Elfie Perdereau

Competition between invasive and indigenous species: an insular case study of subterranean termites

An important requirement for the management of invasive species is to identify the biological and ecological factors that influence the ability of such species to become established and spread within a new environment. Although competition is one of the key interactions determining the coexistence of species and exclusion, few studies directly examine the mechanism of competitive interactions within invasive communities. This study focused on putative competition in a social insect invader, R. flavipes, an American termite introduced into France, and an indigenous European termite, R. grassei. We first characterized and mapped a zone of sympatry between these two species. We then evaluated the degree of direct and indirect competition by comparing several life-history traits: behavioral aggression, chemical recognition and dispersion modes. Interspecific competition revealed that R. flavipes was dominant over R. grassei. Intraspecific competition was not found in R. flavipes while it appeared in varying degrees in R. grassei. These findings seemed to be correlated with the remarkable chemical homogeneity found in R. flavipes in comparison with R. grassei. Genetic analyses revealed that R. flavipes foraged over a greater distance than R. grassei colonies and might suggest a difference in the capacity to produce secondary reproductives. These findings suggest that R. flavipes has a significant advantage owing to competitive asymmetry that may enable the species to become dominant. The interspecific superiority, lack of intraspecific aggression and large extensive colonies, seem to be some of the reasons for its invasive success.

Global genetic analysis reveals the putative native source of the invasive termite, Reticulitermes flavipes, in France

Biological invasions are recognized as a major threat to both natural and managed ecosystems. Phylogeographic and population genetic analyses can provide information about the geographical origins and patterns of introduction and explain the causes and mechanisms by which introduced species have become successful invaders. Reticulitermes flavipes is a North American subterranean termite that has been introduced into several areas, including France where introduced populations have become invasive. To identify likely source populations in the USA and to compare the genetic diversity of both native and introduced populations, an extensive molecular genetic study was undertaken using the COII region of mtDNA and 15 microsatellite loci. Our results showed that native northern US populations appeared well differentiated from those of the southern part of the US range. Phylogenetic analysis of both mitochondrial and nuclear markers showed that French populations probably originated from southeastern US populations, and more specifically from Louisiana. All of the mtDNA haplotypes shared between the United States and France were found in Louisiana. Compared to native populations in Louisiana, French populations show lower genetic diversity at both mtDNA and microsatellite markers. These findings are discussed along with the invasion routes of R. flavipes as well as the possible mechanisms by which French populations have evolved after their introduction.

High occurrence of colony fusion in a European population of the American termite Reticulitermes flavipes

The coexistence of multiple unrelated reproductives within social insect colonies decreases the relatedness among colony members and therefore challenges kin selection theory. This study investigated the colony genetic structure of a French introduced population of the American subterranean termite Reticulitermes flavipes by analyzing genotypes at eight microsatellite loci and at one mtDNA region. Results revealed that all colonies contained numerous related secondary reproductives, and that 31% of colonies possessed more than two unrelated reproductives. The presence of several unrelated reproductives within colonies of this species is commonly assumed to result from colony fusion. Although such a high occurrence of colony fusion is the highest ever observed in a termite population, it is probable that the available methodology underestimated the detection of colony fusion in French populations. Overall, these results suggest that French colonies might differ strongly from the great majority of American colonies in their capacity to produce secondary reproductives as well as in their ability to merge. The nature and evolutionary origin of these population differences are discussed.

Variations in Worker Cuticular Hydrocarbons and Soldier Isoprenoid Defensive Secretions Within and Among Introduced and Native Populations of the Subterranean Termite, Reticulitermes flavipes

In social insects, cuticular hydrocarbons (CHCs) play a central role in nestmate recognition. CHCs have proved to be useful for identifying species and differentiating populations. In combination with CHCs, isoprenoid soldier defensive secretions (SDSs) have been previously used in some termite species for chemotaxonomic analyses. This study compared the levels of chemical variation within and among introduced (French) and native (U.S.) populations of the subterranean termite, Reticulitermes flavipes. Worker CHCs and soldier SDSs from termites collected from colonies in nine populations in Florida, Louisiana, and France were analyzed. Discriminant analyses revealed that both localities and populations can be distinguished by using the variation in CHC profiles. Principal component analyses of CHC profiles as well as the calculation of two distance parameters (Nei and Euclidean) revealed remarkable chemical homogeneity within and among French populations. These analyses also showed that the CHC profiles of French populations were closer to termite populations from Louisiana than to those from Florida. Of the six distinct SDS chemotypes, one was common to populations in France and Louisiana. The possibility that populations in France originated from Louisiana, and the potential causes and consequences of chemical homogeneity within introduced populations are discussed.

Relationship between invasion success and colony breeding structure in a subterranean termite

Factors promoting the establishment and colonization success of introduced populations in new environments constitute an important issue in biological invasions. In this context, the respective role of pre‐adaptation and evolutionary changes during the invasion process is a key question that requires particular attention. This study compared the colony breeding structure (i.e. number and relatedness among reproductives within colonies) in native and introduced populations of the subterranean pest termite, Reticulitermes flavipes. We generated and analysed a data set of both microsatellite and mtDNA loci on termite samples collected in three introduced populations, one in France and two in Chile, and in the putative source population of French and Chilean infestations that has recently been identified in New Orleans, LA. We also provided a synthesis combining our results with those of previous studies to obtain a global picture of the variation in breeding structure in this species. Whereas most native US populations are mainly composed of colonies headed by monogamous pairs of primary reproductives, all introduced populations exhibit a particular colony breeding structure that is characterized by hundreds of inbreeding reproductives (neotenics) and by a propensity of colonies to fuse, a pattern shared uniquely with the population of New Orleans. These characteristics are comparable to those of many invasive ants and are discussed to play an important role during the invasion process. Our finding that the New Orleans population exhibits the same breeding structure as its related introduced populations suggests that this native population is pre‐adapted to invade new ranges.

Endocrine control of cuticular hydrocarbon profiles during worker-to-soldier differentiation in the termite Reticulitermes flavipes

The social organization of termites, unlike that of other social insects, is characterized by a highly plastic caste system. With the exception of the alates, all other individuals in a colony remain at an immature stage of development. Workers in particular remain developmentally flexible; they can switch castes to become soldiers or neotenics. Juvenile hormone (JH) is known to play a key role in turning workers into soldiers. In this study, we analyzed differences in cuticular hydrocarbon (CHC) profiles among castes, paying particular attention to the transition of workers to soldiers, in the subterranean termite species Reticulitermes flavipes. CHCs have a fundamental function in social insects as they serve as cues in inter- and intraspecific recognition. We showed that (1) the CHC profiles of the different castes (workers, soldiers, nymphs and neotenics) are different and (2) when workers were experimentally exposed to a JH analog and thus induced to become soldiers, their CHC profiles were modified before and after the worker-presoldier molt and before and after the presoldier-soldier molt.

Colony Breeding Structure of the Invasive Termite Reticulitermes urbis (Isoptera: Rhinotermitidae)

ABSTRACT Invasive species cause severe environmental and economic problems. The invasive success of social insects often appears to be related to their ability to adjust their social organization to new environments. To gain a better understanding of the biology of invasive termites, this study investigated the social organization of the subterranean termite, Reticulitermes urbis, analyzing the breeding structure and the number of reproductives within colonies from three introduced populations. By using eight microsatellite loci to determine the genetic structure, it was found that all the colonies from the three populations were headed by both primary reproductives (kings and queens) and secondary reproductives (neotenics) to form extended-family colonies. R. urbis appears to be the only Reticulitermes species with a social organization based solely on extended-families in both native and introduced populations, suggesting that there is no change in their social organization on introduction. F-statistics indicated that there were few neotenics within the colonies from urban areas, which did not agree with results from previous studies and field observations. This suggests that although several neotenics may be produced, only few become active reproductives. The results also imply that the invasive success of R. urbis may be based on different reproductive strategies in urban and semiurbanized areas. The factors influencing an individual to differentiate into a neotenic in Reticulitermes species are discussed.

Spatial structuring of the population genetics of a European subterranean termite species

In population genetics studies, detecting and quantifying the distribution of genetic variation can help elucidate ecological and evolutionary processes. In social insects, the distribution of population-level genetic variability is generally linked to colony-level genetic structure. It is thus especially crucial to conduct complementary analyses on such organisms to examine how spatial and social constraints interact to shape patterns of intraspecific diversity. In this study, we sequenced the mitochondrial COII gene for 52 colonies of the subterranean termite Reticulitermes grassei (Isoptera: Rhinotermitidae), sampled from a population in southwestern France. Three haplotypes were detected, one of which was found exclusively in the southern part of the study area (near the Pyrenees). After genotyping 6 microsatellite loci for 512 individual termites, we detected a significant degree of isolation by distance among individuals over the entire range; however, the cline of genetic differentiation was not continuous, suggesting the existence of differentiated populations. A spatial principal component analysis based on allele frequency data revealed significant spatial autocorrelation among genotypes: the northern and southern groups were strongly differentiated. This finding was corroborated by clustering analyses; depending on the randomized data set, two or three clusters, exhibiting significant degrees of differentiation, were identified. An examination of colony breeding systems showed that colonies containing related neotenic reproductives were prevalent, suggesting that inbreeding may contribute to the high level of homozygosity observed and thus enhance genetic contrasts among colonies. We discuss the effect of evolutionary and environmental factors as well as reproductive and dispersal modes on population genetic structure.

Potential spread of the invasive North American termite, Reticulitermes flavipes , and the impact of climate warming

Reticulitermes flavipes is an invasive termite from North America that is found in several European countries, including France from north to south. It feeds on several timber species and can cause major damage when it infests lumber. Termites are urban pests: they are often found in and around towns and their expansion is closely linked to human activity. Although, by law, termite infestations must be reported and treated, R. flavipes continues to spread. To better identify areas that may soon be colonized, it is crucial to understand the mechanisms underlying the termite’s spread at a fine spatial scale. However, the complexity of the species’ dispersal dynamics (i.e., via swarming, budding, or human-mediated transport of infested material) and social organization render this process difficult. The goal of our study was to determine R. flavipes’ potential to expand its current range within a region of France: Centre-Val de Loire. We focused on one administrative department within the region—Indre and Loire—where infestations are common and data on termite presence date back to the 1980s. We developed a spatiotemporal model to study the growth and dispersal of termite colonies within favorable habitat. Habitat favorability was defined based on the density of urbanization and annual mean minimum temperature. First, we modeled temporal population dynamics, using biological parameters describing the transitions between life stages/castes within colonies; we could thus estimate alates production. Then, using this information, we modeled termite dispersal within favorable habitat, and determined the termite’s potential spread. We validated the results by comparing the model’s output with actual data on the termite’s range expansion between 1985 (when the termite was first observed in the region) and 2013. Finally, the model was used to predict the termite’s future spread given climate warming for the period from 2013 to 2030. The results show that an increase in temperature should increase the amount of favorable habitat and, as a consequence, termites could continue to spread within this region. In addition to continuing current control efforts, it will be necessary to enact preventative strategies in newly favorable habitat. In these areas, monitoring efforts should therefore be intensified, as they might be able to slow down the termite’s spread and limit its impact.