Reproductive Isolation and Differential Introgression Shape the Genomic Landscape of the Red Alga Amansia glomerata in the Hawaiian Archipelago

Speciation in marine environments is inherently complex, and the mechanisms underlying the evolution of reproductive isolation remain a fundamental yet understudied challenge in macroalgae. This study investigates two lineages of the marine red alga Amansia glomerata around Oʻahu, Hawaiʻi, to test the hypothesis that lineage boundaries are maintained by strong reproductive barriers resulting from historical geographic isolation. Using genomic sequencing (ddRAD), fine-scale spatial transects, and demographic modeling, we characterized lineage spatial structure and genomic divergence. Our results revealed that lineages remained strongly differentiated across the genome, even where they co-occurred across extensive sympatric regions. Demographic analyses supported a scenario of allopatric divergence followed by secondary contact, likely driven by Pleistocene sea-level fluctuations within the Hawaiian Archipelago. The absence of recombinant hybrids, together with numerous loci acting as barriers to gene flow, is consistent with the evolution of postzygotic isolation. Nevertheless, genomic signatures of introgression indicate that gene flow during secondary contact was spatially structured around the island and heterogeneous across the genome, revealing differential permeability of lineage boundaries at the time of contact. While our findings highlight allopatric divergence and intrinsic reproductive barriers as major drivers of speciation in this system, the potential role of ecological differentiation remains to be explored. Overall, this study provides pioneering insights into the genomics of speciation in Hawaiian seaweeds and underscores their potential as a model system for marine speciation.