have
proven invaluable for elucidating colony
breeding structure and how it varies within and
among species. But understanding the factors
underlying this variation will require ecological
studies of the biotic and abiotic factors that
shape colony breeding structure. Studies of
colony-colony dynamics and relative species
abundance will need to combine molecular
markers for colony identifications with ecolog-
ical, behavioral, and demographic approaches
to understand the factors determining popu-
lation dynamics and species richness. Thus, in
our view, the future of subterranean termite
www.annualreviews.org •Biology of Subterranean Termites 395
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ANRV363-EN54-20 ARI 23 October 2008 13:50
biology is one of an interdisciplinary approach,
with molecular techniques occupying a central
position. The development of additional
tools, especially in genomics and proteomics,
will lead to many new possibilities. We can
look forward to rapid advances in all areas of
subterranean termite biology in the coming
years.
SUMMARY POINTS
1. Coptotermes and Reticulitermes are two of the most species-rich genera of lower termites,
but they are in need of careful taxonomic revision using both morphological and molec-
ular methods.
2. Recent studies have provided important insights into the molecular processes under-
lying caste differentiation, especially in soldier development in Reticulitermes, in which
hexamerins play a key role in modulating the activity of JH.
3 Although it is well known that termites often inbreed, recent evidence suggests that
inbreeding depression may occur in some subterranean termite species with possible
consequences for mate choice and colony breeding structure.
4. Dispersal and sex-biased alate production can promote outbreeding in some subterranean
termite species, but to date there is no evidence for kin discrimination during partner
selection.
5. Molecular markers provide a powerful tool for inferring the breeding structure of sub-
terranean termite colonies. There is considerable variation within and among species in
the relative frequencies of simple and extended family colonies, but many populations
are composed of mainly simple families. Mixed-family colonies, which can form through
colony fusion, appear to be rare.
6. Colonies of most species of Reticulitermes studied to date have fairly limited foraging
ranges, usually less than 10 linear meters, and colony densities can be quite high, reach-
ing up to 300 per hectare in some populations of R. flavipes. Colonies of introduced
populations of R. flavipes are a notable exception, with foraging ranges up to 100 m or
more, rivaling the expansive colonies often formed by C. formosanus.
7. Colonies of Reticulitermes and Coptotermes appear to be territorial with well-established
boundaries, but the mechanisms by which these boundaries are established and main-
tained have yet to be identified.
8. Species of Reticulitermes and Coptotermes are among the most important and destructive
invasive termite species. Current studies are using genetic markers to identify source
populations and to investigate the factors underlying their invasion success.
DISCLOSURE STATEMENT
The authors are not aware of any biases that might be perceived as affecting the objectivity of this
review.
ACKNOWLEDGMENTS
We thank Paul Labadie and Dawn Simms for assistance in preparing the manuscript. Warren
Booth provided helpful comments. This work was partially supported by grants from the USDA
396 Vargo ·Husseneder
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ANRV363-EN54-20 ARI 23 October 2008 13:50
National Research Initiative Competitive Grants Program (2004-35302-14880) to Coby Schal and
ELV; by the W.M. Keck Center for Behavioral Biology at North Carolina State University; by
USDA-ARS Specific Cooperative Agreements to CH; by grants provided by the State of Louisiana
to CH; by grants from USDA T-STAR to J. Kenneth Grace, CH, and ELV; and by a grant from
the National Geographic Society to ELV and CH.
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