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A N D R E W V . S U A R E Z * and N E I L D . T S U T S U I †‡
*Department of Animal Biology and Department of Entomology, University of Illinois, 320 Morrill Hall, 505 South Goodwin Avenue,
Urbana, IL 61801, USA, †Department of Ecology and Evolutionary Biology, University of California at Irvine, 321 Steinhaus Hall,
Irvine, CA 92697-2525, USA
Abstract
A major challenge of invasion biology is the development of a predictive framework that
prevents new invasions. This is inherently difficult because different biological character-
istics are important at the different stages of invasion: opportunity/transport, establish-
ment and spread. Here, we draw from recent research on a variety of taxa to examine the
evolutionary causes and consequences of biological invasions. The process of introduction
may favour species with characteristics that promote success in highly disturbed, human-
dominated landscapes, thus exerting novel forms of selection on introduced populations.
Moreover, evidence is accumulating that multiple introductions can often be critical to the
successful establishment and spread of introduced species, as they may be important
sources of genetic variation necessary for adaptation in new environments or may permit
the introduction of novel traits. Thus, not only should the introduction of new species be
prevented, but substantial effort should also be directed to preventing the secondary
introduction of previously established species (and even movement of individuals among
introduced populations). Modern molecular techniques can take advantage of genetic
changes postintroduction to determine the source of introduced populations and their
vectors of spread, and to elucidate the mechanisms of success of some invasive species.
Moreover, the growing availability of genomic tools will permit the identification of
underlying genetic causes of invasive success.
Keywords: adaptation, behaviour, genetic drift, hybridization, invasive species
history, the ecological shuffling associated with biological plants possess adaptations for long-distance dispersal that
invasions is extraordinarily rapid and can be geographi- likely increase the probability of being transported by
cally widespread. Thus, in many cases both the native and humans, either deliberately or inadvertently (reviewed in
introduced species must adapt quickly or risk extirpation. Levin 2006). By increasing propagule pressure not only
For example, when species are introduced to an envi- do these adaptations increase the probability of introduction,
ronment that is abiotically unsuitable, they may lack but the continued introduction of additional propagules
the genetic variation required for rapid adaptation to after establishment can facilitate invasiveness by
the new circumstances. Likewise, native species in an reducing potentially harmful Allee effects, increasing
invaded habitat may lack defences to a newly introduced genetic diversity, introducing novel genotypes and
predator, competitor or pathogen due to the absence phenotypes, and permitting further adaptive evolution
of a coevolutionary history between the two (e.g. Payne (see below).
et al. 2004; Schlaepfer et al. 2005). Similar characteristics are often observed in invasive
It is also important to remember that biological invasions animals. Many invasive ant species, for example, nest
occur as a multistage process that includes the acquisition ephemerally and have a temporally and spatially fluid
of a propagule in its native range, transport of that propagule colony structure, which allows them to rapidly move their
to a new range, and the introduction, establishment and colonies in response to changing environmental conditions
spread of the invader in the new habitat. Each stage of this (e.g. rising floodwaters, the appearance of a temporary
process poses new challenges and imposes different types food resource; Holway & Case 2000; Holway et al. 2002a).
of selection (Sakai et al. 2001). Each stage thus acts as a When associated with humans, however, this habit translates
filter, weeding out species that lack the characteristics into frequent introduction to new locales, as the ants colonize
needed for survival or the variation necessary for adaptation items that are transported by humans (such as trash, soil or
to novel selection pressures. potted plants), often across long distances (Suarez et al.
In this review, we discuss the role of evolutionary 2001; Suarez et al. 2005). Moreover, many invasive ants
processes in biological invasions in the context of the are characterized by a polygyne colony structure, where
different stages of this process. Specifically, we examine multiple reproductive queens are present in each colony.
the importance of the following evolutionary mechanisms: Thus, when colony fragments are accidentally moved
(i) preadaptation of invasive species in their native range; by humans, there is a high probability that the propagule
(ii) evolution of invasive species in their introduced range; will contain reproductive individuals, and thus be
and (iii) introduced species as a selective force on native viable in the new habitat (Hee et al. 2000; Tsutsui & Suarez
species. We propose that taking an evolutionary approach 2003); whether these characteristic are overrepresented
to the study of biological invasions will provide important among invasive ants relative to ants as a whole remains
insights into both mechanisms of success and their to be tested.
consequences. Moreover, we argue that the efficacy of Having a shared history with humans may also make a
future strategies for the prevention and control of species more likely to invade new environments (Elton
invasive species will hinge on an understanding of the 1958). In addition to being preadapted to human modified
evolutionary processes that are involved in successful landscapes, a close association with humans increases the
invasions. probability of transport through a variety of anthropogenic
vectors (Crooks & Suarez 2006). For example, many intro-
duced insects in North America come from Europe where
The evolution and preadaptation of introduced
they have coevolved with human land practices for hundreds
species in their native range, prior to introduction
of generations and many potential host genera are similar
In general, the species that become successful invaders are between the regions (Elton 1958; Sailer 1978). Interestingly,
not a random sampling of biodiversity. Instead, successful ant invasions into North America do not follow this pattern
invaders are predicted to be species that, in their native (Suarez et al. 2005).
ranges, have evolved traits that predispose them to be When attempting to predict where potential invaders
transported by humans and successfully survive the will be successful, it would be useful to assess how well
selection regimes encountered during transport, introduction, conditions in the native range (which have driven the
establishment and spread. These predictions are borne out historical evolution of the species) match conditions in a
by analyses of invasive vs. noninvasive species. In pines potential introduced range. Because introduced propagules
(Pinus), for example, successful invaders possess characteristics may be more likely to succeed in habitats similar to those
associated with effective dispersal and increased propagule they evolved in, in depth knowledge about both ranges
pressure: high growth rates, consistent and regular repro- may allow for more accurate predictions. Unfortunately,
duction, and small seed masses (Rejmanek & Richardson for many invasive species we know little about their
1996; Grotkopp et al. 2002). Similarly, many other invasive ecology or genetics in native populations.
North America, for example, are characterized by genetic secondary introduction of C. maenas from the native range.
patterns consistent with multiple introductions from Finally, Kolbe and colleagues (Kolbe et al. 2004) show that
different locations in the native range (Kolbe et al. 2004; introduced populations of the lizard, Anolis sangrei, are
Kolbe et al. 2007). Moreover, morphological differentiation more diverse than natives. Future research demonstrating
among introduced populations appears to be a product the benefits of increased genetic diversity in introduced
of differential admixture from this handful of sources populations is still needed to determine its role in invasion
(Kolbe et al. 2007). success post-establishment.
Social insects, which include many successful invasive Equally importantly, individuals in these populations
species, may be particularly sensitive to microevolutionary may possess alleles in combinations that do not exist in the
changes during and after introduction. Not only do these native range, thus increasing the likelihood of novel epistatic
species often have a relatively small number of reproductive interactions or the expression of new phenotypes. In a
individuals, but the hymenopteran social insects also recent study of the invasive reed canarygrass, Phalaris
possess small effective population sizes as a consequence arundinacea, Lavergne & Molofsky (2007; reviewed by
of their haplodiploid genetic system. Moreover, the system Novak 2007) conducted population genetic analyses of
of complimentary (single-locus) sex determination (CSD) native and introduced populations from both the centre
in the hymenoptera may make them particularly vulnerable and the periphery of each range. These data showed that
to losses of genetic diversity. Because heterozygotes at this introduced populations, regardless of their location, had
locus become females and hemizygotes and homozygotes higher levels of genetic diversity than native populations
become males (Crozier 1977), high levels of allelic diversity and possessed many alleles that were not seen in the native
are necessary for this system to operate properly (Beye populations sampled. Also notable is the fact that the vast
et al. 2003). One consequence of having a small founding majority of multilocus genotypes in the introduced range
population followed by inbreeding is the production of were not seen in the native range, indicating admixture
diploid males. Diploid males are often sterile and can among multiple genetically different introductions.
impose a huge cost to the colony (Zayed & Packer 2005). A thorough genetic examination of multiple introduc-
Evidence for diploid male production in introduced social tions is the recent study of the honeybee, Apis mellifera,
insects has been detected in nearly 40 species of Hymen- using > 1100 single nucleotide polymorphism (SNP) loci
optera (Cook 1993; Crozier & Pamilo 1996), including (Whitfield et al. 2006). This species, native to Africa, Europe
in introduced populations of Polistes wasps (Liebert et al. and Asia, was first introduced (deliberately) to the New World
2004; Liebert et al. 2005), the honeybee (Apis mellifera, e.g. in the 1600s, and it has since become the leading pollinator
Drescher & Rothenbuhler 1964), the Argentine ant of many plants, including a number of agriculturally
(Linepithema humile, Tsutsui et al. 2003), and the red important crops (Delaplane 2000). Historical records
imported fire ant (Solenopsis invicta, Ross & Fletcher 1985). suggest that the first introduced hives were ‘German black
bees’, the subspecies A. m. mellifera (Sheppard 1989). Since
then, however, a number of other subspecies have been
Hybridization within and among species
introduced, including the ‘Italian’ bees, A. m. ligustica and
When multiple introductions of a species occur, introduced A. m. carnica (Sheppard 1989), and the infamous African
populations may attain higher levels of genetic diversity ‘killer’ bee (A. m. scutellata), which was accidentally released
than native populations. This is particularly likely when in Brazil in 1956 (Sheppard & Smith 2000; Schneider et al.
the sources of introduced propagules are genetically 2004). The spread of Africanized honeybees since their
divergent native populations. Accordingly, a number of introduction has been a cause for concern for human
genetic studies have shown that intraspecific hybridization health, apiculture and agriculture. The SNP analysis of
among successively introduced populations may provide Whitfield and colleagues examined 14 subspecies in the
the genetic variation necessary for adaptive evolution to native range (including the aforementioned four) and
occur, and may thus be a critically important determinant showed that native populations fall into several well-
of invasive success (Ellstrand & Schierenbeck 2000). For defined, genetically distinct groups. Assignment of intro-
example, Chen et al. (2006) used microsatellite markers to duced bees to these native populations revealed that, for
show that both genetic diversity and the number of private the most part, they are a genetic amalgamation of the succes-
alleles are higher in some introduced Rhagoletis completa sive introductions of various subspecies. Interestingly, the
populations, suggesting that multiple introductions introduction and spread of Africanized honeybees (A. m.
have occurred. Similarly, Roman (2006) used cytochrome scutellata) has affected some parts of the genome more than
oxidase I (COI) mitochondrial DNA (mtDNA) sequence others – alleles descended from A. m. mellifera have been
data to show that a recent northward range expansion of retained at far higher rates than alleles descended from
introduced the European green crab (Carninus maenas) in A. m. ligustica or A. m. carnica. Because the SNPs examined
the northeastern United States was probably caused by a reside within expressed genes, these types of genome-wide
SNP-based studies offer great hope for teasing out genes of is native to the east coast of North America where is it
functional importance for interesting phenotypes, including preyed upon by several species of crabs, including the
behaviours, morphologies and life histories associated with long-established European green crab, Carcinus maenas.
invasive success. Mussels from throughout the range display an inducible
Another potential source of genetic variation is hybridi- defence to the presence of this crab predator — the mussels
zation between introduced and native species in the new grow thicker shells when exposed to waterborne cues that
range. In the San Francisco Bay area, for example, four indicate the presence of the crabs (e.g. Leonard et al. 1999).
different species of Spartina cordgrass have been These thicker shells likely provide greater protection from
introduced from native ranges in Europe, Chile and the attacks by the crabs. More recently, however, another
Eastern seaboard of North America (Ayres et al. 2004). non-native crab species, the Asian shore crab (Hemigrapsus
Since their introduction, some of these species have spread sanguineus), has become established in the region (McDermott
widely and, in some cases, have hybridized with the native 1991). Mussels that co-occur with H. sanguineus in southern
cordgrass, S. foliosa (Daehler & Strong 1997). Genetic stud- New England display the same inducible defence in the
ies using chloroplast DNA markers, for example, have presence of H. sanguineus, but mussels from farther north
shown that the introduced S. alterniflora has hybridized (in allopatry with H. sanguineus) do not (Freeman & Byers
with the native S. foliosa (Anttila et al. 2000), resulting in 2006). These data suggest that in the short time since the
highly invasive clones that then displace the native Asian shore crab’s introduction the southern mussels have
parental species (Gray et al. 1991). In Great Britain, hybrid- evolved the ability to detect and respond defensively,
ization between the native S. maritima and the introduced whereas the naïve mussels have not (Freeman & Byers 2006).
S. alterniflora has given rise to the allopolyploid invasive S. In some cases, invasive species can radically alter abiotic
anglica. Although this invasive reproduces clonally, and and biotic characteristics of ecosystems, thus changing
thus has virtually no interindividual genetic variation, it the strength and form of selection on the species therein
possesses extremely high levels of within-individual (e.g. O’Dowd et al. 2003). The presence of some invasive
genetic variation and heterosis as a result of its hybrid grasses, for example, can alter fire frequencies in their
origin (Ellstrand & Schierenbeck 2000). introduced range, thus producing changes in community
Although it is clear that interspecific hybridization can composition and nutrient cycling, and further altering the
occur between both introduced and native species as well frequency of future fires (reviewed by D’Antonio &
as between two different invaders, it is difficult to estimate Vitousek 1992; Brooks et al. 2004). Other invasive plants
the relative frequencies of these events. However, work by can exude toxic chemicals into the soil, thus creating
Stace (1991) documenting the 2834 plant species that occur conditions that are intolerable for sensitive native plant
in the British Isles provides some insights (reviewed by species (Bais et al. 2002; Bais et al. 2003). Invasive vertebrate
Abbott 1992). Of this number, Stace estimated that 1264 ‘ecosystem engineers’ can similarly cause extreme ecological
(~45%) are introduced species and 21 (~2%) are the changes (Wright & Jones 2006). The large-scale perturba-
product of hybridization between two different introduced tions of fundamental habitat characteristics likely produce
species. About 62% of these hybrids have some docu- myriad simultaneous shifts in natural selection for all
mented level of fertility. Moreover, 70 species were judged species involved, and we are only beginning to understand
to have arisen from hybridization between an introduced the nature and extent of the evolutionary responses.
plant and a native species, and four resulted from hybrid-
ization between a hybrid and a native species. Nearly half
Mutualism and facilitation
of the hybrids between a native and introduced plant
showed some evidence of fertility. Mutualism and facilitation are becoming widely recog-
nized as important evolutionary forces that contribute to
the success of invaders (Simberloff & Von Holle 1999;
Introduced species as a selective pressure on native
Richardson et al. 2000; Bruno et al. 2003). Native species
species
that facilitate one another, for example, may be able to
There is a rich and voluminous body of research documenting better resist invaders (Bruno et al. 2003). In contrast,
the negative consequences of invasive species on native facilitative and mutualistic interactions among introduced
taxa in their introduced ranges (Parker et al. 1999; Mack species can lead to invasional meltdown: more severe
et al. 2000). However, studies that examine the nature and ecological impacts than those expected if the invaders did
strength of selection exerted by the invaders are rarer. not synergistically interact with one another (Simberloff &
Recent studies of an introduced crab illustrate the selective Von Holle 1999).
force that invasive species can bring to bear on native The growing number of empirical studies on facilitation
species and demonstrate how adaptive responses may act and invasion illustrates an impressive array of possible
to ameliorate this selection. The blue mussel, Mytilus edulis, interactions and potential for selection. Direct interactions
manuscript. Funding was provided by the United States Chen YH, Opp SB, Berlocher SH, Roderick GK (2006) Are
Department of Agriculture (NRI-CGP 2004-3502-14865; to NDT), bottlenecks associated with colonization? Genetic diversity and
the California Department of Consumer Affairs and the Structural diapause variation of native and introduced Rhagoletis completa
Pest Control Board (NDT) and the National Science Foundation populations. Oecologia, 149, 656–667.
(DEB 0516452, to AVS). Christian CE (2001) Consequences of a biological invasion reveal
the importance of mutualism for plant communities. Nature
(London), 413, 635–639.
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California. Ecological Applications, 10, 711–725. invader: the marsh frog Rana ridibunda. Britain. Molecular
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biological invasions dominated by long-distance jump dispersal:
insights from Argentine ants. Proceedings of the National Academy
of Sciences of the United States of America, 98, 1095 –1100. Andrew Suarez loves grooming, pursuing small prey items and
Suarez AV, Holway DA, Ward PS (2005) The role of opportunity sunning himself on south-facing stones. Neil Tsutsui is an evolu-
in the unintentional introduction of nonnative ants. Proceedings tionary biologist whose research interests include behavioural
of the National Academy of Sciences of the United States of America, ecology, chemical ecology and genetics.
102, 17032–17035.