Tracing the introduction history of the invasive swimming crab Charybdis hellerii (A. Milne-Edwards, 1867) in the Western Atlantic: evidences of high genetic diversity and multiple introductions

Abstract

The swimming crab Charybdis hellerii is an invader with global distribution in warm waters. Native to the Indo-Pacific, this species invaded the eastern Mediterranean Sea after the Suez Canal opening. In 1987, it was first reported in the Western Atlantic, probably transported via ballast water of ships. Since then, it has been registered from many localities along the American coast from the USA to southern Brazil where it has rapidly established reproducing populations. Our main aim was to investigate the introduction history of this species along the American coast, using a phylogeographic approach. Additionally, we attempted to clarify the identity of this invasive species by molecular analyses and morphological assessment in order to provide a basis for our main investigation. C. hellerii was confirmed as a single species, but both cytochrome c oxidase subunit I and 16S rDNA revealed a genetic structure, splitting the potential source populations of American introductions into two groups: “western Indian Ocean and Mediterranean Sea” (WIO + MS) versus “eastern Indian + western Pacific oceans” (EIO + WPO). Most specimens from America clustered with the former group, supporting the hypothesis that the Mediterranean Sea represented the main source of Western Atlantic populations. However, the clustering of animals from southern Brazil with the latter group indicates that introductions from the eastern Indian or Pacific oceans must also have occurred. The existence of a third group, found exclusively within the American range and genetically related to EIO + WPO, also indicates an independent introduction from an unsampled locality from the native range. The haplotype and nucleotide diversities of American localities were comparable to those of source populations, contradicting a founder effect prediction. This finding might be related to the high propagule pressure associated with introductions via ballast water and the occurrence of multiple introductions from genetic distinct sources. The direct comparison of the haplotype numbers suggested no genetic bottleneck during introduction from the Mediterranean Sea, but a bottleneck might have occurred during introductions from the eastern Indian or Pacific oceans.