Founder effects shape linkage disequilibrium and genomic diversity of a partially clonal invader

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 (Ho), 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 Ho and Pi, rather, the
increased Ho 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.