1 | INTRODUCTION
The transport of species beyond their native ranges by human actions is
breaking down biogeographical barriers and causing global reorganization
of biota (Capinha et al. 2015,
van Kleunen et al. 2015), with the
ensuing invasions posing a serious threat to biodiversity, agriculture
and human health (Simberloff et al.
2013). Successful invaders must disperse into a geographically distant
area, establish a viable and fertile population, and spread throughout
this new environment, where the biotic and abiotic pressures may differ
from those they faced in their native range
(Kolar and Lodge 2001). This invasion
pathway occurs despite the reduction of genetic diversity that typically
follows introductions of invasive species, which is usually associated
with inbreeding costs and a loss of adaptive potential. For these
reasons, invasions are often seen as paradoxical, since invaders are
able to overcome these costs to become ecologically dominant in their
novel environment, outcompeting native species adapted to local
ecological conditions (Sax and Brown
2000, Facon et al. 2006).
Several life-history traits of invaders may favor them over the course
of their invasion. Specific breeding systems, modes of dispersal or
physiological characteristics may influence their ability to spread and
their establishment success, which thus enhance their colonization rate.
Exploring invasion mechanisms relies on unraveling whether these traits
differ between introduced and native populations. These differences may
result from evolutionary events occurring in the invaded population
during the initial phase of introduction
(Wares et al. 2005), evolving after the
introduction due to new ecological pressures
(Keller and Taylor 2008), or may already
be present within native populations, thereby pre-adapting the source
population for invasion success. Therefore, determining the source
population of invasive species is critical to conduct comparative
studies of life-history traits between introduced and native ranges to
understand how they evolved under distinct biotic and abiotic pressures.
Exploring invasion mechanisms also requires assessment of the invasion
history, in which a series of demographic events may influence the
invasion process and patterns of genetic diversity. A simple invasion
history may be the result of a single introduction from the native
range; however, an invasive population may also stem from multiple
introductions out of the native range, either from the same or different
source populations. Similarly, distinct invasive populations may stem
from different introduction events from one source population, or from
different source populations from the native range. Finally, a
successful invasive population itself may become a source for subsequent
invasions -a phenomenon coined the ‘bridgehead effect’(Lombaert et al. 2010,
Bertelsmeier and Keller 2018). Therefore,
distinct invasion histories have different outcomes in terms of patterns
of genetic diversity and life-history trait evolution. The bottleneck
event following an introduction usually results in a loss of genetic
diversity in the introduced population
(Dlugosch and Parker 2008), but the
amount of genetic diversity lost may vary under different invasion
histories. The reduction of genetic diversity may be limited when the
initial colonizing force is large, when the introduced population is
subsequently re-invaded by additional individuals during multiple
introduction events, or when the introduced population is invaded by
individuals from several genetically distinct source populations
(Facon et al. 2006). In rare cases, when
there are several introductions from different source populations and
these interbreed within an invasive population, genetic diversity may
even be higher within this population than its native source populations
(Facon et al. 2008). In contrast, the
bridgehead effect may result in a severe loss of diversity, as
subsequent introductions arise from an already depauperate introduced
population. However, the bridgehead effect may promote the spread of
phenotypic traits enhancing invasion success in secondary invasive
populations, as these traits are already selected for and widespread in
the initial introduced population. Investigating patterns of genetic
diversity in native and introduced populations can therefore provide
information on the invasion history of invasive species.
Reticulitermes flavipes is a subterranean termite species native
from Texas to Massachusetts in the eastern USA. The termite has become
invasive in localities both near to and distant from the eastern USA.
This includes the western USA (Austin et
al. 2005, McKern et al. 2006), the
Province of Ontario in Canada (Kirby
1965), the Bahamas (Scheffrahn et al.
1999), Chile (Clément et al. 2001) and
Uruguay in South America (Austin et al.
2005, Su et al. 2006) and France,
Germany, Austria and Italy in western Europe
(Kollar 1837,
Weidner 1937,
Clément et al. 2001,
Ghesini et al. 2010). Previous genetic
analysis based on microsatellite markers and mtDNA haplotypes have shown
that the introduced French population exhibits an average decrease in
genetic diversity of 60-80% compared to native USA populations
(Perdereau et al. 2013). The analysis
also revealed the occurrence of three main genetic clusters within the
native USA range -the ‘Eastern cluster’ (West Virginia, Virginia,
Delaware, North and South Carolina), the ‘Gulf Coast cluster’ (Florida
and Eastern Mississippi–Louisiana) and the ‘Southern Louisiana cluster’
(the New Orleans and Baton Rouge regions in Louisiana)
(Perdereau et al. 2013). Notably, some
microsatellite and mtDNA haplotypes found in France were unique to the
Southern Louisiana cluster (Perdereau et
al. 2013). This finding, together with a similarity in chemical
profiles and breeding structures found between France and Louisiana
(Perdereau et al. 2010b,
Perdereau et al. 2015), suggested thatR. flavipes was introduced to France from Louisiana, most likely
during the 17th and 18th centuries via wood trade between New Orleans
and the major French ports on the Atlantic coast
(Dronnet et al. 2005,
Perdereau et al. 2010a,
Perdereau et al. 2013). Although the
Louisiana origin of the invasive French population appears well
supported, several points remain unclear. First, Perdereau et al.
(2019) recently identified a French
haplotype more closely related to the ‘Eastern cluster’ than Louisiana,
suggesting multiple native populations from the USA may have invaded
France. Additionally, the source(s) of the Canadian and Chilean
invasions remain unidentified. Although several populations of R.
flavipes occur in the Northeastern and Midwestern USA (i.e.,adjacent to Ontario), the only haplotype found in Canada was shared with
Louisiana and France (Perdereau et al.
2013). Therefore, it is unclear whether the Canadian population arose
from a primary introduction from Louisiana or from a secondary
introduction through France (i.e., bridgehead introduction), as
Canada and France share a long common history. Similarly, Chile’s unique
haplotype was closest to one shared between Louisiana and France
(Perdereau et al. 2013), raising the same
question regarding primary versus secondary introduction. Overall, these
findings suggest a complex invasion history for R. flavipes and
raise the question of how many native populations may have served as
sources of the introduced populations and what the role of bridgeheads
might be in the global distribution of this species.
Substantial variability in breeding structure is present among the
native USA populations of R. flavipes . Most populations are
comprised of colonies headed by a monogamous pair of primary
(alate-derived) reproductives (simple family). However, some populations
are mainly comprised of colonies headed by a few secondary reproductives
(i.e., nymph-derived neotenics; extended-family), and other
populations comprised of fused colonies (mixed-family colonies)
(Vargo and Husseneder 2009,
Vargo et al. 2013,
Aguero et al. 2020). Interestingly, the
French introduced population of R. flavipes differs from most
native populations, exhibiting a set of ‘invasive’ traits that enable
colonies to form amplified versions of the extended and mixed-family
forms. French colonies contain several hundred secondary reproductives
and are usually spatially expansive
(Dronnet et al. 2005,
Vargo and Husseneder 2009,
Perdereau et al. 2010a). They display
highly similar chemical signatures, which reduces intraspecific
antagonism between non-nestmate workers and allows for frequent fusions
between colonies (Bagneres et al. 1990,
Clément et al. 2001,
Perdereau et al. 2010a,
Perdereau et al. 2010b). Interestingly,
this set of phenotypic traits occurs to a lesser extent in a population
from Louisiana (Vargo 2019), which may
have enhanced the invasion success of this introduced population in
France (Perdereau et al. 2010a,
Perdereau et al. 2010c,
Perdereau et al. 2015). However, whether
this set of traits is common among all introduced populations ofR. flavipes remains unknown.
Here, we used population genetic analyses and approximate Bayesian
computation (ABC) to investigate the invasion history of R.
flavipes . Using ddRadSeq, we first generated a SNP dataset sequencing
23 native populations in the USA and six introduced populations of this
species in France, Germany, Chile, Uruguay, the Bahamas and Canada. We
then assessed patterns of genetic structure within the entire native
range of the species, and within each of the introduced populations.
Finally, in order to elucidate the invasion history of R.
flavipes , we compared support for different invasion scenarios modeling
the number, size, and origin of each introduction event and their
admixture using ABC.