Native to eastern Asia, the Formosan subterranean termiteCoptotermes formosanus(Shiraki) is recognized as one of the 100 worst invasive pests in the world, with established populations in Japan, Hawaii and the southeastern United States. Despite its importance, the native source(s) ofC. formosanusintroductions and their invasive pathway out of Asia remain elusive. Using ~22,000 SNPs, we retraced the invasion history of this species through approximate Bayesian computation and assessed the consequences of the invasion on its genetic patterns and demography. We show a complex invasion history, where an initial introduction to Hawaii resulted from two distinct introduction events from eastern Asia and the Hong Kong region. The admixed Hawaiian population subsequently served as the source, through a bridgehead, for one introduction to the southeastern US. A separate introduction event from southcentral China subsequently occurred in Florida showing admixture with the first introduction. Overall, these findings further reinforce the pivotal role of bridgeheads in shaping species distributions in the Anthropocene and illustrate that the global distribution ofC. formosanushas been shaped by multiple introductions out of China, which may have prevented and possibly reversed the loss of genetic diversity within its invasive range.

Social insects are among the most serious invasive pests in the world, particularly successful at monopolizing environmental resources to outcompete native species and achieve ecological dominance. The invasive success of some social insects is enhanced by their unicolonial structure, under which the presence of numerous queens and the lack of aggression against non-nestmates allow high worker densities, colony growth, and survival while eliminating intra-specific competition. In this study, we investigated the population genetics, colony structure and levels of aggression in the tawny crazy ant, Nylanderia fulva, which was recently introduced into the United States from South America. We found that this species experienced a genetic bottleneck during its invasion lowering its genetic diversity by 60%. Our results show that the introduction of N. fulva is associated with a shift in colony structure. This species exhibits a multicolonial organization in its native range, with colonies clearly separated from one another, whereas it displays a unicolonial system with no clear boundaries among nests in its invasive range. We uncovered an absence of genetic differentiation among populations across the entire invasive range, and a lack of aggressive behaviors towards conspecifics from different nests, even ones separated by several hundreds of kilometers. Overall, these results suggest that across its entire invasive range in the U.S.A., this species forms a single supercolony spreading more than 2000 km. In each invasive nest, we found several, up to hundreds, of reproductive queens, each being mated with a single male. The many reproductive queens per nests, together with the free movement of individuals between nests, leads to a relatedness coefficient among nestmate workers close to zero in introduced populations, calling into question the stability of this unicolonial system in which indirect fitness benefits to workers is apparently absent.

Genetic diversity acts as a reservoir for potential adaptations, yet selection tends to reduce this diversity over generations. However, sexually antagonistic selection (SAS) may promote diversity by selecting different alleles in each sex. SAS arises when an allele is beneficial to one sex but harmful to the other. Usually, the evolution of sex chromosomes allows each sex to independently reach different optima, thereby circumventing the constraint of a shared autosomal genome. Because the X chromosome is found twice as often in females than males, it represents a hot spot for SAS, offering a refuge for recessive male-beneficial but female-costly alleles. Hymenopteran species do not have sex chromosomes; females are diploid and males are haploid, with sex usually determined by heterozygosity at the complementary sex-determining locus. For this reason, their entire genomes display an X-linked pattern, as every chromosome is found twice as often in females than in males, which theoretically predisposes them to SAS in large parts of their genome. Here we report an instance of sexual divergence in the Hymenoptera, a sexually reproducing group that lacks sex chromosomes. In the invasive ant Nylanderia fulva , a postzygotic SAS leads daughters to preferentially carry alleles from their mothers and sons to preferentially carry alleles from their grandfathers for a substantial region (∼3%) of the genome. This mechanism results in nearly all females being heterozygous at these regions and maintains diversity throughout the population, which may mitigate the effects of a genetic bottleneck following introduction to an exotic area and enhance the invasion success of this ant.