Unravelling the global invasion routes of a worldwide invader, the red swamp crayfish (Procambarus clarkii)

Understanding how introduced species succeed and become widely distributed within non-native areas is critical to reduce the threats posed by them. Our goal was to reconstruct the main invasion routes and invasion dynamics of a global freshwater invader, the red swamp crayfish, Procambarus clarkii, through the analysis of its genetic variability in both native and invasive ranges. We inferred invasion routes and population structure from the analysis of a fragment (608 base pairs) of the mitochondrial marker cytochrome c oxidase subunit I from 1,062 individuals of P. clarkii in addition to 354 GenBank sequences, for a total of 122 populations (22 natives and 100 invaded). Genetic structure was assessed using analysis of molecular variance and non-metric multidimensional scaling analyses. We analysed haplotype frequencies for the genetic variability in each locality and region. The haplotype network was depicted by using PopART software. A high haplotype diversity was found in the native range (haplotype diversity [Hd]: 0.90), but also in some non-native areas, such as western U.S.A. (Hd: 0.80), areas of Mexico (Hd: 0.78), and some hotspots in Europe (e.g. southern Spain or Italy), suggesting a complex pattern of multiple introductions. We grouped all localities in five differentiated groups according to biogeographic origin: the native area, west Americas, east U.S.A., Asia, and Europe. Additionally, the identification of 15 haplotypes shared between at least two localities, the phylogenetic network estimation and indices of genetic differentiation among localities allowed us to identify a large genetic admixture in the native range; the two independent invasion routes (i.e. westwards and eastwards) in U.S.A. from the native range (Louisiana and Texas) with translocations within each area; a stepping-stone introduction from U.S.A. to Japan (involving few individuals) themselves introduced to China afterwards; the entry of P. clarkii from Louisiana (U.S.A.) into southern Spain and their multiple secondary introductions over Europe as well as other possible introductions in central Europe. Our study emphasises the need for unravelling the global invasion routes and the demographic processes underlying the introduction of exotic species (i.e. admixture, bridgehead invasion effect, and propagule pressure) to control the spread of invasive species. Our findings highlight the value of genetic analyses to identify the geographic origin of source populations as well as the variability of invaded areas in order to reconstruct invasion dynamics and facilitate management of invasive species (e.g. through environmental DNA monitoring).