Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture vs. maritime traffic effects

Abstract

Worldwide marine invaders, such as the brown alga Undaria pinnatifida, offer challenging models for unraveling the apparent paradox of sustainable settlement of exotic species over a large spectrum of environments. Two intergenic noncoding mitochondrial loci were found to be highly informative at the within-species level. Twenty-five haplotypes were found over the whole dataset (333 base pairs, 524 individuals, and 24 populations). The native range showed striking population genetic structure stemming from low diversity within and high differentiation among populations, a pattern not observed in the introduced range of this seaweed. Contrary to classical expectations of founding effects associated with accidental introduction of exotic species, most of the introduced populations showed high genetic diversity. At the regional scale, genetic diversity and sequence divergence showed contrasting patterns in the two main areas of introduction (Europe and Australasia), suggesting different processes of introduction in the two regions. Gene genealogy analyses point to aquaculture as a major vector of introduction and spread in Europe but implicate maritime traffic in promoting recurrent migration events from the native range to Australasia. The multiplicity of processes and genetic signatures associated with the successful invasion confirms that multiple facets of global change, e.g., aquaculture practices, alteration of habitats, and increased traffic, act in synergy at the worldwide level, facilitating successful pandemic introductions.

Fig. 1.

Distribution of the 25 mtDNA haplotypes detected in the 24 wild and cultivated U. pinnatifida populations sampled around the world. Color-motif pie charts display relative frequencies of each haplotype in each population. Foreground colors of the pie charts refer to the clusters defined as in Fig. 2: red, cluster A; red and blue, cluster B1; and green, cluster B2. The international code of the country of origin of each population is indicated in parentheses.

Fig. 2.

Haplotypic network and regional distribution of the 25 U. pinnatifida mtDNA haplotypes. Circle sizes are proportional to the number of individuals observed for each haplotype, and color pie charts indicate the distribution of the haplotype among wild populations in the five world-wide regions and crops. Connecting lines show mutational pathways among haplotypes; triangles represent single-site substitutions; perpendicular bars, indels; and boxed bars, blocks of 16 and 2 tandem indels. Unlabeled red nodes indicate inferred steps not found in the sampled populations. Clusters group closely related haplotypes.