Whole-genome sequencing reveals forgotten lineages and recurrent hybridizations within the kelp genus Alaria (Phaeophyceae).

The genomic era continues to revolutionize our understanding of the evolution of biodiversity. In phycology, emphasis remains on assembling nuclear and organellar genomes, leaving the full potential of genomic datasets to answer long-standing questions about the evolution of biodiversity largely unexplored. Here, we used whole-genome sequencing (WGS) datasets to survey species diversity in the kelp genus Alaria, compare phylogenetic signals across organellar and nuclear genomes, and specifically test whether phylogenies behave like trees or networks. Genomes were sequenced from across the global distribution of Alaria (including Alaria crassifolia, A. praelonga, A. crispa, A. marginata, and A. esculenta), representing over 550 GB of data and over 2.2 billion paired reads. Genomic datasets retrieved 3,814 and 4,536 single-nucleotide polymorphisms (SNPs) for mitochondrial and chloroplast genomes, respectively, and upwards of 148,542 high-quality nuclear SNPs. WGS revealed an Arctic lineage of Alaria, which we hypothesize represents the synonymized taxon A. grandifolia. The SNP datasets also revealed inconsistent topologies across genomic compartments, and hybridization (i.e., phylogenetic networks) between Pacific A. praelonga, A. crispa, and putative A. grandifolia, and between some lineages of the A. marginata complex. Our analysis demonstrates the potential for WGS data to advance our understanding of evolution and biodiversity beyond amplicon sequencing, and that hybridization is potentially an important mechanism contributing to novel lineages within Alaria. We also emphasize the importance of surveying phylogenetic signals across organellar and nuclear genomes, such that models of mixed ancestry become integrated into our evolutionary and taxonomic understanding.

Phylogeography of sugar kelp: Northern ice-age refugia in the Gulf of Alaska.

Many Northeast (NE) Pacific fishes and invertebrates survived Pleistocene glaciations in northern refugia, but the extent that kelps survived in northern areas is uncertain. Here, we test the hypothesis that populations of sugar kelp (Saccharina latissima) persisted in the Gulf of Alaska during ice-age maxima when the western margin of the Cordilleran ice sheet covered coastal areas around the NE Pacific Ocean. We estimated genetic diversities within and phylogeographical relationships among 14 populations along 2,800 km in the NE Pacific and Bering Sea with partial sequences of mitochondrial DNA 5'-cytochrome oxidase subunit I (COI, bp = 624, n = 543), chloroplast DNA ribulose-1,5-bisphosphate carboxylase large subunit-3' (rbcL, bp = 735, n = 514), and 11 microsatellite loci. Concatenated sequences of rbcL and COI showed moderate levels of within-population genetic diversity (mean h = 0.200) but substantial differences among populations (ΦST = 0.834, p < .0001). Microsatellites showed moderate levels of heterozygosity within populations (mean H E = 0.391). Kelps in the same organellar lineage tended to cluster together, regardless of geographic origins, as indicated in a principal coordinate analysis (PCoA) of microsatellite genotypes. The PCoA also showed evidence of nuclear hybridizations between co-occurring organellar lineages. Individual admixture plots with population clusters of K = 2, 6, and 9 showed increasing complexity with considerable historical admixture between some clusters. A time-calibrated phylogeny placed divergences between rbcL-COI lineages at 1.4 million years at most. The time frames of mutation in the rbcL-COI lineages and microsatellite population clusters differed among locations. The existence of ancient lineages in the Gulf of Alaska, moderate levels of genetic diversity, and the absence of departures from neutrality are consistent with northern refugia during multiple Croll-Milankovitch climate cycles in the Pleistocene Epoch.

Biocomplexity in Populations of European Anchovy in the Adriatic Sea.

The sustained exploitation of marine populations requires an understanding of a species' adaptive seascape so that populations can track environmental changes from short- and long-term climate cycles and from human development. The analysis of the distributions of genetic markers among populations, together with correlates of life-history and environmental variability, can provide insights into the extent of adaptive variation. Here, we examined genetic variability among populations of mature European anchovies (n = 531) in the Adriatic (13 samples) and Tyrrhenian seas (2 samples) with neutral and putative non-neutral microsatellite loci. These genetic markers failed to confirm the occurrence of two anchovy species in the Adriatic Sea, as previously postulated. However, we found fine-scale population structure in the Adriatic, especially in northern areas, that was associated with four of the 13 environmental variables tested. Geographic gradients in sea temperature, salinity and dissolved oxygen appear to drive adaptive differences in spawning time and early larval development among populations. Resolving adaptive seascapes in Adriatic anchovies provides a means to understand mechanisms underpinning local adaptation and a basis for optimizing exploitation strategies for sustainable harvests.

Problems and Cautions With Sequence Mismatch Analysis and Bayesian Skyline Plots to Infer Historical Demography.

Sequence mismatch analysis (MMA) and Bayesian skyline plots (BSP) are commonly used to reconstruct historical demography. A survey of 173 research articles (2009-2014), which included estimates of historical population sizes from mtDNA or cpDNA, shows a widespread genetic signature of demographic or spatial population expansion in species of all major taxonomic groups. Associating these expansions with climatic events can provide insights into the origins of lineage diversity, range expansions (or contractions), and speciation. However, several variables can introduce error into reconstructions of demographic history, including levels of sequence polymorphism, sampling scheme, sample size, natural selection, and estimates of mutation rate. Most researchers use substitution rates estimated from divergences in phylogenetic trees dated with fossils, or geological events. Recent studies show that molecular clocks calibrated with phylogenetic divergences can overestimate the timings of population-level events by an order of magnitude. Overestimates disconnect historical population reconstructions from climatic history and confound our understanding of the factors influencing genetic variability. If mismatch distributions and BSPs largely reflect demographic history, the widespread signature of population expansion in vertebrate, invertebrate, and plant populations appears to reflect responses to postglacial climate warming.

Incorporating deep and shallow components of genetic structure into the management of Alaskan red king crab.

Observed patterns of genetic variability among marine populations are shaped not only by contemporary levels of gene flow, but also by divergences during historical isolations. We examined variability at 15 SNP loci and in mtDNA sequences (COI, 665 bp) in red king crab from 17 localities in the North Pacific. These markers define three geographically distinct evolutionary lineages (SNPs, F(CT) = 0.054; mtDNA Φ(CT) = 0.222): (i) Okhotsk Sea-Norton Sound-Aleutian Islands, (ii) southeastern Bering Sea-western Gulf of Alaska, and (iii) Southeast Alaska. Populations in the Bering Sea and in Southeast Alaska are genetically heterogeneous, but populations in the center of the range are homogeneous. Mitochondrial DNA diversity drops from h = 0.91 in the northwestern Pacific to h = 0.24 in the Southeast Alaska. Bayesian skyline plots (BSPs) indicate postglacial population expansions, presumably from ice-age refugia. BSPs of sequences simulated under a demographic model defined by late Pleistocene temperatures failed to detect demographic variability before the last glacial maximum. These results sound a note of caution for the interpretation of BSPs. Population fragmentation in the Bering Sea and in Southeast Alaskan waters requires population management on a small geographic scale, and deep evolutionary partitions between the three geographic groups mandate regional conservation measures.