Worldwide invasion by the little ﬁre ant: routes
of introduction and eco-evolutionary pathways
Jacques H. C. Delabie,
Alexander S. Mikheyev,
and Arnaud Estoup
1 INRA, UMR CBGP (INRA/IRD/Cirad/Montpellier SupAgro), Montferrier-sur-Lez cedex, France
de Toulouse, UPS, EDB (Laboratoire Evolution et Diversite
Biologique), Toulouse, France
3 CNRS, EDB (Laboratoire Evolution et Diversite
Biologique), Toulouse, France
rio de Mirmecologia, CEPEC-CEPLAC & UESC, Itabuna, Bahia, Brazil
5 Department of Zoology, Tel-Aviv University, Tel-Aviv, Israel
partement de biologie des organismes animaux, Faculte
des sciences de l’universite
de Douala, Douala, Cameroun
7 Institut de Recherche sur la Biologie de l’Insecte, UMR CNRS 6035, Faculte
des Sciences et Techniques, Tours, France
8 Laboratoire d’Ethologie Expe
rimentale et Compare
e, CNRS UMR 7153, Universite
Paris 13, Villetaneuse, France
9 Department of Biology, University of San Diego, San Diego, CA, USA
10 Section of Integrative Biology, University of Texas, Austin, TX, USA
11 Biologie I, Universita
t Regensburg, Regensburg, Germany
Biological invasions are recognized as a major component
of global change (Vitousek et al. 1997). The successful
establishment and spread of species across previously
unoccupied habitats has been shown to cause biodiversity
declines (e.g. Clavero and Garcia-Berthou 2005), to
disrupt ecosystems functions (e.g. Crooks 2002) and to
incur severe socio-economic losses around the World
(e.g. Shogren and Tschirhart 2005). The role of human
activity has become a primary driver in the current dis-
placement of species at the global scale (McKinney and
Lockwood 1999; Foley et al. 2005). When displaced, spe-
cies are introduced in new environments where they
probably lack speciﬁc adaptations, and may also undergo
bottleneck events (Sakai et al. 2001). Invasive species,
which thrive in their introduced environment, thus over-
come this hypothetical lack of adaptation, despite a
biological invasion, introduction routes,
parthenogenesis, reproduction system,
J. Foucaud, INRA, UMR CBGP (INRA/IRD/
Cirad/Montpellier SupAgro), Campus
international de Baillarguet, CS 30016,
F-34988 Montferrier-sur-Lez cedex, France.
Tel.: +33 4 99 62 33 46;
fax: 33 4 99 62 33 45;
Received: 8 December 2009
Accepted: 24 December 2009
First published online: 2 February 2010
Biological invasions are generally thought to occur after human aided migra-
tion to a new range. However, human activities prior to migration may also
play a role. We studied here the evolutionary genetics of introduced popula-
tions of the invasive ant Wasmannia auropunctata at a worldwide scale. Using
microsatellite markers, we reconstructed the main routes of introduction of the
species. We found three main routes of introduction, each of them strongly
associated to human history and trading routes. We also demonstrate the over-
whelming occurrence of male and female clonality in introduced populations
of W. auropunctata, and suggest that this particular reproduction system is
under selection in human-modiﬁed habitats. Together with previous researches
focused on native populations, our results suggest that invasive clonal popula-
tions may have evolved within human modiﬁed habitats in the native range,
and spread further from there. The evolutionarily most parsimonious scenario
for the emergence of invasive populations of the little ﬁre ant might thus be a
two-step process. The W. auropunctata case illustrates the central role of
humans in biological change, not only due to changes in migration patterns,
but also in selective pressures over species.
Evolutionary Applications ISSN 1752-4571
ª 2010 Blackwell Publishing Ltd 3 (2010) 363–374 363
probable low size and genetic variability of the introduced
propagule. Some authors therefore argue that biological
invasions are paradoxical events (Sax and Brown 2000;
Frankham 2005a). However, recent studies refute this
‘paradoxical’ vision of bioinvasions, mostly through the
demonstration of high propagule pressure and main-
tained, or even increased, genetic variability in the intro-
duced populations (Kolbe et al. 2004; Lavergne and
Molofsky 2007; Roman and Darling 2007; Dlugosch and
Hays 2008; Facon et al. 2008).
Five ant species appear in the list of the 100 world’s
worst invasive organisms (Lowe et al. 2000), and these
ant species have long been recognized to pose important
threats to biodiversity and human activities (Holway et al.
2002). Our study focuses on one of the least studied of
these particularly harmful invasive species, the little ﬁre
ant, Wasmannia auropunctata (Roger, 1863) (Formicidae:
Myrmicinae). This species originates from Central and
South America and is successfully spreading over the
World tropics since the beginning of the last century. Its
introduced range now encompasses many Caribbean
islands, Florida, several West-African countries, and a
large number of Paciﬁc islands (Wetterer and Porter
2003). It also recently established populations in the Med-
iterranean zone, in Israel, which is raising concerns about
its potential distribution range outside the tropics
(Vonshak et al. 2009b).
Previous studies demonstrated that two types of popu-
lations coexist within the native range of W. auropunctata
(Foucaud et al. 2009b; Orivel et al. 2009). In French Gui-
ana, natural forest habitats, and especially ﬂoodplains
along creeks, are occupied by low density, mostly sexually
reproducing populations. On the contrary, human-
disturbed habitats of the native range are generally occu-
pied by high density, dominant, populations (see Orivel
et al. 2009; Foucaud et al. 2009b for details). These latter
populations generally display an extraordinary ‘clonal’
reproduction system, where males are produced clonally,
female queens are parthenogens and workers are pro-
duced sexually (see Fig. S1; Fournier et al. 2005a). These
clonal populations also display a speciﬁc mating pattern,
where the mated male and female tend to harbor more
divergent genotypes than in sexually reproducing popula-
tions (Foucaud et al. 2009b). The sexually produced
worker offspring of these clonal couples is therefore
highly heterozygous. This particular genetic architecture
may be selected for in native human-disturbed habitats,
and may provide the opportunity to invade other
human-disturbed areas (Foucaud et al. 2009b).
In agreement with this, Foucaud et al. (2006) hypothe-
sized that the introduced populations of W. auropunctata
originated from the dominant, clonally reproducing pop-
ulations of the native range. This hypothesis is, however,
based on the study of a single introduction area, New
Caledonia (Foucaud et al. 2006). A ﬁrst attempt of bio-
geographical study of native and introduced populations
of W. auropunctata invasion has recently been completed
(Mikheyev and Mueller 2007). Using a single mitochon-
drial region (between cytochrome oxidase subunits I and
II), Mikheyev & Mueller provided useful insights into the
species biogeography, but the low level of variation and
the mode of inheritance of the markers used did not
make it possible to address the evolutionary processes at
play during the invasion.
The present study, which is based on an extensive world-
wide set of molecular data obtained at 12 microsatellite
loci, aimed at answering two main questions. First, what
are the main routes of introduction of W. auropunctata
around the globe? Second, what evolutionary processes
could have enabled some W. auropunctata populations to
invade remote areas? To address both questions, we deci-
phered the reproduction system and genotypic patterns of
introduced populations, and compared these data with
data gathered from previous studies focusing on the native
range of the species (Foucaud et al. 2009b). This, in turn,
enabled us to construct a parsimonious scenario for the
worldwide invasion of W. auropunctata.
Field work was conducted in 16 countries belonging to
the introduced range of W. auropunctata (Fig. 1; Table 1).
A total of 251 nests (i.e. an aggregation of workers, brood
and/or queens within a woodstick, under stones or
between dead leaves) belonging to 60 sites of the intro-
duced range of W. auropunctata were collected from 1997
to 2007. The number of collected nests per site varied
from one to 25 nests (Mean ± SD: 5 ± 4 nests). For most
of the nests (except Dominican, Cuban, Galapagos and
Cocos Island nests), a large number of workers and most
if not all of the reproductives were collected. The distance
between sampled nests was always larger than two meters,
to avoid sampling neighboring nests that most probably
exchange workers and hence underestimating the genetic
diversity within the sampled sites. Most of the samples
(140 nests from 15 countries) were speciﬁcally collected
for the present study. The Gabonese, Hawaiian and
Floridian samples are different from the samples analyzed
in Mikheyev et al. (2009). The New Caledonian and
Israeli samples (82 and 29 nests, respectively) were used
in previous genetic studies (Foucaud et al. 2006 and Von-
shak et al. 2009a, respectively). For addressing some ques-
tions, we also used data from previously published
population samples collected within the native range of
W. auropunctata (Foucaud et al. 2007, 2009b).
Worldwide invasion by W. auropunctata Foucaud et al.
364 ª 2010 Blackwell Publishing Ltd 3 (2010) 363–374
Figure 1 Routes of introduction of Wasmannia auropunctata. Note: Colored dots represent genetically distinct introduced clonal populations.
The dark green area represents the native range of W. auropunctata (Wetterer and Porter 2003), and black stars represent areas where popula-
tions from the native range have been sampled. The code letter for each introduced country is given in Table 1. Estimated dates of introduction
are indicated between brackets when available (see Table S1 for detailed references).
Table 1. Number of sampled nests and genotyped queens, males and workers, for each surveyed country.
Number of genotyped individuals
Queens Males Workers
Native Brazil B 66 250 135 527 Foucaud et al. 2009b
Native French Guiana FG 103 255 210 1107 Foucaud et al. 2009b
Native Costa Rica CR 8 25 6 63 This study
Total 177 530 351 1697
Introduced Cameroon Ca 55 196 79 250 This study
Introduced Gabon Ga 19 59 45 150 This study
Introduced Israel Is 29 56 44 229 Vonshak et al. 2009a
Introduced Florida FL 11 26 8 88 This study
Introduced Cuba Cu 2 5 0 23 This study
Introduced Guadeloupe G 10 2 0 75 This study
Introduced Dominican Republic DR 1 0 0 8 This study
Introduced Dominica DR 1 0 0 8 This study
Introduced Cocos Island Ci 1 2 0 7 This study
Introduced Galapagos Islands Gi 1 0 0 8 This study
Introduced New Caledonia NC 82 580 208 702 Foucaud et al. 2006
Introduced Tahiti T 9 69 45 71 This study
Introduced Hawaii H 9 16 0 71 This study
Introduced Vanuatu V 10 18 2 71 This study
Introduced Australia A 7 14 10 54 This study
Introduced Papua New Guinea P 3 4 0 23 This study
Introduced Solomons S 1 13 0 32 This study
Total 251 1060 441 1870
Foucaud et al. Worldwide invasion by W. auropunctata
ª 2010 Blackwell Publishing Ltd 3 (2010) 363–374 365
The microsatellite genotyping was carried out as described
in Foucaud et al. (2006). Brieﬂy, for each sampled nest,
DNA was extracted from at least seven workers and most
if not all collected reproductives. Our microsatellite geno-
typing data set includes 3371 individuals collected in the
introduced range of W. auropunctata, genotyped at 12
microsatellite loci (Fournier et al. 2005b). For certain
comparisons, we additionally used another microsatellite
genotyping data set including 2578 individuals from the
native range of W. auropunctata, genotyped at 12 micro-
satellite loci (Table 1). This latter microsatellite data set
corresponds to that published in recent studies focusing
on native populations of W. auropunctata (Foucaud et al.
2009b), except for eight additional nests collected in
Costa Rica in 1997.
Reproduction system and relationships between
We characterized the reproductive systems and the rela-
tionships between genotypes by investigating individual
microsatellite genotypes visually and using two programs
we developed in the Pascal object programming language
(inquiries about details of the programs should be sent
to the corresponding author). The ﬁrst program was
used to identify clones (i.e. identical multilocus geno-
types) in a given sample of genotypes. The second pro-
gram was used to construct dendrograms from
individual genotypes (queens, males or workers) using
the Neighbor-Joining algorithm (Saitou and Nei 1987).
The genetic distance used to construct the dendrograms
was a variant of Chakraborty and Jin’s allele-shared
distance (Chakraborty and Jin 1993), as deﬁned in
Fournier et al. (2005a).
The identiﬁcation of the main routes of introduction
turned out to be relatively simple due to the introduc-
tion of almost entirely clonal queen and male genotypes
in each invaded area (see Results section). In particular,
we could directly assess the relationships between two
areas when they shared a common queen and/or male
clonal genotype. We considered two genotypes to be clo-
nal when they shared identical multilocus genotypes at
12 microsatellite loci, or when they differed either (i) by
only one dinucleotide repeat at one of the 12 genotyped
loci (as this pattern is likely to correspond to one muta-
tional event at a microsatellite locus) or (ii) by homozy-
gosity for one allele at a single heterozygous locus of the
clonal queen genotype (as this pattern probably corre-
sponds to a recombination or gene conversion event
during thelytoky; Foucaud et al. 2006). The genotypes
used to infer introduction routes were either the geno-
types of the males and queens collected in the ﬁeld, or
the genotypes of queens and males inferred from the
genotypes of collected workers (cf. workers are sexually
produced; Fournier et al. 2005a; Foucaud et al. 2006,
2007, 2009a). The ‘direction’ of the identiﬁed routes of
introduction was assessed by the estimated dates of
introduction in the given countries (i.e. from the oldest
to the most recently invaded country). Historical
information regarding dates of introduction of W. auro-
punctata invasion was gathered from Wetterer and Por-
ter (2003) and from various experts and local people
(see Fig. 1 and Table S1 for details).
Previous studies that focused on the native populations
of W. auropunctata found that clonal couples (i.e. male/
queen mating pairs) differed signiﬁcantly from sexual
couples regarding their heterozygosity and difference in
microsatellite allelic size (see below for deﬁnitions;
Foucaud et al. 2009b). Both statistics were signiﬁcantly
higher in clonal couples, indicating a trend for out-
breeding in these native populations (i.e. mating with
genetically distant individuals). These clonal mating pairs
result in signiﬁcantly more heterozygous workers in clo-
nal populations than sexual populations in the native
range of W. auropunctata. We here investigated the same
statistics in the introduced populations of the species.
The differences between the queen and male genotypes
of a given couple were assessed using a personal pro-
gram that computes basic population genetic statistics
(i.e. observed heterozygosity and mean difference in
allele size within and between multilocus genotypes).
Within-individual heterozygosity, Ho
, was computed as
the number of loci of an individual genotype showing
different alleles. Heterozygosity of a queen-male couple,
, was computed as the mean number of times the
male allele was different from each queen allele at a
given locus. Within-individual difference in allelic size,
, was computed as the difference in base pairs
between the two alleles at a given locus of a single indi-
vidual genotype. Difference in allelic size of a queen-
male couple, DS
, was computed as the mean difference
between the male allele and the two queen alleles at a
given locus. Because microsatellite sequences mutate
under a stepwise model (Estoup et al. 2002), the differ-
ences in allele size between two microsatellite DNA cop-
ies measured either within or between individuals is
related to the coalescence time and hence the level of
divergence between the two compared genomes. Ho and
DS statistics were computed for every locus, and we cal-
culated their means for every population, nested in a
single ‘type’ of population (three types: Native Sexual,
Worldwide invasion by W. auropunctata Foucaud et al.
366 ª 2010 Blackwell Publishing Ltd 3 (2010) 363–374
Native Clonal, Introduced Clonal; see Results section).
We then tested for statistical differences in mean Ho
and DS values for couples or workers: (i) between all
three types of populations using a non-parametrical
Friedman test, and (ii) between each pair of popula-
tions’ type using non-parametrical Wilcoxon sign rank
tests. We used loci as statistical units for all statistical
Reproduction system of introduced populations
The ﬁrst result of our study is that most if not all intro-
duced populations of W. auropunctata are reproducing
clonally. All the 110 nests where both queens and males
were collected showed direct proofs of clonal reproduc-
tion by both queens and males (i.e. groups of identical
queen genotypes and groups of identical male genotypes).
One hundred and two of the 103 nests where only queens
were collected provided direct proof of clonal reproduc-
tion by queens (i.e. groups of identical queen genotypes).
In all those nests, males were directly or indirectly shown
to reproduce clonally (i.e. male genotypes inferred from
queens’ spermathecal contents or from workers were
identical to known clonal male genotypes, respectively).
Thirty-four of the 38 nests that lacked reproductives at
the time of collection provided indirect proof of clonal
reproduction by both queens and males (i.e. inferred
queen genotypes identical to known clonal queen
genotypes and inferred male genotypes identical to known
clonal male genotypes). It was not possible to determine
the type of reproduction system for only ﬁve of the 251
nests collected in the introduced range of W. auropuncta-
ta (three in Gabon, one in Guadeloupe and one in Flor-
ida). In those nests, the sampled or inferred genotypes of
reproductives were neither identical nor close to known
clonal genotypes. Furthermore, those nests were geneti-
cally monogynous and monoandrous. Hence, the male
and queen of these nests could have reproduced sexually
or clonally. Altogether, the proportion of nests sampled
in the introduced range of W. auropunctata where both
male and queens reproduce clonally (i.e. clonal nests) was
over 98%. We did not ﬁnd any introduced nest reproduc-
ing uniquely via sexuality, as was found in the native
range of the species, where entire populations (composed
of many nests) are either sexual or clonal (Foucaud et al.
2009b). In this previous study of the native range, we
found around one-third of sampled nests to be exclusively
sexual, which contrasts with the ﬁgure of 98% obtained
here in the introduced range.
The overwhelming preponderance of the clonal repro-
duction in the introduced range of W. auropunctata does
not necessarily imply that clonal reproductives never
reproduce sexually. Some rare sexual reproduction events,
already observed in New Caledonia (Foucaud et al. 2006)
and Gabon (Mikheyev et al. 2009), were also apparent
here in introduced populations of Tahiti, Cameroon and
other Gabonese populations. In these countries, some
new clonal queen lineages were indeed derived from sex-
ual recombination by local clonal queen and male lin-
eages (see Fig. S2 and Foucaud et al. 2006 for a detailed
description of derived lineages). However we did not
detect any new clonal male lineage arising in those coun-
tries. We could therefore distinguish between two types
of clonal couples within the introduced range of W.
auropunctata. First, the original couples of clones are
likely composed of the originally introduced male and
queen genotypes (showing distinct genotypes without
recombination events). Second, the derived couples of
clones are composed of the original male genotype and a
queen genotype deriving from a sexual reproduction
event between the original male and queen genotypes.
Routes of introduction
Since virtually all introduced populations were clonal, we
directly assessed the relationships among the queen and
male genotypes from the introduced and the native range
of W. auropunctata and hence infer on introduction
routes. Our results show two major types of introduction
First, the Caribbean zone has been invaded by multiple
couples of clonal queens and males (Figs 1 and 2). Several
Caribbean countries share clonal queen genotypes, includ-
ing Guadeloupe and Dominica, Guadeloupe and Domini-
can Republic, and Cuba and Florida (i.e. on Fig. 2A:
Guadeloupe 1 – Dominica 2; Guadeloupe 2 – Dominican
Republic; Cuba 2 – Florida 4). The slight differences
between some of these genotypes are likely due to single
mutational or recombination events during thelytoky.
Interestingly enough, we observed a greater diversity of
male genotypes in the Caribbean zone, as only Cuba and
Florida share a clonal male genotype (i.e. on Fig. 2B:
Cuba 2 – Florida 3). All other introductions were
founded by single couples of clonal queen and male geno-
We could directly retrace the introduction histories for
three groups of invaded countries. First, the clonal queen
genotype shared by Guadeloupe and Dominica is also
shared with Gabon, Cameroon, New Caledonia and Tahiti
(Fig. 2A). This clonal queen genotype is mated to four
distinct male genotypes: one in Guadeloupe, one in Dom-
inica, one shared between Gabon and Cameroon, and one
shared between New Caledonia and Tahiti (Fig. 2B). Sec-
ond, the clonal male shared by Cuba and Florida is also
shared with Hawaii (Fig. 2B). It is also worth pointing
Foucaud et al. Worldwide invasion by W. auropunctata
ª 2010 Blackwell Publishing Ltd 3 (2010) 363–374 367
that the clonal Hawaiian queen genotype mated to this
clonal male is also related to a Floridian queen genotype
(Fig. 2A). Finally, one clonal queen genotype is shared
between the Melanesian populations from the Solomon
Islands, Vanuatu, Papua New Guinea and Australia
(Fig. 2A). This clonal queen genotype is mated to two
distinct male genotypes: one shared between Vanuatu and
Papua New Guinea, and one shared between the Solomon
Islands and Australia (Fig. 2B).
Treating together our microsatellite data set from the
introduced range and our previous data set from the
native range revealed two additional clusters of related
genotypes. While other genetic distances led to very simi-
lar topologies, these two clusters must however be ana-
lyzed cautiously because of the low bootstrap values of
some of the nodes of the queen tree (a feature expected
when bootstrapping individual tree over loci). The ﬁrst
cluster included the clonal queen genotypes found in the
Caribbean zone and some of the clonal queen genotypes
found in French Guiana (i.e. genotypes French Guiana C1
to C5; Fig. 2A). Two alternative hypotheses may explain
this cluster: (i) the clonal genotypes introduced in the
Caribbean Islands originate from the northern part of
South America, and (ii) the clonal populations of French
Guiana are a re-introduction of W. auropunctata from
the Caribbean zone. While the deﬁnitive data to distin-
guish these two hypotheses are lacking, the ﬁrst hypothe-
sis seems more probable because Guianese clonal queen
genotypes share a large proportion of their alleles at each
locus with the neighboring sexual populations and hence
likely originated from these sexual populations (Foucaud
et al. 2007). A larger sample from the northern coast of
the native range is needed to further disentangle these
two hypotheses. The second cluster included the queen
Figure 2 Neighbor-Joining dendrograms of the microsatellite (allele-shared) distances between individual queen (A) and male (B) genotypes.
Note: Groups of introduced queens and males present in more than one country that share clonal genotypes for queens, males or both, were
highlighted with colors similar to Fig. 1. Individual genotypes from the introduced and native ranges of Wasmannia auropunctata are written in
upper case and lower case letters, respectively. All introduced and, due to space limitation, a randomly chosen subset of native genotypes were
included for both sexes. Similar results were obtained when using all individual genotypes (not shown).
Worldwide invasion by W. auropunctata Foucaud et al.
368 ª 2010 Blackwell Publishing Ltd 3 (2010) 363–374
genotypes from the native populations of Costa Rica and
the introduced populations of Cocos Island (belonging to
the Costa Rican state). It is interesting to note that this
relationship in our microsatellite data set parallels previ-
ous ﬁndings based on mitochondrial DNA (Mikheyev
and Mueller 2007).
We could not infer any routes of introduction for the
clonal populations of Galapagos Islands and Israel, as well
as any origin for the Melanesian clonal populations.
These couples of clonal queen and male genotypes did
not match or showed tight relationships with any other
genotype from the native range of W. auropunctata. These
introductions probably correspond to three independent
routes that may originate from the native area or the
Caribbean area (e.g. the hypothesized Brazilian origin of
the Israeli population; Vonshak et al. 2009b).
Genotypic patterns of introduced populations
The characterization of the genotypic patterns of native
populations provides some useful insights into the native
origin of introduced populations of W. auropunctata.As
a matter of fact, heterozygosity and difference in allele
size differ markedly between sexual and clonal popula-
tions of the native range (see Methods section; Foucaud
et al. 2009a,b). We thus compared the heterozygosity and
difference in allele size between the male and queen geno-
types of three distinct types of couples: sexual couples of
the native range, clonal couples of the native range and
clonal couples of the introduced range. When treating
altogether all three types of couples, we found signiﬁcant
differences for both statistics (Friedman tests: Ho
= 18; P <10
: F = 7.16; P = 0.027; Table 2).
When considering the types of couples by pair, the males
and females genotypes from clonal couples from both the
introduced and native areas had signiﬁcantly higher
level of between-individuals heterozygosity and difference
in allele size than those from native sexual couples
(Wilcoxon sign rank tests: all P-values <0.05; Table 2).
On the other hand, there was no signiﬁcant difference
between introduced and native clonal couples for both
statistics (Wilcoxon sign rank tests: all P > 0.23).
When considering the same statistics measured within
individual worker genotypes, we found signiﬁcant differ-
ences for heterozygosity, but not for difference in allele
size (Friedman tests: Ho
= 7.17; P = 0.028; DS
F = 3.50; P = 0.17; Table 2). Pairwise analyses revealed
that workers from clonal populations from both the
introduced and native areas had signiﬁcantly (or nearly
for introduced populations) higher level of heterozygosity
than those from native sexual populations (Table 2).
There was no signiﬁcant difference between workers of
introduced and native clonal populations for both statis-
tics (Wilcoxon sign rank tests: all P > 0.11).
Examining our data in detail, we found that the non-
signiﬁcant differences between workers of the introduced
and native sexual populations were at least partly due to
the presence of sexually derived female clones in some of
the introduced areas (in New Caledonia, Tahiti and
Western Africa). It is worth stressing that the genotypes
of these derived female clones display some alleles of the
genotype of their male mate, resulting in couples (and
hence workers) with lower heterozygosity and difference
in allele size (see Foucaud et al. 2006 for details). When
removing the derived clonal genotypes from our data set,
heterozygosity, but not difference in allele size, was signif-
icantly higher in the worker offspring of the originally
introduced clonal couples than in the worker offspring of
the native sexual populations (Wilcoxon sign rank test:
: Z = 2.43; P = 0.015). The worker offspring of the
originally introduced clonal couples remained similar to
workers from native clonal populations for both statistics
(all P-values >0.39).
Altogether, we found that introduced clonal popula-
tions were similar to native clonal populations and
strongly dissimilar to native sexual populations with
Table 2. Heterozygosities (Ho) and differences in allele size (DS) in couples and workers from native sexual, native clonal and introduced clonal
Native sexual Native clonal Introduced clonal
Mean SE Mean SE Mean SE NaS-NaC NaS-lntC NaC-lntC
Ho 0.668 0.093 0.897 0.021 0.890 0.019 *** ** ** NS
DS 7.502 1.604 11.992 0.852 9.768 0.512 * ** * NS
Ho 0.710 0.032 0.852 0.026 0.808 0.018 * ** 0.08 NS
DS 7.859 0.761 11.214 1.043 8.485 0.400 NS * NS NS
Note: Levels of signiﬁcativity of Friedman and Wilcoxon sign rank tests have been included, where NS: P > 0.10, ***P <10
*P < 0.05. Native sexual, native clonal and introduced clonal populations are designated by NaS, NaC and IntC respectively.
Foucaud et al. Worldwide invasion by W. auropunctata
ª 2010 Blackwell Publishing Ltd 3 (2010) 363–374 369
regards to heterozygosity and difference in allele size of
couples and workers.
The present worldwide study enables us to reconstruct
some of the main routes of introduction of W.
auropunctata and provides some insights into the ecologi-
cal and evolutionary factors that may have favored the
current expansion of its distribution range around the
globe. This in turn suggests some general mechanisms
that could be involved in other, potentially numerous,
cases of biological invasions.
Routes of introduction
Our study highlights the fact that the key factor explain-
ing the current distribution of W. auropunctata over the
world is trade and historical shipping routes. While this
idea has been proposed long ago (Passera 1994; Wetterer
and Porter 2003), our study illustrates it in a striking way
(Fig. 1). Overall, we can distinguish several ‘human cul-
tural routes’ of introduction of W. auropunctata. First,
our study pinpoints the Caribbean zone as being an
introduced area of primary importance. To date, Carib-
bean populations were classiﬁed among native popula-
tions of W. auropunctata (Mikheyev and Mueller 2007),
with, however, substantial doubts (Wetterer and Porter
2003). Our study indicates that Caribbean populations
are most likely introduced and not native. All Caribbean
populations are indeed clonal, similarly to other intro-
duced populations, whereas native populations are either
clonal or sexual. Moreover, male and female clonal geno-
types were highly dispersed throughout the Caribbean
area, a situation that is parsimoniously explainable by
human-mediated dispersal. Altogether, our microsatellite
data set clearly shows that the Caribbean zone has under-
gone multiple introductions of W. auropunctata , maybe
from the northern coast of South America, represented
here by our Guianese samples. The diversity of male and
female clones that encompasses all the Caribbean area
indicates that introductions are most probably ancient
and/or frequent events. This situation probably arose
through the extensive human exchange between South
and Central America and the Caribbean islands that fol-
lowed the European colonization in the XVI
This latter result parallels those of a previous study based
on a mitochondrial DNA marker (Mikheyev and Mueller
Our study also shows that the Caribbean zone has been
an important platform for secondary long-distance intro-
ductions all over the World. We found two main routes
of introduction connected to the Caribbean zone (Fig. 1).
First, a ‘French’ introduction route connects the French
Caribbean island Guadeloupe to former (Gabon, Camer-
oon) and present French overseas territories (New Cale-
donia, Tahiti). Second, we also demonstrate the existence
of an ‘Hispano-American’ introduction route linking
sequentially Cuba to Florida, and Florida to Hawaii. The
latter link between Floridian and Hawaiian introduced
population, recently proposed by Mikheyev et al. (2009),
is here clearly evidenced. The geographical and socio-eco-
nomical proximity of the Caribbean archipelago to the
tropical American mainland (i.e. the native area of W.
auropunctata), together with its ongoing history of strong
connection with other tropical areas worldwide through a
variety of ‘cultural’ networks, are the probable causes of
the intermediate position of the Caribbean populations in
the worldwide invasion of W. auropunctata.
Two other introduction routes illustrate the ‘cultural’
component of the invasion of W. auropunctata. First, we
show that Australia, Vanuatu, Papua New Guinea and the
Solomon Islands have been invaded by only one clonal
queen and two clonal male genotypes. The most probable
explanation for this strong link between these populations
is the introduction of W. auropunctata through the tradi-
tional exchange of plants and goods between Melanesian
peoples. We could not further trace back the origin of
these introduced populations, but mtDNA data indicate
that they probably originate from the Caribbean area
(Mikheyev and Mueller 2007). Finally, our microsatellite
data suggest, without strong statistical support, an intro-
duction of the Cocos Island population from the Costa
Rican mainland, a scenario already suspected in previous
studies (Solomon and Mikheyev 2005; Mikheyev and
That cultural and commercial networks represent key
factors in the current distribution and origins of intro-
duced populations has already been shown in others inva-
sive species, including other invasive ants. Trade explains
much of the current distribution of Solenopsis invicta
(Tschinkel 2006; Caldera et al. 2008; Zhang et al. 2009),
Linepithema humile (Suarez et al. 2001; Corin et al. 2007;
Sunamura et al. 2009a) and other invasive ant species
(McGlynn 1999). Cultural and economical hubs, such as
the Caribbean area, are also ‘invasive species hubs’, as
recently illustrated by the presence of three distinct
supercolonies of L. humile in the port of Kobe, Japan
(Sunamura et al. 2009b).
Eco-evolutionary pathways to invasion
The present study does not strictly link any known intro-
duced population to a known native population. This
result was somewhat expected given the high genetic
diversity and strong structure of native W. auropunctata
Worldwide invasion by W. auropunctata Foucaud et al.
370 ª 2010 Blackwell Publishing Ltd 3 (2010) 363–374
populations (Foucaud et al. 2009b). Recent studies
pointed that high-density, dominant populations were
present in the native geographical range of W.
auropunctata (Orivel et al. 2009). The large majority of
these native dominant populations were headed by clonal
queens and males displaying a speciﬁc genetic pattern of
outbreeding (i.e. clonal male and queen from a given
couple tend to possess divergent genotypes; Foucaud et al.
2009b). We found here that virtually all introduced
populations were also clonal, and that these introduced
populations stemmed from clonal couples associating
male and queen genotypes that also produced particularly
heterozygous workers. Dominant populations from the
native range and invasive population from the introduced
range are therefore similar in term of reproduction
system and speciﬁc mating patterns, and distinct from the
native sexual populations. This work hence provides
indirect evidences that the introduced populations of W.
auropunctata originate from the native dominant popula-
It is worth pointing that all native dominant popula-
tions are located in human-disturbed habitats, in sharp
contrast to native non-dominant populations, located in
natural habitats such as primary forests. It has therefore
been hypothesized that the high heterozygosity of workers
from native clonal populations might help them to cope
with the particular biotic and abiotic conditions of
human-disturbed habitats (Foucaud et al. 2009b). Several
studies have suggested that the maintenance of highly het-
erozygous combinations of genes might be advantageous
to maintain viable populations in habitats where abiotic
conditions are extreme or changing (Kearney and Shine
2004; Frankham 2005b; Ferreira and Amos 2006), as
found for temperature and humidity in human-disturbed
habitats of the native range of W. auropunctata (Orivel
et al. 2009). Alternatively, highly heterozygous combina-
tions of genes may enable individuals to better exploit
their environment, particularly when resources are abun-
dant (Reznick et al. 2000; Vorburger 2005), which is
probably the case in human-disturbed habitats such as
plantations (Delabie et al. 1994). If the maintenance of
speciﬁc gene combinations is required to maintain viable
populations in human-disturbed habitats, then the male
and female clonal reproduction system of W. auropuncta-
ta is expected to be advantageous in these habitats,
because it lacks recombination, contrary to a sexual
reproduction system. The results we obtained here on
introduced populations, which were almost only sampled
in invaded human-disturbed habitats, are consistent with
this hypothesis. Laboratory experiments are needed to test
for ﬁtness differences between sexual and clonal popula-
tions from both native and introduced ranges using abi-
otic conditions speciﬁc to human-disturbed habitats.
An additional advantage of the male and female clo-
nal reproduction system of W. auropunctata is expected
during remote introduction events. Even if the number
of initial founders is small, this system indeed prevents
the rapid erosion of the introduced population genetic
diversity through drift, thus limiting genetical side effects
of bottlenecks (i.e. inbreeding depression for sexually
reproducing populations, Keller et al. 1994; Haag et al.
Scenario of the little ﬁre ant worldwide invasion
A traditional vision of biological invasions, illustrated in
Fig. 3A, assumes that it is a single step process, where an
‘exotic’ species from a ‘distant’ native area establishes and
spreads into an introduced area (Richardson et al. 2000;
Sakai et al. 2001; Colautti and MacIsaac 2004). In agree-
ment with this, most current deﬁnitions of bioinvasions
explicitly insist on the occurrence of a long-distance
transport between the native and introduced ranges
(Colautti and MacIsaac 2004; Vermeij 2005; Falk-Petersen
et al. 2006; but see Vale
ry et al. 2009). In the case of W.
auropunctata, our data, together with previous studies
(Foucaud et al. 2009b), suggests that a two-step process
as illustrated in Fig. 3B is actually more parsimonious.
The ﬁrst step occurs within the native range of the spe-
cies, where mostly clonal populations, likely originating
from natural habitats, spread to and dominate some
human-disturbed habitats (Foucaud et al. 2009b). Because
natural and human-disturbed habitats are often spatially
adjacent within the native range of the species, it is likely
that the propagule pressure exerted from the natural on
the human-disturbed habitats is signiﬁcantly higher than
traditionally supposed between ‘distant’ native and intro-
duced ranges. This is expected to favor the emergence of
dominant populations adapted to human-disturbed
The second step is the transfer, establishment and local
spread of populations from the native to the remote
introduced areas of the species. The most parsimonious
hypothesis is that these introduced invasive populations
stem from the native clonal populations of the human-
disturbed habitats, for at least three reasons. First, our
study shows that the main vector of W. auropunctata
long-distance dispersal is trade, in accordance with previ-
ous results on this species (Mikheyev and Mueller 2007)
as well as many other pests (McGlynn 1999; Mack et al.
2000; Sunamura et al. 2009b). Because human-modiﬁed
areas are nowadays extensively connected on a global scale
(Rahel 2007; Tatem and Hay 2007), it is therefore highly
probable that the propagule uptake from the native range
of W. auropunctata is several orders higher from the high-
density populations typical of human-disturbed habitats
Foucaud et al. Worldwide invasion by W. auropunctata
ª 2010 Blackwell Publishing Ltd 3 (2010) 363–374 371
than from low-density populations of natural habitats.
Second, it is now widely recognized that one of the major
impacts of human activities on Earth’s ecosystems is bio-
tic and abiotic homogenization (McKinney and Lockwood
1999; Tilman et al. 2001; Olden et al. 2004; Foley et al.
2005; Ewers et al. 2009). It may therefore not be neces-
sary, or at least less difﬁcult, for introduced populations
to adapt to new environmental conditions (i.e. human-
disturbed habitats of the introduced range), as long as
they come from human-disturbed habitats of the native
range. Finally, putative genetic costs of introductions of
small size propagules (e.g. inbreeding depression) can be
avoided by clonal populations but not by sexual popula-
tions of the native range of W. auropunctata (Sakai et al.
The two-step scenario illustrated in Fig. 3 might apply
to a substantial proportion of invasive species, including
ants. In S. invicta for instance, populations introduced in
the USA originate from native areas that are disturbed
naturally or by human activities and where the species is
ecologically dominant (Calcaterra et al. 2008). Second, S.
invicta was most probably dispersed from ports from the
Buenos Aires region into Port Mobile, Alabama (Lofgren
1986). Finally, it has been shown that S. invicta is subse-
quently favored by human-induced ecological change in
its introduced range (King and Tschinkel 2008). Other
invasive species that are found in close contact with
humans within their native range could also comply with
our two-step scenario as was noticed in previous studies
(e.g. Sakai et al. 2001).
Our study of the worldwide invasion by W. auropunctata
illustrates the central role of human-induced biological
change. This human-induced change does not seem to
only modify species migration patterns, but also selective
pressures over species in both their native and introduced
ranges. In the case of W. auropunctata, it is likely that the
dramatic biological shifts that putatively occurred during
the transition from natural to human-disturbed habitats
within its native range is the basis of the worldwide inva-
sion success of the species.
The W. auropunctata case also illustrates the arbitrary
aspect of the use of geographical factors (i.e. native/intro-
duced ranges) as a conceptual basis in the study of bio-
logical invasions (see Vale
ry et al. 2009). We argue that
invasion biologists should rather use objective ecological
factors (i.e. habitats and niches) as a basis to decipher the
evolution of invasiveness in wild populations. The need
to root invasion biology deeper into ecology and evolu-
tion has already been underlined in several seminal publi-
cations (Heger and Trepl 2003; Facon et al. 2006; Lee and
Figure 3 Schematic representation of the traditional vision of bioinvasions (A) and of the most parsimonious scenario of the worldwide invasion
of Wasmannia auropunctata (B).
Worldwide invasion by W. auropunctata Foucaud et al.
372 ª 2010 Blackwell Publishing Ltd 3 (2010) 363–374
We would like to thank Barbara Gerber for her great help
in the lab, Tommy Thompson for sampling the Hawai’ian
Wasmannia population, and Benoı
t Facon and Ruth
Hufbauer for helping us improve earlier versions of this
manuscript. This work was supported by a grant from the
re de l’Ecologie et du De
ble – appel d’offre ECOTROP to AE and JO and by a
grant CORUS no 02 412 062 du Ministe
re des Affaires
res to MT. JHCD acknowledges his research grant
by CNPq. Data used in this work were (partly) produced
through molecular genetic analysis technical facilities of
the IFR119 Montpellier Environnement Biodiversite
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Additional Supporting Information may be found in the online version of this
Figure S1. Schematic representation of the gene transmission between two
consecutive generations in the two types of reproduction system found in
Figure S2. Schema (A) and example drawn from the Cameroon sample (B) of
the diversiﬁcation of clonal queen genotypes in several populations of the intro-
Table S1. Estimated dates of introduction of Wasmannia auropunctata in the
sampled introduced range.
Please note: Wiley-Blackwell are not responsible for the content or functional-
ity of any supporting materials supplied by the authors. Any queries (other than
missing material) should be directed to the corresponding author for the article.
Worldwide invasion by W. auropunctata Foucaud et al.
374 ª 2010 Blackwell Publishing Ltd 3 (2010) 363–374