Genomic diversity gradients and functional differentiation put Northeast Pacific ribbon kelp lineages in the speciation grey zone

<p><span>The transition from reproductively isolated populations to species is not well understood. Genotyping entire genomes holds promise to enhance insights into the process of speciation and the evolutionary relationships among related taxa. Gulf of Alaska ribbon kelp was once recognized as four species before they were folded into <em>Alaria</em> <em>marginata</em> on the basis of DNA barcode markers, though several lineages have continued to be recognized. Here, we used whole genome sequencing datasets to test the hypothesis that these lineages represent incipient species. Whole genomes of 69 individuals from five genetically distinctive lineages in the Gulf of Alaska (USA) and Salish Sea (Canada) were analyzed, along with 63 genomes from three other species of <em>Alaria</em>. Our analysis of &gt;3.4 million Single Nucleotide Polymorphisms reaffirms that organellar and nuclear phylogenetic signals are incongruent in <em>Alaria</em>, producing different topologies among five organellar and six nuclear <em>A</em>. <em>marginata</em> lineages. Lineages also display reproductive isolation, evidenced by a lack of recent admixture across genomes. Genetic distances between <em>A</em>. <em>marginata</em> lineages exceed levels expected of population-level divergence but fall short of distances between species of <em>Alaria</em>. Moreover, we provide evidence of functional genomic differences between the <em>A</em>. <em>marginata</em> lineages, exceeding differences expected between populations, but falling short of larger differences among species. Our results place <em>A</em>. <em>marginata</em> lineages in an evolutionary grey zone, where lineages display substantial differentiation, but not to the level expected of <em>Alaria</em> species. This information shifts taxonomic conversations towards a genome-scale framework that provides a more comprehensive picture of divergence, connectivity, and functional innovation for defining lineages.</span></p>