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

Abstract

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).

Brought more than twice: the complex introduction history of the red swamp crayfish into Europe

“…It has been generally thought that the European range of the red swamp crayfish results from the expansion of these two founder populations, driven by multiple (an unknown number, but arguably thousands) uncontrolled translocations (for example in the Iberian Peninsula, Gutiérrez-Yurrita et al, 1999). This assumption seems to be supported by the high haplotype diversity of invasive populations in southwestern Spain, and by such diversity progressively decreases as one moves towards the North, as recently reported by Oficialdegui et al (2019). However, other introduction events from different sources cannot be ruled out in some European countries (Patoka et al, 2014 and references therein;Weiperth et al, 2019).…”

Impacts of climate change on the global potential distribution of two notorious invasive crayfishes

“…The signal crayfish Pacifastacus leniusculus (Dana, 1852), which is native to western North America, has been introduced into Europe and Japan (Azuma, Usio, Korenaga, Koizumi, & Takamura, 2011;Bubb, Thom, & Lucas, 2004;Kawai, Mitamura, & Ohtaka, 2004;Kouba, Petrusek, & Kozák, 2014;Usio et al, 2016). The red swamp crayfish Procambarus clarkii (Girard, 1852) is native to north-eastern Mexico and southern USA and has successfully spread to North and Central America, Europe, Asia, Africa, and South America (Gherardi, 2006;Kouba et al, 2014;Loureiro, Anastácio, Araujo, Souty-Grosset, & Almerão, 2015;Oficialdegui et al, 2019).…”

Stable resource polymorphism along the benthic littoral–pelagic axis in an invasive crayfish

“…Created between 1963 and 2007, these lakes are characterized by different environmental conditions arising from various levels of maturity and management practices (Zhao, Grenouillet, Pool, Tudesque, & Cucherousset, 2016). Native from Northern America, P. clarkii is one of the most invasive crayfish species worldwide (Oficialdegui et al, 2019). The species was introduced to France in 1976, and its presence in the studied area was first documented in 1995 (Changeux, 2003), indicating that the colonization process is relatively recent in those lakes.…”