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Is It Easy to Be Urban? Convergent Success in Urban Habitats among Lineages of a Widespread Native Ant

  • Sean B. Menke ,

    sean_menke@ncsu.edu

    Affiliations Department of Entomology, North Carolina State University, Raleigh, North Carolina, United States of America, Department of Biology, North Carolina State University, Raleigh, North Carolina, United States of America, W. M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, North Carolina, United States of America

  • Warren Booth,

    Affiliations Department of Entomology, North Carolina State University, Raleigh, North Carolina, United States of America, W. M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, North Carolina, United States of America

  • Robert R. Dunn,

    Affiliations Department of Biology, North Carolina State University, Raleigh, North Carolina, United States of America, W. M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, North Carolina, United States of America

  • Coby Schal,

    Affiliations Department of Entomology, North Carolina State University, Raleigh, North Carolina, United States of America, W. M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, North Carolina, United States of America

  • Edward L. Vargo,

    Affiliations Department of Entomology, North Carolina State University, Raleigh, North Carolina, United States of America, W. M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, North Carolina, United States of America

  • Jules Silverman

    Affiliation Department of Entomology, North Carolina State University, Raleigh, North Carolina, United States of America

Is It Easy to Be Urban? Convergent Success in Urban Habitats among Lineages of a Widespread Native Ant

  • Sean B. Menke, 
  • Warren Booth, 
  • Robert R. Dunn, 
  • Coby Schal, 
  • Edward L. Vargo, 
  • Jules Silverman
PLOS
x

Abstract

The most rapidly expanding habitat globally is the urban habitat, yet the origin and life histories of the populations of native species that inhabit this habitat remain poorly understood. We use DNA barcoding of the COI gene in the widespread native pest ant Tapinoma sessile to test two hypotheses regarding the origin of urban populations and traits associated with their success. First, we determine if urban samples of T. sessile have a single origin from natural populations by looking at patterns of haplotype clustering from across their range. Second, we examine whether polygynous colony structure – a trait associated with invasion success – is correlated with urban environments, by studying the lineage dependence of colony structure. Our phylogenetic analysis of 49 samples identified four well supported geographic clades. Within clades, Kimura-2 parameter pairwise genetic distances revealed <2.3% variation; however, between clade genetic distances were 7.5–10.0%, suggesting the possibility of the presence of cryptic species. Our results indicate that T. sessile has successfully colonized urban environments multiple times. Additionally, polygynous colony structure is a highly plastic trait across habitat, clade, and haplotype. In short, T. sessile has colonized urban habitats repeatedly and appears to do so using life history strategies already present in more natural populations. Whether similar results hold for other species found in urban habitats has scarcely begun to be considered.

Introduction

Unlike most habitats, urban and managed environments are growing in area in nearly all geographic regions [1]. In the language of global change, these expanding urban environments are “non-analogue”, which is to say they do not have a direct analogue in contemporary natural conditions [2], [3]. These changes in global environments have favored a narrow subset of species [4][7], including invasive species, introduced beyond their native range [6], [8], [9], but also species native to the regions [7], [10][13]. Yet, while a large body of work has focused on the history and traits of invasive species [14][16], only a small handful of studies have considered the traits associated with and origin of urban populations of native species [7]. Put simply, how do urban populations of native species arise?

The urban habitat is one of the fastest growing habitats globally, and the habitat in which most humans now live [1]. As such, the species with the most interactions with humans are and will increasingly be those in urban environments [8], [12]. The study of the evolutionary origins of such species and their traits is a new and growing field [7]. The differences in life histories of species in urban environments relative to in their native habitats are diverse, but include increased geographic distributions, decreased home ranges, higher densities, changes in foraging, increased reproductive output, and other life history traits [7], [11], [14], [16][19]. At least some of the traits that seem to be favored in urban environments are also those that are favored in invasive species and more generally disturbance specialists, such as short generation times, rapid reproduction, good dispersal, and plastic behaviors and life history traits [4], [15], [20]. In invasive species, at least some of the traits present in the invaded range but absent in the native range represent microevolutionary responses to novel environments. Whether the same is true for native species in the urban environment is unclear.

Globally, the family of ants (Formicidae) is one of the most prominent groups of organisms, and includes many species that perform important ecological services relevant to humans and the ecosystems on which humans depend [21]. Many ant species that perform these services persist in urban environments [22]. In addition, ants may perform services in urban environments that are not necessarily valuable elsewhere, such as the removal of food, waste and other items. However, most urbanized environments are also accumulating pest species (species that pose problems for humans), including invasive and native species some of which are of economic and public health concern, species it might be said, that perform disservices [23][26]. While the native species that inhabit urban environments have received some attention in the pest control literature [23], [24], their origins and basic biology remain essentially unexplored. For example, Tapinoma sessile, the odorous house ant, is the most widespread native ant in the United States, occurring in most habitat types between the eastern and western coasts of northern Mexico to southern Canada from sea level to 4,000 m (Fig. 1, unpublished data, http://www.antmacroecology.org/projects.html). It has also been a common structural pest species for over 100 years [23], [27], both inside and outside of buildings [23], [28] and it has been reported that it is rapidly expanding its range in urban environments [29]. Yet only a few studies, all taking place in urban areas [27], [30][32], have explicitly studied its basic biology, and only a few more studies [33][37] have mentioned anything about the biology of this species in natural habitats. Due in part to a lack of knowledge on the basic biology of this species in different habitats or different parts of its range, little is known about how, when, and why it has been successful, particularly in urban environments.

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Figure 1. Distribution of Tapinoma sessile North America.

Museum and literature collection records (small gray circles), and the 49 localities represented in this study (west – purple triangles; mountain – orange circles; south – blue squares; north – green diamonds).

https://doi.org/10.1371/journal.pone.0009194.g001

Although it has not received much study, reports to date suggest that T. sessile possesses many features within the suite of traits referred to as the “invasive syndrome” [14], suggesting that such a syndrome may promote success both in non-native habitats but also in non-analogue habitats such as cities. Traits implicated in this syndrome include large colonies, colonies with multiple queens that mate within the nest, and colonies that often occupy many interconnected nests with little to no territorial aggression among them [25]. Fellers [36] and Milford [33] reported that colonies of the odorous house ant were small, occupying single nests, and acted as a subdominant species in natural habitats. In contrast, studies of pest populations in urban habitats have reported that the odorous house ant forms large polydomous populations that act as behaviorally dominant ants [27], [30], [31]. But it remains uncertain whether these invasive traits are actually found only in urban populations of T. sessile. Moreover, it is unknown whether there was a single colonization of the urban environment by T. sessile, with the subsequent evolution of the “invasive syndrome” traits, or instead, independent biogeographic shifts from native into urban environments. The observation that few native species have become pests in disturbed habitats suggests that the traits necessary for such a lifestyle are uncommon, and that they neither readily evolve nor are very plastic, whether for T. sessile or any other ant species. On the other hand, the wide geographic range of T. sessile and its occurrence in diverse habitats represent characteristics of a generalist species that can obviously plastically adapt to numerous different environments and may provide important insight about the origin of urban populations.

We chose to address two related hypotheses regarding the phylogeography of T. sessile. First we studied whether all urban samples of T. sessile have a single common origin from one or more natural populations, suggesting a single successful invasion of a novel environment and subsequent human transport. An alternative hypothesis is that urban populations descend from local natural populations, suggesting repeated successful invasions of a novel environment. We assessed these hypotheses using a phylogeographic approach to determine whether urban samples across the range of the species in the United States are genetically similar to nearby samples found in native habitats. Second, we looked at whether polygynous colony structure, a colony-level trait thought to be linked with success in invading novel habitats, is consistently associated with the transition to urban lifestyle, or alternatively, if it is also common in natural habitats. We assessed this by studying the lineage dependence of colony structure.

Methods

Specimen Collection

Forty-nine collections of T. sessile were made from 47 localities (Fig. 1, Appendix S1) throughout the continental United States. Specimens were collected by the authors or provided by other biologists and pest management professionals. The habitat at the collection point was divided into two broad categories: urban and natural. At 18 of the collections it was possible to determine if the nest site was monogynous or polygynous by collecting either the entire nest or by collecting numerous queens from the same nest. We considered all multi-queen colonies to be polygynous, but we were not able to ascertain if all queens within in a nest were reproductively viable or contributing brood. In order to determine if colony collections from a nest site represent a complete colony or just a colony fragment from a satellite nest in a polydomous colony, worker aggression assays were used. Single workers from the collected colony were introduced to the nest entrances of adjacent colonies, within a 10 meter (m) radius, that were identified by baiting and visual surveys. If these workers were treated aggressively and killed, we inferred that our collections represented a complete colony, whereas if the workers were accepted at the new nest entrance then the nest collection represented part of a larger polydomous colony. Based upon laboratory trials worker introductions to a different colony always result in worker mortality. Voucher specimens were deposited at the Bohart Museum, Department of Entomology, University of California at Davis (UCD) (Appendix S1).

Molecular Techniques

Total genomic DNA was extracted from 68 whole individual ants represnting 49 nests of T. sessile and 1 nest of T. erraticum (see Appendix S1) using DNeasy Tissue extraction kit (QIAGEN, Valencia, CA). Cytochrome oxidase I (COI) gene sequences, commonly used in “DNA barcoding”, were amplified using primers LepF1 (5′-ATTCAACCAATCATAAAGATATTGG-3′) and LepR1 (5′-TAAACTTCTGGATGTCCAAAAAATCA-3′) [38], [39], which targeted a 658-bp fragment. Polymerase chain reactions (PCRs) were performed in 30 µl volumes containing: 1X PCR buffer, 2 mM MgCl2, 100 µM dNTPs, 3 pM of each primer, 0.5 U Taq DNA polymerase (Bioline, Taunton, MA), ∼50 ng DNA template, and ddH2O to 30 µl. PCR cycling conditions were comprised of an initial denaturation stage of 1 min at 94°C, followed by 4 cycles each consisting of 1 min at 94°C, 1.5 min at 45°C, and 1.5 min at 72°C. This was followed by 34 cycles each consisting of 1 min at 94°C, 1.5 min at 45°C, and 1 min at 72°C, carried out using a PTC-200 thermal cycler (MJ Research Inc.). All 68 DNA extracts amplified under these conditions. PCR products were visualized on a 2.5% agarose gel to confirm samples contained a single band, and they were subsequently purified using QIAquick PCR purification kit (QIAGEN, Valencia, CA) and bidirectionally sequenced following the methodology outlined in Copren et al. [40]. Sequence alignments were performed using the Vector NTI Advance 10 program (Invitrogen, Carlsbad, CA).

Phylogenetic Analysis

Sequence alignment was performed using the Vector NTI (v10) software (Invitrogen). Phylogenetic relationships were initially examined using Molecular Evolutionary Genetics Analysis (MEGA), version 4 [41]. Four methods were employed, Neighbor-joining (NJ), UPGMA, Maximum parsimony, and Minimum evolution. Under these methods all characters were weighted equally and bootstrap replicates set to 10,000. Subsequently, hierarchical likelihood ratio tests for DNA substitution at the COI gene were performed using MrModeltest version 2.3 [42] and Bayesian analysis performed using MrBayes version 3.1.3 [43]. Two independent MCMC analyses, each with one cold and three hot chains, were run for 107 generations. Burn-in was set to discard the first 1000 of 10,000 sampled trees. Convergence of chains to a stationary distribution was assessed by inspection using the computer program Tracer v1.5, and confirmed by obtaining values of the average standard deviation of split likelihood frequencies less than 0.01 between the two runs. Tapinoma erraticum was used as an out-group. Sequence divergence within and between clades was calculated using Kimura-2 parameter pairwise genetic distance using MEGA version 4.

The evolutionary relationship between mtDNA sequences was also calculated through the construction of minimum spanning networks using the program TCS 1.21 [44] which follows the method outlined by Templeton et al. [45]. Given the sparse collection for some regions we felt that our data set was not suitable to infer significance of phylogeographic patterns observed using tests such as Nested Clade Analyses. Networks found to be unconnected at the 90% probability of parsimony were linked by decreasing the connection probability to a minimum of 60%.

Analysis of molecular variance (AMOVA) was used to assess genetic structure hierarchically based on geographic clustering (following identification by phylogenetic tree and minimum spanning network construction) and habitat association. Calculations were performed using the Arlequin 3.11 software [46].

Results

Ecological Data

Of the 49 T. sessile nest collections that were processed, colony structure and habitat varied widely, from an acorn-nesting monogynous colony with about 50 workers in a deciduous forest (sample 43 – north clade), to a polygynous colony containing two queens and approximately 250 workers nesting under a rock in a high elevation meadow (sample 14 – mountain clade), to a very large colony with millions of workers and thousands of queens nesting in and around several buildings on a college campus (sample 36 – north clade). Colony structure was recorded in 18 of the collections based on number of queens collected at one nest site. Twenty-three collections were made in natural environments, most of which were stray workers collected by entomologists without any information on colony structure. Twenty-six collections were made in urban environments, most provided as stray workers by pest management professionals from infestations in homes. For the six monogynous colonies sampled, the entire colony was hand-collected and workers introduced to the nearest surrounding nests were all killed demonstrating colony differentiation. The 12 polygynous colonies sampled were identified when single nests or single nest fragments contained multiple queens, but again we considered all multi-queen colonies to be polygynous, although we were not able to ascertain if all queens within in a nest were reproductively viable or contributing brood. The polygynous nests collected in urban areas, such as south clade samples 18 & 19 and north clade samples 30 & 36, had multiple nest sites along building margins which demonstrated no worker aggression between nests and contained millions of workers and thousands of queens, whereas the polygynous colonies collected from natural areas, such as mountain clade sample 14 and north clade sample 38, were isolated nests under a rock or log with fewer than 20 queens.

Genetic Data

A 658-bp fragment of the COI region was amplified and sequenced for 67 specimens of T. sessile and a single specimen of T. erraticum. Where multiple individuals from a single nest were sequenced a single within-nest haplotype resulted. Overall, there were 39 unique T. sessile haplotypes. Of the 658 nucleotide sites in the aligned data matrix and included in the phylogenetic analysis, 115 were variable and 105 were parsimony informative. Haplotypes are named Ts-1 to Ts-39 and the corresponding GenBank accession numbers are (GU373531-GU373569, GU388394). Average base frequencies were A:0.295, C:0.184, G:0.137, T:0.384. Widespread haplotypes were few, and most clades were comprised of predominantly unique haplotypes (Fig. 2, Appendix S1). No haplotypes were shared between clades (Fig. 2).

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Figure 2. Minimum spanning network calculated by TCS 1.21 using mitochondrial COI sequences.

Haplotypes with the highest ancestral probability are displayed as squares, while other haplotypes are displayed as ovals. Shaded boxes/ovals represent urban samples, hollow stars are monogynous colonies, filled stars are polygynous colonies, and colors correspond to Figure 1. Colored boxes define networks identified with 90% probability of parsimony. Connections between networks were determined through decreasing the probability to a minimum of 60%.

https://doi.org/10.1371/journal.pone.0009194.g002

Phylogenetic Analysis

Identical consensus tree topologies where produced under the four methods investigated using MEGA, (Bootstrap support for NJ method reported in Fig. 3). MrModeltest identified the GTR+G+I model as best fitting the data. Bayesian analysis produced 9,000 trees after disregarding the burn-in (Fig. 3) and strongly supported the monophyly of a western clade (posterior probability of 100, bootstrap support of 99%). With a posterior probability of 83 and bootstrap support of 79%, a polyphyletic mountain clade was separated from strongly supported monophyletic southern and northern clades (posterior probabilities of 100 and 99, respectively, and bootstrap support of 99% each).

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Figure 3. Fifty percent majority rule consensus tree from the Bayesian analysis.

Numbers below branches indicate posterior probability values and numbers above indicate nonparametric bootstrap values from the Neighbor-Joining method. Only values >50% (or 0.5 posterior probability) are shown. Colors correspond to Figure 1. Samples denoted with a white star refer to monogynous colonies and black stars refer to polygynous colonies. Taxon labels in color represent urban samples.

https://doi.org/10.1371/journal.pone.0009194.g003

Minimum spanning networks (TCS) analysis of mtDNA sequences produced four unconnected haplotype networks (Fig. 2) with 95% probability of parsimony, corresponding to the four geographic clades identified in figure 3. The west clade consisted of haplotypes Ts1 through Ts3; the mountain clade haplotypes Ts4 through Ts13; the south clade haplotypes Ts14 through Ts23; and the north clade consisted of haplotypes Ts24 through Ts39. Networks were connected by reducing the probability of parsimony to 60%. In doing this, the north clade was connected to both the south and mountain clades by 35 and 29 mutational steps respectively, while the west clade was connected only to the mountain clade by an additional 39 mutational steps (Fig. 2).

The genetic structure of the different clades was found to be strongly associated with the geographic distribution of the samples. AMOVA results revealed that variation between clades explained 81.5% of the genetic variation (Table 1). Variation within clades also proved significant corresponding to 18.5% of the variation. Kimura-2 parameter pairwise distances between clades ranged from 0.072 to 0.103. Within-clade distances ranged between 0.002 in the western clade and 0.022 in the mountain clade (Table 2). There was an area of broad overlap between the south and north clades along the eastern coast of the United States with samples from Washington DC (17), Knoxville, Tennessee (18), and Rocky Mount and Raleigh in North Carolina (19 and 20) clustering with the south clade, while other samples from Washington DC (28), the mountain regions in Tennessee (38, 39, 48), and numerous other sites in North Carolina (30–32, 35–36, 41, 45) clustered with the north clade (Figs. 1 & 2). Despite this area of broad geographic overlap, the two clades had strong bootstrap and Bayesian support (89% and 95%, respectively) and large differences (7.4%) in average sequence divergence (Fig. 3, Table 2).

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Table 1. AMOVA results for DNA sequence data analysis of Tapinoma group by clade, habitat type, or habitat within north clade.

https://doi.org/10.1371/journal.pone.0009194.t001

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Table 2. Average Kimura-2 parameter distances with bootstrap standard errors based on 658 base pairs of the mitochondrial COI gene within a clade on the diagonal in bold and between clades beneath the diagonal.

https://doi.org/10.1371/journal.pone.0009194.t002

Samples collected from urban environments were not found to be derived from a single source location, but instead were more closely related to geographically proximate samples from natural habitats. AMOVA performed over all samples, regardless of clade, revealed significant variation between samples grouped by habitat (Table 1). This is likely to have resulted from variation existing between clades, and thus not actual differentiation based solely on habitat type. When analysis was performed using samples from a single clade (only the North contained sufficient samples to test significance) no significant variation was detected between groups (Urban vs. Natural). More than 99% of the variation was explained among populations within groups. For example, north clade samples from natural habitats in Indiana (43), North Carolina (31), and Tennessee (38 & 39) clustered with samples from urban sites in Indiana (40), North Carolina (32), and Tennessee (48), respectively (Fig. 3). Similarly, in the south clade samples 21 & 27, collected from forest sites in Arkansas, clustered with samples from urban sites in Alabama (26), Arkansas (16), Oklahoma (23–25), and Texas (22). Single haplotypes were found to contain samples from both urban and natural biomes (Ts23 & Ts24) (Fig. 2).

Colony structure also varied within each clade in which it was recorded and within different habitats. Polygynous colonies were commonly found in both urban and natural environments and in each of the three clades in which colony type was recorded (Fig. 3, Appendix S1). Monogynous colonies were also collected in both the south and north clades in both urban and natural environments, but no confirmed monogynous colonies were collected in the mountain clade. Monogynous and polygynous colonies were often collected in close proximity to each other, such as samples 38 & 39 and 35 & 41 (Fig. 3, Appendix S1) and samples of both colony structure type were found to share haplotypes (Ts29) (Fig. 2).

Discussion

Our phylogenetic analysis of T. sessile collections from the mainland U.S. identified four well supported clades: one found in the western U.S., one in the mountain region (Utah and Colorado), a third spanning the north-central to northeastern U.S., and a fourth covering the south-central to southeastern U.S. (Fig. 1). Some mixing of haplotypes was noted within North Carolina, Washington DC and Tennessee, indicating that this region may act as a break point between the north and south clades (Fig. 1). Within clades, genetic distances were low but significant indicating that within region population genetic structure may exist. The level of genetic difference detected between clades suggests that separate clades may represent unique evolutionary lineages and warrant further investigation (Table 2). It is important to note, however, that our collection sites represented three broadly discontinuous regions (western, mountain, midwestern/eastern), and that further collections between these and other geographic regions could unveil more clades and transition zones between clades.

Do Urban Colonies Have a Single Common Origin?

Based on evidence of significant genetic variation at the regional level, no differences between habitats, and overlapping haplotypes (Figs. 2 & 3, Table 1), we reject our initial hypothesis that urban populations have become established following a single invasion event with subsequent human-mediated dispersal responsible for a continent-wide distribution. Under this hypothesis, we expected urban samples to form a monophyletic group separate from those derived from natural populations. Our results favor the alternative and to our minds more interesting hypothesis that urban populations of T. sessile have arisen multiple times from nearby populations in natural habitats.

Is Polygynous Colony Structure Associated with the Transition to Urban Habitats?

Based on both behavioral observations and phylogenetic analysis we reject the hypothesis that polygynous colonies are solely associated with urban environments. Rather, colony structure appears to be a plastic trait across habitat type, clade, and haplotype (Figs. 2 & 3). Although the polygynous nests in urban environments had the greatest observed density of both queens and workers compared to nests in natural habitats, colony size varied dramatically within a given environment. For example, within a natural grassland, nests ranged in size from monogynous with 250 workers (39) to polygynous with 5 queens and 960 workers (38), while in urban residential areas both small monogynous (20) and very large polygynous nests with millions of workers and thousands of queens (19) were collected. Our results suggest that multiple lineages of T. sessile have been able to successfully invade the urban environment and that this may be due to the plastic expression of colony structure.

Does Tapinoma sessile Have Phylogeographic Structure?

Our results, based on within- and between-clade divergence at the mitochondrial gene COI, suggest that the taxonomic status of T. sessile warrants further investigation; it may be comprised of a species complex. In recent years, the taxonomic status of many “species” has been called into question following the application of DNA bar-coding techniques [39], [47][50]. Sequence divergence at COI is generally higher between than within species [51], [52]. For example, intraspecific sequence divergence in COI ranged from 0.27% to 1.24% among 256 bird species, while average interspecific sequence divergence was 7.9% for 260 bird species [53]. Similarly, intraspecific sequence divergences ranged from 0–3.2% in the Lycaenidae butterfly family, while the average interspecific divergence was 9.4% [54]. Recent work on ants by Fisher & Smith [55] reported intraspecific variation reaching almost 8% among eight different species of ants in Madagascar, while Wild [51] found intraspecific variation in 11 species of ants in the genus Linepithema did not exceed 5%. Therefore, divergence values exceeding the greatest reported intraspecific range (i.e., >8%) in morphologically and molecularly described ant species [55] may therefore indicate the presence of unrecognized sibling species. Moreover, wide ranging species that occupy a diverse array of ecological niches may represent cryptic species complexes. Hebert et al. [39], for example, recommended splitting the species recognized as the neotropical skipper butterfly, Astraptes fulgerator, a common and widely distributed species originally described in 1775, into 10 largely sympatric species based on DNA bar-coding at the COI gene along with morphological and natural history information. In the case of T. sessile, recent but limited molecular evidence presented in a poster by Smith et al. [56] demonstrated sequence divergence of 9% and preliminary morphological evidence by Hamm [57] together suggest that T. sessile may represent multiple cryptic species. Our results, from sampling across the U.S. showing within-clade divergence ranging from 0.2 to 2.3% and among-clade divergence of 7.5 to 10.0%, offer support for the idea that the taxonomic status of T. sessile warrants further investigation. It is not surprising that T. sessile may represent multiple species given that T. sessile occupies the widest geographic range of any native North American ant species and tolerates diverse ecological environments [58]. But, our current sampling does not reveal an obvious correlation with habitat preferences, given that both natural and urban populations were intermixed.

Tapinoma sessile is an intriguing case-study because throughout its geographic distribution it occurs in adjacent natural and urban environments (Fig. 1 & 2) and there appears to be a great deal of plasticity in colony structure both within a habitat and between urban and natural environments. How colony structure and queen number are determined in ants has a long history as an evolutionarily important question [59][61]. It remains uncertain if the large colonies in urban environments represent a change in colony structure throughout urban habitats, and if so, whether they represent the evolution of a novel phenotype (unicoloniality) or a plastic expansion of existing variation in phenotype of colony structure that might have been favored historically due to the generalist nature of T. sessile. A similar situation occurs in the little fire ant (Wasmannia auropunctata) in its native range where plasticity in colony type and reproductive structure have been reported along a habitat disturbance gradient [62], [63]. Expansion in colony size among social insects is associated with ecological success, and in ants it has been demonstrated that colonies become more effective competitors when numerically superior [36], [64]. It has also been suggested that more behaviorally dominant ants succeed in urban environments [65]. The suggested importance of behavioral dominance is interesting, given that T. sessile in most natural studies has been regarded as an insinuator rather than a dominant species [36], [66]. Nevertheless, we have observed that extremely large colonies of T. sessile in urban environments dominate the urban landscape and control baits in the presence of several aggressive invasive ant species, including Solenopsis invicta and Tetramorium caespitum (personal observation). This apparent expansion in colony size in urban populations of T. sessile is similar to the change in colony size among invasive social insects globally [25], [67], [68] and suggests the intriguing possibility that success in urban environments is not unlike succeeding on new continents. If so, both urbanization and species introductions may be favoring a suite of species with similar traits.

A key remaining question with regard to both urban adapted species and invasive species, is how large, typically polygynous colonies arise and what benefits such colonies provide for success in novel environments [25], [60], [67]. A recent review found that unicoloniality and large colonies with multiple queens, more generally, is very common in introduced species [14], [25]. Perhaps the simplest explanation is that such colonies can arise through multiple mechanisms. In some cases, they may result from population bottlenecks like in the Argentine ant, Linepithema humile [69], [70], although this does not appear to be the case in T. sessile. In other cases, they may result from shifts in the frequency of particular genes, like in the red-imported fire ant, Solenopsis invicta, where colony structure is determined by the Gp-9 gene [71][73]. Alternatively, they may represent the facultative expression of a phenotype that for whatever reason is successful in new and disturbed environments, which appears to be the case in the little fire ant, Wasmannia auropunctata, in both its native and invasive range [62], [63]. This we suspect is the case for T. sessile. Surprisingly though, it remains unclear just what advantages such large multiqueen colonies bring ants [59], [60]. It may be that such colonies best take advantage of patchy environments in urban and disturbed habitats, but we know so little that it is difficult even to say if such habitats are more or less patchy from the perspective of ants. While we now know a great deal about some common invasive ant species such as the red-imported fire ant [73], the little fire ant [61][63], and Argentine ants [17], [74][80], T. sessile the most common ant in North America offers many remaining mysteries, from the West coast to the East coast and the deserts nearly all the way to the tundra, this species or group of species succeeds.

Supporting Information

Appendix S1.

List of all colonies used in the study, including the number of workers sequenced, Haplotype, Genbank accession number, and museum where physical specimens are deposited.

https://doi.org/10.1371/journal.pone.0009194.s001

(0.03 MB XLS)

Acknowledgments

We would like to thank G. Buczkowski, A.V. Suarez, A. Toennisson, B.P. Powell, S. Yanoviak, R.A. Johnson, L. Sanchez, M.D. Weiser, A. Ellison, J.T. Longino, P.S. Ward, R. Boulay, A. Lenoir, R.E. Sutton, J. Lund, S. King, T. Judd, S. Philpott, J. Shik, S. Kamble, D. Kimberling, D. Hilburn, and E. Spicer for sending us specimens; A. Smith for advice on molecular techniques; B. Wiegmann for help with analyses; P. Lester, Alex Smith, and two anonymous reviewers for comments on the manuscript.

Author Contributions

Conceived and designed the experiments: SM WB RRD JS. Performed the experiments: SM. Analyzed the data: SM WB. Contributed reagents/materials/analysis tools: SM WB RRD CS ELV JS. Wrote the paper: SM WB RRD CS ELV JS.

References

  1. 1. United Nations (2007) Population division world urbanization prospects: The 2007 revision. United Nations2007Population division world urbanization prospects: The 2007 revision.In: Affairs' UDoEaS, editor.
  2. 2. Williams JW, Jackson ST (2007) Novel climates, no-analog communities, and ecological surprises. Frontiers in Ecology and the Environment 5: 475–482.JW WilliamsST Jackson2007Novel climates, no-analog communities, and ecological surprises.Frontiers in Ecology and the Environment5475482
  3. 3. Williams JW, Jackson ST, Kutzbach JE (2007) Projected distributions of novel and disappearing climates by 2100 AD. PNAS 104: 5738–5742.JW WilliamsST JacksonJE Kutzbach2007Projected distributions of novel and disappearing climates by 2100 AD.PNAS10457385742
  4. 4. Thompson K, McCarthy MA (2008) Traits of British alien and native urban plants. Journal of Ecology 96: 853–859.K. ThompsonMA McCarthy2008Traits of British alien and native urban plants.Journal of Ecology96853859
  5. 5. Palumbi SR (2001) Evolution - Humans as the world's greatest evolutionary force. Science 293: 1786–1790.SR Palumbi2001Evolution - Humans as the world's greatest evolutionary force.Science29317861790
  6. 6. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, et al. (2000) Biotic invasions: Causes, epidemiology, global consequences, and control. Ecological Applications 10: 689–710.RN MackD. SimberloffWM LonsdaleH. EvansM. Clout2000Biotic invasions: Causes, epidemiology, global consequences, and control.Ecological Applications10689710
  7. 7. Shochat E, Warren PS, Faeth SH, McIntyre NE, Hope D (2006) From patterns to emerging processes in mechanistic urban ecology. Trends in Ecology & Evolution 21: 186–191.E. ShochatPS WarrenSH FaethNE McIntyreD. Hope2006From patterns to emerging processes in mechanistic urban ecology.Trends in Ecology & Evolution21186191
  8. 8. Dunn RR, Gavin MC, Sanchez MC, Solomon JN (2006) The pigeon paradox: dependence of global conservation on urban nature. Conservation Biology 20: 1814–1816.RR DunnMC GavinMC SanchezJN Solomon2006The pigeon paradox: dependence of global conservation on urban nature.Conservation Biology2018141816
  9. 9. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52: 273–288.D. PimentelR. ZunigaD. Morrison2005Update on the environmental and economic costs associated with alien-invasive species in the United States.Ecological Economics52273288
  10. 10. Lundholm J, Marlin A (2006) Habitat origins and microhabitat preferences of urban plant species. Urban Ecosystems 9: 139–159.J. LundholmA. Marlin2006Habitat origins and microhabitat preferences of urban plant species.Urban Ecosystems9139159
  11. 11. Marzluff JM, McGowan KJ, Donnelly R, Knight RL (2001) Causes and consequences of expanding American Crow populations. In: Marzluff JM, Bowman R, Donelly R, editors. Avian ecology and conservation in an urbanizing world. Norwell, MA: Kluwer Academic Press. pp. 332–363.JM MarzluffKJ McGowanR. DonnellyRL Knight2001Causes and consequences of expanding American Crow populations.JM MarzluffR. BowmanR. DonellyAvian ecology and conservation in an urbanizing worldNorwell, MAKluwer Academic Press332363
  12. 12. Miller JR, Hobbs RJ (2002) Conservation where people live and work. Conservation Biology 16: 330–337.JR MillerRJ Hobbs2002Conservation where people live and work.Conservation Biology16330337
  13. 13. LaSorte FA, Boecklen WJ (2005) Temporal turnover of common species in avian assemblages in North America. Journal of Biogeography 32: 1151–1160.FA LaSorteWJ Boecklen2005Temporal turnover of common species in avian assemblages in North America.Journal of Biogeography3211511160
  14. 14. Cremer S, Ugelvig LV, Drijfhout FP, Schlick-Steiner BC, Steiner FM, et al. (2008) The evolution of invasiveness in garden ants. PLoS ONE 3: e3838.S. CremerLV UgelvigFP DrijfhoutBC Schlick-SteinerFM Steiner2008The evolution of invasiveness in garden ants.PLoS ONE3e3838
  15. 15. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends in Ecology & Evolution 16: 199–204.CS KolarDM Lodge2001Progress in invasion biology: predicting invaders.Trends in Ecology & Evolution16199204
  16. 16. Novak SJ (2007) The role of evolution in the invasion process. Proceedings of the National Academy of Sciences 104: 3671–3672.SJ Novak2007The role of evolution in the invasion process.Proceedings of the National Academy of Sciences10436713672
  17. 17. Suarez AV, Holway DA, Tsutsui ND (2008) Genetics and behavior of a colonizing species: The invasive Argentine ant. The American Naturalist 172: S72–S84.AV SuarezDA HolwayND Tsutsui2008Genetics and behavior of a colonizing species: The invasive Argentine ant.The American Naturalist172S72S84
  18. 18. Hegglin D, Bontadina F, Contesse P, Gloor S, Deplazes P (2007) Plasticity of predation behaviour as a putative driving force for parasite life-cycle dynamics: the case of urban foxes and Echinococcus multilocularis tapeworm. Functional Ecology 21: 552–560.D. HegglinF. BontadinaP. ContesseS. GloorP. Deplazes2007Plasticity of predation behaviour as a putative driving force for parasite life-cycle dynamics: the case of urban foxes and Echinococcus multilocularis tapeworm.Functional Ecology21552560
  19. 19. Slabbekoorn H, Peet M (2003) Ecology: Birds sing at a higher pitch in urban noise. Nature 424: 267–267.H. SlabbekoornM. Peet2003Ecology: Birds sing at a higher pitch in urban noise.Nature424267267
  20. 20. Lockwood JL, Hoopes MF, Marchetti MP (2007) Invasion Ecology. Malden, MA: Blackwell Publishing. 304 p.JL LockwoodMF HoopesMP Marchetti2007Invasion Ecology.Malden, MABlackwell Publishing304
  21. 21. Folgarait PJ (1998) Ant biodiversity and its relationship to ecosystem functioning: a review. Biodiversity and Conservation 7: 1221–1244.PJ Folgarait1998Ant biodiversity and its relationship to ecosystem functioning: a review.Biodiversity and Conservation712211244
  22. 22. Sanford MP, Manley PN, Murphy DD (2009) Effects of urban development on ant communities: Implications for ecosystem services and management. Conservation Biology 23: 131–141.MP SanfordPN ManleyDD Murphy2009Effects of urban development on ant communities: Implications for ecosystem services and management.Conservation Biology23131141
  23. 23. Hedges SA (1998) Field Guide for the Management of Structure Infesting Ants; Moreland D, editor. Cleveland OH: G.I.E. Inc. 304 p.SA Hedges1998Field Guide for the Management of Structure Infesting Ants; Moreland D, editor.Cleveland OHG.I.E. Inc304
  24. 24. Smith MR (1965) House-infesting ants of the eastern United States. Their recognition, biology, and economic importance. Washington, D.C.: United States Department of Agriculture. 105 p.MR Smith1965House-infesting ants of the eastern United States. Their recognition, biology, and economic importance. Washington, D.C.: United States Department of Agriculture. 105
  25. 25. Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annual Review of Ecology and Systematics 33: 181–233.DA HolwayL. LachAV SuarezND TsutsuiTJ Case2002The causes and consequences of ant invasions.Annual Review of Ecology and Systematics33181233
  26. 26. Lowe S, Browne M, Boudjelas S, De Poorter M (2004) 100 of the World's Worst Invasive Alien Species: A selection from the Global Invasive Species Database. 12 p. S. LoweM. BrowneS. BoudjelasM. De Poorter2004100 of the World's Worst Invasive Alien Species: A selection from the Global Invasive Species Database.12The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN). The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN).
  27. 27. Smith MR (1928) The biology of Tapinoma sessile Say, an important house-infesting ant. Annals of the Entomological Society of America 21: 307–330.MR Smith1928The biology of Tapinoma sessile Say, an important house-infesting ant.Annals of the Entomological Society of America21307330
  28. 28. Scharf ME, Ratliff CR, Bennett GW (2004) Impacts of residual insecticide barriers on perimeter-invading ants, with particular reference to the Odorous house ant, Tapinoma sessile. Journal of Economic Entomology 97: 601–605.ME ScharfCR RatliffGW Bennett2004Impacts of residual insecticide barriers on perimeter-invading ants, with particular reference to the Odorous house ant, Tapinoma sessile.Journal of Economic Entomology97601605
  29. 29. Hedges SA (2000) Coast To Coast. PCT Onlinecom. SA Hedges2000Coast To Coast. PCT Onlinecom.
  30. 30. Buczkowski G, Bennett G (2006) Dispersed central-place foraging in the polydomous odorous house ant, Tapinoma sessile as revealed by a protein marker. Insectes Sociaux 53: 282–290.G. BuczkowskiG. Bennett2006Dispersed central-place foraging in the polydomous odorous house ant, Tapinoma sessile as revealed by a protein marker.Insectes Sociaux53282290
  31. 31. Barbani LE (2003) Foraging Activity and Food Preferences of the Odorous House Ant (Tapinoma sessile Say) (Hymenoptera: Formicidae). Blacksburg, Virginia. 76 p.LE Barbani2003Foraging Activity and Food Preferences of the Odorous House Ant (Tapinoma sessile Say) (Hymenoptera: Formicidae). Blacksburg, Virginia. 76
  32. 32. Buczkowski G, Bennett G (2008) Seasonal polydomy in a polygynous supercolony of the odorous house ant, Tapinoma sessile. Ecological Entomology 33: 780–788.G. BuczkowskiG. Bennett2008Seasonal polydomy in a polygynous supercolony of the odorous house ant, Tapinoma sessile.Ecological Entomology33780788
  33. 33. Milford ER (1999) Ant communities in flooded and unflooded riparian forest of the middle Rio Grande. The Southwestern Naturalist 44: 278–286.ER Milford1999Ant communities in flooded and unflooded riparian forest of the middle Rio Grande.The Southwestern Naturalist44278286
  34. 34. Fellers JH (1989) Daily and seasonal activity in woodland ants. Oecologia 78: 69–76.JH Fellers1989Daily and seasonal activity in woodland ants.Oecologia786976
  35. 35. Vogt JT, Reed JT, Brown RL (2004) Temporal foraging activity of selected ant species in northern Missippi during summer months. Journal of Entomological Science 39: 444–452.JT VogtJT ReedRL Brown2004Temporal foraging activity of selected ant species in northern Missippi during summer months.Journal of Entomological Science39444452
  36. 36. Fellers JH (1987) Interference and Exploitation in a Guild of Woodland Ants. Ecology 68: 1466–1478.JH Fellers1987Interference and Exploitation in a Guild of Woodland Ants.Ecology6814661478
  37. 37. Smallwood J (1982) Nest relocations in ants. Insectes Sociaux 29: 138–147.J. Smallwood1982Nest relocations in ants.Insectes Sociaux29138147
  38. 38. Hajibabaei M, Janzen DH, Burns JM, Hallwachs W, Hebert PDN (2006) DNA barcodes distinguish species of tropical Lepidoptera. Proceedings of the National Academy of Sciences of the United States of America 103: 968–971.M. HajibabaeiDH JanzenJM BurnsW. HallwachsPDN Hebert2006DNA barcodes distinguish species of tropical Lepidoptera.Proceedings of the National Academy of Sciences of the United States of America103968971
  39. 39. Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America 101: 14812–14817.PDN HebertEH PentonJM BurnsDH JanzenW. Hallwachs2004Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator.Proceedings of the National Academy of Sciences of the United States of America1011481214817
  40. 40. Copren KA, Nelson LJ, Vargo EL, Haverty MI (2005) Phylogenetic analyses of mtDNA sequences corroborate taxonomic designations based on cuticular hydrocarbons in subterranean termites. Molecular Phylogenetics and Evolution 35: 689–700.KA CoprenLJ NelsonEL VargoMI Haverty2005Phylogenetic analyses of mtDNA sequences corroborate taxonomic designations based on cuticular hydrocarbons in subterranean termites.Molecular Phylogenetics and Evolution35689700
  41. 41. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Mol Biol Evol 24: 1596–1599.K. TamuraJ. DudleyM. NeiS. Kumar2007MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0.Mol Biol Evol2415961599
  42. 42. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. JAA Nylander2004MrModeltest v2. Program distributed by the author.Evolutionary Biology Centre, Uppsala University. Evolutionary Biology Centre, Uppsala University.
  43. 43. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.F. RonquistJP Huelsenbeck2003MrBayes 3: Bayesian phylogenetic inference under mixed models.Bioinformatics1915721574
  44. 44. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1659.M. ClementD. PosadaKA Crandall2000TCS: a computer program to estimate gene genealogies.Molecular Ecology916571659
  45. 45. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. cladogram estimation. Genetics 132: 619–633.AR TempletonKA CrandallCF Sing1992A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. cladogram estimation.Genetics132619633
  46. 46. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47–50.L. ExcoffierG. LavalS. Schneider2005Arlequin (version 3.0): An integrated software package for population genetics data analysis.Evolutionary Bioinformatics Online14750
  47. 47. Huang J, Xu Q, Sun ZJ, Tang GL, Su ZY (2007) Identifying earthworms through DNA barcodes. Pedobiologia 51: 301–309.J. HuangQ. XuZJ SunGL TangZY Su2007Identifying earthworms through DNA barcodes.Pedobiologia51301309
  48. 48. Landry B, Powell JA, Sperling FAH (1999) Systematics of the Argyrotaenia fianciscana (Lepidoptera: Tortricidae) species group: Evidence from mitochondrial DNA. Annals of the Entomological Society of America 92: 40–46.B. LandryJA PowellFAH Sperling1999Systematics of the Argyrotaenia fianciscana (Lepidoptera: Tortricidae) species group: Evidence from mitochondrial DNA.Annals of the Entomological Society of America924046
  49. 49. Ascunce MS, Ernst JA, Clark A, Nigg HN (2008) Mitochondrial Nucleotide Variability in Invasive Populations of the Root Weevil Diaprepes abbreviatus (Coleoptera: Curculionidae) of Florida and Preliminary Assessment of Diaprepes sp. from Dominica. Journal of Economic Entomology 101: 1443–1454.MS AscunceJA ErnstA. ClarkHN Nigg2008Mitochondrial Nucleotide Variability in Invasive Populations of the Root Weevil Diaprepes abbreviatus (Coleoptera: Curculionidae) of Florida and Preliminary Assessment of Diaprepes sp. from Dominica.Journal of Economic Entomology10114431454
  50. 50. Wilcox TP, Hugg L, Zeh JA, Zeh DW (1997) Mitochondrial DNA sequencing reveals extreme genetic differentiation in a cryptic species complex of Neotropical Pseudoscorpions. Molecular Phylogenetics and Evolution 7: 208–216.TP WilcoxL. HuggJA ZehDW Zeh1997Mitochondrial DNA sequencing reveals extreme genetic differentiation in a cryptic species complex of Neotropical Pseudoscorpions.Molecular Phylogenetics and Evolution7208216
  51. 51. Wild AL (2009) Evolution of the Neotropical ant genus Linepithema. Systematic Entomology 34: 49–62.AL Wild2009Evolution of the Neotropical ant genus Linepithema.Systematic Entomology344962
  52. 52. Avise JC, Walker D (1999) Species realities and numbers in sexual vertebrates: Perspectives from an asexually transmitted genome. Proceedings of the National Academy of Sciences of the United States of America 96: 992–995.JC AviseD. Walker1999Species realities and numbers in sexual vertebrates: Perspectives from an asexually transmitted genome.Proceedings of the National Academy of Sciences of the United States of America96992995
  53. 53. Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM (2004) Identification of birds through DNA barcodes. PLoS Biology 2: 1657–1663.PDN HebertMY StoeckleTS ZemlakCM Francis2004Identification of birds through DNA barcodes.PLoS Biology216571663
  54. 54. Wiemers M, Fiedler K (2007) Does the DNA barcoding gap exist? - a case study in blue butterflies (Lepidoptera: Lycaenidae). Frontiers in Zoology 4: 8.M. WiemersK. Fiedler2007Does the DNA barcoding gap exist? - a case study in blue butterflies (Lepidoptera: Lycaenidae).Frontiers in Zoology48
  55. 55. Fisher BL, Smith MA (2008) A Revision of Malagasy species of Anochetus Mayr and Odontomachus Latreille (Hymenoptera: Formicidae). PLoS ONE 3: e1787.BL FisherMA Smith2008A Revision of Malagasy species of Anochetus Mayr and Odontomachus Latreille (Hymenoptera: Formicidae).PLoS ONE3e1787
  56. 56. Smith MA, Umphrey GJ, Fisher BL, Hebert PD (2005) Rapid assessment of ant diversity in a northern world heritage site using DNA barcodes, Poster. MA SmithGJ UmphreyBL FisherPD Hebert2005Rapid assessment of ant diversity in a northern world heritage site using DNA barcodes, Poster.The Natural History Museum. London, UK. The Natural History Museum. London, UK.
  57. 57. Hamm CA (2008) Phylogeography of Tapinoma sessile in California. Fresno: California State University, Fresno. 58 p.CA Hamm2008Phylogeography of Tapinoma sessile in California.FresnoCalifornia State University, Fresno58
  58. 58. Fisher BL, Cover SP (2007) Ants of North America: A Guide to the Genera. Berkeley, CA: University of California Press. 194 p.BL FisherSP Cover2007Ants of North America: A Guide to the Genera. Berkeley, CA: University of California Press. 194
  59. 59. Hölldobler B, Wilson EO (1977) The number of queends: an important trait in ant evolution. Naturwissenschaften 64: 8–15.B. HölldoblerEO Wilson1977The number of queends: an important trait in ant evolution.Naturwissenschaften64815
  60. 60. Helanterä H, Strassmann JE, Carrillo J, Queller DC (2009) Unicolonial ants: where do they come from, what are they and where are they going? Trends in Ecology & Evolution 24: 341–349.H. HelanteräJE StrassmannJ. CarrilloDC Queller2009Unicolonial ants: where do they come from, what are they and where are they going?Trends in Ecology & Evolution24341349
  61. 61. Keller L (2007) Uncovering the biodiversity of genetic and reproductive systems: time for a more open approach. The American Naturalist 169: 1–8.L. Keller2007Uncovering the biodiversity of genetic and reproductive systems: time for a more open approach.The American Naturalist16918
  62. 62. Foucaud J, Fournier D, Orivel J, Delabie JHC, Loiseau A, et al. (2007) Sex and clonality in the Little Fire Ant. Molecular Biology and Evolution 24: 2465–2473.J. FoucaudD. FournierJ. OrivelJHC DelabieA. Loiseau2007Sex and clonality in the Little Fire Ant.Molecular Biology and Evolution2424652473
  63. 63. Foucaud J, Orivel J, Fournier D, Delabie JHC, Loiseau A, et al. (2009) Reproductive system, social organization, human disturbance and ecological dominance in native populations of the little fire ant, Wasmannia auropunctata. Molecular Ecology. J. FoucaudJ. OrivelD. FournierJHC DelabieA. Loiseau2009Reproductive system, social organization, human disturbance and ecological dominance in native populations of the little fire ant, Wasmannia auropunctata.Molecular Ecology
  64. 64. Holway DA (1999) Competitive mechanisms underlying the displacement of native ants by the invasive Argentine ant. Ecology 80: 238–251.DA Holway1999Competitive mechanisms underlying the displacement of native ants by the invasive Argentine ant.Ecology80238251
  65. 65. Thompson B, McLachlan S (2007) The effects of urbanization on ant communities and myrmecochory in Manitoba, Canada. Urban Ecosystems 10: 43–52.B. ThompsonS. McLachlan2007The effects of urbanization on ant communities and myrmecochory in Manitoba, Canada.Urban Ecosystems104352
  66. 66. Bristow CM (1984) Differential Benefits from Ant Attendance to Two Species of Homoptera on New York Ironweed. The Journal of Animal Ecology 53: 715–726.CM Bristow1984Differential Benefits from Ant Attendance to Two Species of Homoptera on New York Ironweed.The Journal of Animal Ecology53715726
  67. 67. Chapman RE, Bourke AFG (2001) The influence of sociality on the conservation biology of social insects. Ecology Letters 4: 650–662.RE ChapmanAFG Bourke2001The influence of sociality on the conservation biology of social insects.Ecology Letters4650662
  68. 68. Vargo EL, Husseneder C (2009) Biology of subterranean termites: insights from molecular studies of Reticulitermes and Coptotermes. Annual Review of Entomology 54: 379–403.EL VargoC. Husseneder2009Biology of subterranean termites: insights from molecular studies of Reticulitermes and Coptotermes.Annual Review of Entomology54379403
  69. 69. Tsutsui ND, Suarez AV, Holway DA, Case TJ (2000) Reduced genetic variation and the success of an invasive species. Proceedings of the National Academy of Sciences of the United States of America 97: 5948–5953.ND TsutsuiAV SuarezDA HolwayTJ Case2000Reduced genetic variation and the success of an invasive species.Proceedings of the National Academy of Sciences of the United States of America9759485953
  70. 70. Tsutsui ND, Suarez AV, Holway DA, Case TJ (2001) Relationships among native and introduced populations of the Argentine ant (Linepithema humile) and the source of introduced populations. Molecular Ecology 10: 2151–2161.ND TsutsuiAV SuarezDA HolwayTJ Case2001Relationships among native and introduced populations of the Argentine ant (Linepithema humile) and the source of introduced populations.Molecular Ecology1021512161
  71. 71. Ross KG, Vargo EL, Keller L (1996) Social evolution in a new environment: the case of introduced fire ants. Proceedings of the National Academy of Sciences of the United States of America 93: 3021–3025.KG RossEL VargoL. Keller1996Social evolution in a new environment: the case of introduced fire ants.Proceedings of the National Academy of Sciences of the United States of America9330213025
  72. 72. Gotzek D, Ross Kenneth G (2007) Genetic regulation of colony social organization in fire ants: an integrative overview. The Quarterly Review of Biology 82: 201–226.D. GotzekG. Ross Kenneth2007Genetic regulation of colony social organization in fire ants: an integrative overview.The Quarterly Review of Biology82201226
  73. 73. Tschinkel WR (2006) The Fire Ants. Cambridge, MA: The Belknap Press of Harvard University Press. 723 p.WR Tschinkel2006The Fire Ants.Cambridge, MAThe Belknap Press of Harvard University Press723
  74. 74. Tsutsui ND, Suarez AV, Grosberg RK (2003) Genetic diversity, asymmetrical aggression, and recognition in a widespread invasive species. Proceedings of the National Academy of Sciences of the United States of America 100: 1078–1083.ND TsutsuiAV SuarezRK Grosberg2003Genetic diversity, asymmetrical aggression, and recognition in a widespread invasive species.Proceedings of the National Academy of Sciences of the United States of America10010781083
  75. 75. Giraud T, Pedersen JS, Keller L (2002) Evolution of supercolonies: The Argentine ants of southern Europe. Proceedings of the National Academy of Sciences of the United States of America 99: 6075–6079.T. GiraudJS PedersenL. Keller2002Evolution of supercolonies: The Argentine ants of southern Europe.Proceedings of the National Academy of Sciences of the United States of America9960756079
  76. 76. Roura-Pascual N, Suarez AV, Gomez C, Pons P, Touyama Y, et al. (2004) Geographical potential of Argentine ants (Linepithema humile Mayr) in the face of global climate change. Proceedings of the Royal Society of London Series B-Biological Sciences 271: 2527–2534.N. Roura-PascualAV SuarezC. GomezP. PonsY. Touyama2004Geographical potential of Argentine ants (Linepithema humile Mayr) in the face of global climate change.Proceedings of the Royal Society of London Series B-Biological Sciences27125272534
  77. 77. Holway DA, Suarez AV (2004) Colony-structure variation and interspecific competitive ability in the invasive Argentine ant. Oecologia 138: 216–222.DA HolwayAV Suarez2004Colony-structure variation and interspecific competitive ability in the invasive Argentine ant.Oecologia138216222
  78. 78. Thomas ML, Payne-Makrisa CM, Suarez AV, Tsutsui ND, Holway DA (2006) When supercolonies collide: territorial aggression in an invasive and unicolonial social insect. Molecular Ecology 15: 4303–4315.ML ThomasCM Payne-MakrisaAV SuarezND TsutsuiDA Holway2006When supercolonies collide: territorial aggression in an invasive and unicolonial social insect.Molecular Ecology1543034315
  79. 79. Menke SB, Fisher RN, Jetz W, Holway DA (2007) Biotic and abiotic controls of Argentine ant invasion success at local and landscape scales. Ecology 88: 3164–3173.SB MenkeRN FisherW. JetzDA Holway2007Biotic and abiotic controls of Argentine ant invasion success at local and landscape scales.Ecology8831643173
  80. 80. Walters AC, Mackay DA (2005) Importance of large colony size for successful invasion by Argentine ants (Hymenoptera: Formicidae): Evidence for biotic resistance by native ants. Austral Ecology 30: 395–406.AC WaltersDA Mackay2005Importance of large colony size for successful invasion by Argentine ants (Hymenoptera: Formicidae): Evidence for biotic resistance by native ants.Austral Ecology30395406