1. Introduction
The invasion process can be divided into a series of stages during which there are barriers that must be overcome for a population to become invasive [
1,
2]. Understanding these intricacies is an important part of predicting and managing biological invasions [
3]. During the first stage, the transport and introduction of individuals into a new geographical range has a decisive impact on the diversity and genetic structure of introduced populations [
4,
5,
6,
7,
8]. During the second stage, two factors will determine whether a viable population can be established: the ability of these individuals to survive new environmental conditions and to attain an adequate effective population size to allow a sustainable population to be founded [
1,
2,
7]. During the last stage, the invasive population will display demographic and spatial expansion, which is rooted in a strong capacity to reproduce and disperse [
4,
9]. The process may be accelerated by additional factors, such as human-mediated transport and mechanisms promoting long-distance dispersal [
10,
11,
12,
13]. Recently, Roques et al. [
14] carried out a detailed analysis of six invasive species and demonstrated that long-distance translocation associated with anthropogenic activities play a major role in determining rates of spread. Consequently, the spread of an invasive species is a complex process with significant effects on population spatial distribution and genetic structure within the introduced range [
15].
Reticulitermes flavipes is an invasive subterranean termite (Rhinotermitidae) that lives in forests and urban areas, where it can cause significant damage to wooden structures of human origin [
16]. It is native to the US, where it can be found from the eastern part of country (Massachusetts to Florida) to the Midwest and South (Nebraska and Texas). It has been unintentionally introduced into other countries in the Americas (i.e., the Bahamas, Canada, Chile, and Uruguay) and in Europe (i.e., Austria, France, Germany, Italy, and Canary Islands) [
17,
18]. A recent study of the termite’s genetics revealed that French populations (formerly known as
R. santonensis) most likely came from an area in or around New Orleans, Louisiana [
17]. It has been hypothesized that
R. flavipes was accidentally introduced to France during the 18th century, when Louisiana was a French territory, arriving in shipments of agricultural products and/or timber [
17,
19].
Reticulitermes flavipes is now well established in France: its range extends over the western half of the country, from Paris to Marseille. It is common in urban areas but also occurs in certain pine forests along the Atlantic coast. Rochefort and La Rochelle were the first two cities in which termite damage to anthropogenic structures was reported—they are two major ports along the Atlantic Coast that played an important role in international trade during the period mentioned above [
20,
21].
Reticulitermes flavipes remains extremely widespread and abundant in urban and natural areas in and around these two cities. All of the evidence points to the following scenario: individuals of
R. flavipes first arrived in one or several ports along the Atlantic Coast on ships coming from Louisiana. They reproduced and established themselves before spreading to other cities and expanding into local forests. If such is the case, the French populations of
R. flavipes have been evolving independently for about 200 years [
17].
In temperate habitats, termites of subterranean genera such as
Reticulitermes display a high degree of invasiveness and frequently infest anthropogenic structures [
22,
23,
24]. Subterranean termites have cryptic nesting habits and form complex colonies whose diffuse nests and multiple feeding sites are connected by underground tunnels. New colonies are typically founded by a pair of primary reproductives (i.e., winged adults, one queen, and one king) that mated after swarming. In the royal couple’s progeny, sterile individuals (i.e., workers, soldiers, larvae, and young nymphs) can differentiate into secondary reproductives [
25], also known as neotenics (i.e., non-winged reproductives), which can interbreed and reproduce within their parental colonies [
26]. This process of differentiation can occur either following the death of one or two primary reproductive(s) or during colony growth and expansion. Indeed, the presence of neotenics allows budding, which is an alternative mode of colony foundation. Furthermore, in some cases, different colonies can fuse into a single social unit that contains several unrelated reproductives and that covers a broad spatial area [
27,
28]. It is therefore clear that colony breeding structure directly influences colony growth and dispersal in
Reticulitermes species, which then affect termite population dynamics.
Interestingly, the ability of colonies to produce neotenics seems to be highly variable among species and populations [
16]. Research on
R. flavipes populations has highlighted the relationship between invasion success and colony breeding structure [
29]. Whereas native populations (i.e., in the US) are mainly composed of colonies headed by monogamous pairs of primary reproductives, the presumed source population (i.e., in New Orleans) and introduced populations (e.g., in France and Chile) tend to exhibit a unique colony breeding structure, in which there are hundreds of related neotenics, and where colonies show an unusual propensity to fuse. In France, this breeding structure is associated with the colonies’ spatial breadth, which commonly exceeds several hundred meters [
28,
29,
30,
31]. These two colony-level traits are thought to be preadaptations, allowing termite colonies to successfully invade new ranges, mainly because these traits allowed introduced colonies to reproduce and become established right after their introduction and then spread more rapidly via human-mediated dispersal [
29]. Recently, researchers have developed temporal and spatial models integrating these traits that have been used to predict termite’s future spread [
32]. More specifically, these studies aim to predict what will happen under conditions of climate warming in the Centre-Val de Loire region of France, where the termite’s presence was first recorded in the 1980s [
32]. The results show that increasing temperatures should increase the amount of favorable habitat and, consequently, termites could continue to spread within this region and throughout France.
The objective of this study was to characterize the post-establishment dynamics of R. flavipes in its French introduced range. More specifically, the aim was to identify and evaluate the genetic links among infestations to identify the invasion pathways that the termite may have followed at national and regional scales. We focused on two highly infested regions, Île-de-France (center = Paris) and Centre-Val de Loire (center = Tours), and estimated population variation, maternal lineages (i.e., haplotypes), and population genetic structure (i.e., microsatellite genotypic distribution). We also characterized colony breeding system along the invasion front in Centre-Val de Loire, from west to northeast. This study contributes to our understanding of how R. flavipes spreads within new environments, and confirms that certain anthropogenic factors might strongly affect the termite’s population dynamics.