Revisiting the species problem in Northeast Pacific ribbon kelp lineages (genus Alaria): Lessons learned using whole genome data

Abstract

The transition from interbreeding populations to species continues to represent difficult terrain for phylogenetic investigations. Genotyping entire genomes holds promise for enhancing insights into the process of speciation and evolutionary relationships among recently speciated taxa. Northeast Pacific ribbon kelp was once recognized as four species before they were folded into Alaria marginata based on DNA barcodes, although several lineages continue to be recognized. We used whole genome sequencing to determine whether these lineages represente species. Whole genomes of 69 individuals from five genetically distinctive lineages in the Gulf of Alaska (United States) 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 reaffirmed that organellar and nuclear phylogenetic signals are incongruent in Alaria, producing different topologies among five organellar and six nuclear A. marginata lineages. Lineages appeared to be reproductively isolated, as evidenced by strong clustering and lack of recent admixture across nuclear genomes. Genetic divergence between A. marginata lineages also exceeded intra-lineage divergence, proxied by A. esculenta populations, but fell short of distances observed across other species of Alaria. Despite the genomic data supporting predictions of the biological and genetic species concepts, we encountered inherent limitations in declaring species status. While our work shifts taxonomic conversations toward a genome-scale framework that provides a more comprehensive picture of divergence and connectivity, our work also highlights that philosophical challenges inherent to defining species persist and that integrative approaches continue to be necessary in the genomic era.

Keywords: Alaria; Gulf of Alaska; high‐throughput sequencing; nuclear; populations; shotgun sequencing; speciation.