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 Alaria marginata 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 Alaria. Our analysis of >3.4 million Single Nucleotide Polymorphisms reaffirms that organellar and nuclear phylogenetic signals are incongruent in Alaria, producing different topologies among five organellar and six nuclear A. marginata lineages. Lineages also display reproductive isolation, evidenced by a lack of recent admixture across genomes. Genetic distances between A. marginata lineages exceed levels expected of population-level divergence but fall short of distances between species of Alaria. Moreover, we provide evidence of functional genomic differences between the A. marginata lineages, exceeding differences expected between populations, but falling short of larger differences among species. Our results place A. marginata lineages in an evolutionary grey zone, where lineages display substantial differentiation, but not to the level expected of Alaria 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.

The following datasets represent tab delimited tables of exon coverage calculated for various populations and species of ribbon kelp (genus Alaria). The tables include gene names and functional annotations (UniProt IDs). The values for coverage are 1) standardized using mean coverage for confirmed single copy exons within each specimen analysed, then 2) averaged for each populations/lineage/species of interest. 1=expected coverage, <1=less than expected level of coverage, 0=no coverage, >1=more than expected coverage. Values of 0 could be interpreted as exon loss, while high values could be interpreted as duplications/expansions, though caveats to these interpretations are explored in our manuscript. The exons represent annotations for the Alaria esculenta genome, onto which reads from all datasets were mapped.

Three datasets are presented, one each for populations of Alaria esculenta, one for lineages of Alaria marginata, and one for all species/populations analysed. Only exons (i.e. rows) with differential coverage are presented (standardized coverage values of 0 or >4).

Links to other publicly accessible locations of the data: https://doi.org/10.6084/m9.figshare.21757691.v2.

Link to Alaria esculenta genome: https://doi.org/10.6084/m9.figshare.16712797.v2

Workflow information: https://github.com/tbringloe/WGS-NOVAC

Any program that can open tab delimited text documents. Can also be imported into Excel.