Demography and Localized Reservoirs of Diversity Underlie Global Divergence in the Giant Kelp Macrocystis pyrifera.

Accurate assessments of genetic diversity are crucial for effective management of natural resources. Numerous evolutionary mechanisms and genetic constraints can shape lineage divergence, challenging our quantification of biodiversity. Here, using whole genome resequencing of globally distributed giant kelp, Macrocystis pyrifera (Order: Laminariales), we show clear separation of genetic groups across the Pacific based on 99 genotyped individuals and 799,160 SNPs. Additionally, divergence across 88 genotyped individuals (53 derived in silico and 35 newly sequenced) considering 5,466,408 SNPs is attributed to both historical demographic processes and differential selection. Between Central California and the South Pacific (Chile, Tasmania, New Zealand), high divergence has occurred with very weak levels of gene flow, with concurrent timing of divergence. In parts of the South Pacific, kelp exhibited nucleotide diversity comparable to Central Californian populations but showed stronger signals of directional selection and excesses of rare alleles, with fewer genes showing signs of negative selection and some carbon-related genes under positive selection. In contrast, Central Californian kelp had an excess of genes with synonymous mutations and showed evidence of a recent population contraction, as indicated by linkage disequilibrium and Tajima's D. In all populations, genome-wide background divergence was paired with narrow genomic intervals of high nucleotide diversity and high linkage disequilibrium, which predominantly contained pervasive repetitive sequences. These repetitive regions were larger and more often shared among genetic groups in the South Pacific. They also appear to harbour genes of unknown function and alleles at intermediate frequency, suggesting that giant kelp maintain reservoirs of diversity within linked repeats, and this phenomenon is more pronounced in South Pacific M. pyrifera. Overall, the discovery of differential selection and structural variation as key drivers of divergence points to underappreciated genomic mechanisms of adaptation in kelp. These results will be useful for informing efforts to enhance climate resilience by identifying the evolutionary potential underlying kelp forest adaptation in the future.