4 | DISCUSSION
Our study provides insights into the invasion pathway of the termiteReticulitermes flavipes , highlighting numerous and recent
human-mediated jump dispersals in both the native and introduced range
of this species. We first revealed a strong clustering among individuals
within the native range of this species in the eastern USA. Yet, these
individual differences were not due to geography, as highly different
individuals were found in the same locality and highly similar ones in
localities separated by several thousand kilometers. This finding
indicates extensive movement of colonies throughout the native range,
likely through human transportation. We also highlight a complex
invasion history with multiple events out of the native range and
bridgehead introductions from the introduced population in France. The
apparent genetic shuffling within the native range limits our ability to
assign an exact source population(s) for the different introduced
ranges. However, similar to the effect of multiple introductions into
the invasive range, admixture in the native range prior to invasion can
potentially favor invasion success by increasing the genetic diversity
later conveyed to the introduced ranges.
Our findings revealed the occurrence of multiple introductions from
different native localities serving as sources for the invasive ranges
of France, Chile and Canada. Additionally, Canada and Chile received
secondary invasions from the introduced population in France, which
acted as a bridgehead. Some previous results indicated there may have
been several introductions into France (Perdereau et al. 2019).
Reticulitermes flavipes was first reported in Austria in 1837; however,
it probably occurred earlier in Western Europe, when it was identified
as R. santonensis (Kollar 1837).
Despite being unable to definitively link its source population(s) to
the New Orleans region as previously suggested (Perdereau et al. 2013,
2015), our data, based on a larger sample size and more informative
markers, do not rule out this possibility, suggesting that this invasive
population originated from somewhere in the southeastern USA, from
Louisiana to South Carolina. However, it is possible that the French
population originated from colonies originally coming from the New
Orleans region that had been transported elsewhere within the native
range, such as South Carolina. Such long-distance jump dispersal within
the native range necessarily hampers clear identification of the source
population(s). Likewise, although our results suggest that the Canadian
and Chilean introduced populations originated from admixture between the
introduced population of France and native localities in the northern
range of R. flavipes, these results suffer from low confidence,
potentially due to genetic mixing between native localities. Overall,
these findings indicate that jump dispersal may not be restricted to a
single region within the native range of this species. Instead, such
dispersal appears common with R. flavipes , suggesting that the
evolutionary mechanisms promoting this phenomenon are globally
distributed across the species distribution range.
The genetic patterns observed in R. flavipes may be explained by
numerous and recent jump dispersal events across the native range,
likely mediated via human trade and transportation. This finding
exemplifies species spread by stratified dispersal , whereby
individuals disperse at different spatial scales, from local to
long-distance movement (Shigesada et al.
1995). Local scale dispersal relies on the biological dispersal ability
of the species, ranging from limited (i.e., budding) to moderate
dispersal (i.e., nuptial flight). In contrast, long-distance
dispersal is often human-mediated and therefore considered stochastic
and difficult to determine. Notably, our study revealed both 1)
genetically distinct individuals inhabiting the same locality and 2)
genetically similar individuals separated by several thousand
kilometers. The geographic distance separating highly similar
individuals far exceeds the biological dispersal ability of this
species, suggesting these individuals were artificially transported to a
different locality. Additionally, the finding of genetically distinct
individuals within the same or adjacent localities indicates a low level
of mixing between those individuals. This may stem from reduced local
dispersal, by which transported individuals interbreed and do not
disperse far from their landing point. A high proportion of new
reproductives of R. flavipes do in fact interbreed with their
nestmates during mating flights (25%); however, the proportion of
inbred successful founders is significantly reduced among established
colonies (DeHeer and Vargo 2006).
Therefore, this inbreeding depression may select against the
interbreeding of artificially transported colonies. Also, R.
flavipes usually disperse through nuptial flights, which should enhance
gene flow over large scales (Vargo 2003).
Consequently, a scenario by which transported individuals interbreed and
do not disperse far from their landing point may not alone explain the
pattern observed in this study. The finding of highly genetically
different individuals within the same locality suggests that some of the
long-distance jump dispersal events are probably too recent to allow
transported individuals to admix with local colonies to homogenize the
gene pool within populations.
The global spread of invasive species is strongly influenced by
long-distance jump dispersal, even once established within an introduced
range (Suarez et al. 2001). These
long-distance jump dispersal events are more effective, and often
required, for rapidly reaching widespread distributions. The worldwide
distribution of the Argentine ant has been shown to primarily stem from
human-mediated jump dispersal, rather than from its classical spread
through colony budding, as the latter would have to be three orders of
magnitude higher to explain its actual distribution
(Suarez et al. 2001). This finding is
also exemplified in the global distribution of the red imported fire antSolenopsis invicta , which utilized long-range jump dispersal to
first invade the southeastern US, and subsequently Asia and Australia
from its bridgehead in the USA (Ascunce et
al. 2011). In general, eusocial organisms like ants
(Bertelsmeier et al. 2018) and termites
(Buczkowski and Bertelsmeier 2017,
Blumenfeld and Vargo 2020) appear adept
at utilizing human-mediated jump dispersal to broaden their global
distributions. These serial long-distance movements are also observed
among regions within invasive ranges, across a wide variety of taxa,
such as the aforementioned S. invicta throughout the southern USA
(Lofgren 1986) and China
(Ascunce et al. 2011), the western
mosquitofish Gambusia affinis in New Zealand
(Purcell and Stockwell 2015), and plants
in China (Horvitz et al. 2017). Although
most studies demonstrate the importance of human-mediated dispersal in
shaping invasion dynamics following establishment, it often remains
unclear whether long-distance jump dispersal pre-exists in the native
range of invasive species, and its relative importance in the pattern of
genetic diversity observed at the global scale of these species.
Native ranges of many invasive species often remain geographically
structured (Voisin et al. 2005,
Beck et al. 2008,
Leinonen et al. 2008,
Verhoeven et al. 2011). For example,
native populations of S. invicta are strongly geographically
differentiated (Ross et al. 2007). Though
rare long-distance dispersals have been reported
(Ahrens et al. 2005), these events
occurred far in the past and have been attributed to strong winds during
nuptial flights or the rafting of entire colonies during flooding events
(Hölldobler and Wilson 1990), rather than
from human-mediated transport (Ahrens et
al. 2005). Native populations of another termite invaderCoptotermes formosanus in China are highly structured, with
distinct native populations representing different genetic clusters
(Blumenfeld et al. 2020). This structuring suggests reduced gene flow
across populations, and therefore a limited number of human-mediated
dispersal events within the native range of this species. Our results
stand in sharp contrast with the strong population structure commonly
uncovered within the native ranges of invasive species, as frequent jump
dispersal appears to have occurred in the native range of R.
flavipes . Understanding the factors driving the differences between
these two invasive termite species may shed light on key evolutionary
mechanisms underlying their invasion success. Furthermore, while most
studies focus on unraveling invasion pathways out of a native range, our
results stress the need to consider evolutionary processes and
human-mediated dispersal that may already be present within the native
range of an invasive species, as these can affect the level and
distribution of genetic diversity in both the native and invasive
ranges.
Extensive human-mediated jump dispersal has been reported in the native
range of a few species. For example, in the invasive tree Acacia
pycnantha , extensive transport and replanting throughout its native
Australian range prior to its introduction to South Africa resulted in
highly admixed genotypes already present in the native range. This
feature has consequently prevented an accurate identification of the
native source population(s), as highly admixed genotypes and comparable
genetic diversity were present in both ranges of the species
(Le Roux et al. 2013). A similar pattern
has been found in the North American rangeland weed, Centaurea
diffusa , where an extremely low level of population structure in the
native range hindered the assignment of its introduced population to its
likely native source location (Marrs et
al. 2008). However, the genetic patterns observed in these studies are
slightly different than the one observed in R. flavipes , as the
inability to pinpoint the origins of invasive populations stems from the
near-panmixia found across the native range. Therefore, the patterns in
these other species most likely stem from an ancient and continuous
genetic shuffling throughout the native range. In contrast, the lack of
geographic structure despite highly genetically different individuals
indicates recent and stochastic long-distance dispersal in R.
flavipes .
The invasion success of termites is tightly linked with their ability to
eat wood, nest in wood and cultivated plants and readily generate
secondary reproductives, as all 28 species of invasive termites share
these three traits (Evans et al. 2013).
These traits are common in lower termites like R. flavipes andC. formosanus , and ensure that any piece of wood serving as a
nest or foraging site has the potential to become a viable propagule
(Evans et al. 2010,
Evans et al. 2013). Although these traits
may enhance the frequency of human-mediated dispersal in R.
flavipes , their occurrence in both species cannot explain the
difference in long-distance dispersal in the native ranges of these two
species. In R. flavipes , repeated human-mediated dispersal could
reflect a higher degree of propagule pressure from different USA
regions, representing multiple hubs of intense human activity and timber
production. Forests and timber production are unequally distributed
across the eastern USA (Brown et al.
1999, Howard and Liang 2019), and may
therefore require significant wood transportation throughout this part
of the country from high to low timber-producing regions. Similarly, the
frequency of human-mediated dispersal may reflect the connectivity
between native regions. In the introduced population of R.
flavipes in France, the distribution of genetic diversity is associated
with the railway network, highlighting its possible role in displacing
termites over long distances (Andrieu et
al. 2017, Suppo et al. 2018,
Perdereau et al. 2019). In the USA, about
14,000km of track were active by 1850, mainly in the eastern USA
(141,000km in 1880 and over 400,000km in 1916)
(United States Census Bureau 1890,
Chandler 1965). In contrast, the first
10km railway was built in China in 1881, but less than 13,000km were in
use by 1948 for the whole country. This difference in connectivity may
explain the numerous long-distance dispersal events in the native range
of R. flavipes and their absence in the Chinese native range ofC. formosanus . Interestingly, the railroad network in the USA has
also been suggested to represent a major dispersal mode for C.
formosanus in its invasive range in this country
(Austin et al. 2008). Overall, many
invasive social insect species originate from South America or East Asia
(Tsutsui et al. 2000,
Heller 2004,
Ross et al. 2007,
Eyer et al. 2018a,
Eyer et al. 2018b,
Eyer et al. 2020). The population
structure observed in most native populations may simply reflect the
reduced connectivity between native regions in these areas, potentially
resulting from a lack of internal trade among regions or difficulty in
reaching isolated geographic areas. Our findings in R. flavipesmay shed light on frequent long-distance dispersal already present
within native ranges of invasive species, especially those originating
from regions with a long history of dense transport networks.
While the invasion scenario of numerous introductions from distinct
source populations and their admixture in the invasive range may explain
the levels of admixture observed in the introduced populations of France
and Chile, we cannot rule out the possibility that admixed introduced
populations re-invaded the native range of R. flavipes.Similarly, it is possible that populations were already admixed before
propagules were transported worldwide. Native populations of many
invasive species often remain geographically isolated and locally
adapted. It has been suggested that a temporary loss of local adaptation
in recent invaders fundamentally alters the fitness consequences of
admixture (Verhoeven et al. 2011).
Long-distance dispersal in the native range enhances gene flow between
distant populations that are otherwise isolated. Similar to
post-introduction increases of genetic diversity through multiple
introduction events (Kolbe et al. 2004,
Stenoien et al. 2005,
García et al. 2017), admixture between
native populations prior to an introduction event may enhance the amount
of genetic diversity brought to the invasive range. Admixture may
improve invasion success through recombination between distinct
genotypes, potentially creating novel combinations of traits, and/or
increasing the level of genetic diversity upon which natural selection
can act. Pre- or post-introduction admixture may also reduce the
inbreeding load by reducing the expression of recessive deleterious
alleles or lead to heterosis effects, potentially improving the
establishment and early success of invasive species
(Ellstrand and Schierenbeck 2000,
Drake 2006,
Keller and Taylor 2008,
Hahn and Rieseberg 2016). Overall,
increased genetic diversity via admixture may favor subsequent
introductions given the novel selection pressures invasive species face
in their new environments (Verhoeven et
al. 2011).