Genomic variation of an invasive species may be affected by complex demographic histories and evolutionary changes during invasions. Here, we describe the relative influence of bottlenecks, clonality, and population expansion in determining genomic variability of the widespread red macroalga Agarophyton vermiculophyllum. Its introduction from mainland Japan to the estuaries of North America and Europe coincided with shifts from predominantly sexual to partially clonal reproduction and rapid adaptive evolution. A survey of 62,285 SNPs for 351 individuals from 35 populations, aligned to 24 chromosome-length scaffolds indicate that linkage disequilibrium (LD), observed heterozygosity (H_o), Tajima’s D, and nucleotide diversity (Pi) were greater among non-native than native populations. Evolutionary simulations indicate LD and Tajima’s D were consistent with a severe population bottleneck. Also, the increased rate of clonal reproduction in the non-native range could not have produced the observed patterns by itself but may have magnified the bottleneck effect on LD. A bottleneck or clonality limitedly impact H_o and Pi, rather, the increased H_o and Pi in the non-native range is possibly due to elevated marker diversity in the genetic source populations. We refined the previous invasion source region to a ~50km section of northeastern Honshu Island. Outlier detection methods failed to reveal any consistently differentiated loci shared among invaded regions, likely because of the complex A. vermiculophyllum demographic history. Our results reinforce the importance of demographic history, specifically founder effects, in driving genomic variation of invasive populations, even when localized adaptive evolution and reproductive system shifts are observed.

The dataset includes ddRAD-seq data in beagle format produced from ANGSD, the assembled Agarophyton vermiculophyllum genome, and all scripts used for data analysis and figure generation. Download and view README.md for additional dataset information.

Demultiplexed raw reads are available as an NCBI BioProject (PRJNA700770), and the NCBI BioSample accessions are available in the BioSampleObjects.txt file included in the dataset. The assembled Agarophyton vermiculophyllum genome was submitted to NCBI BioSample (SAMN17860744).