Glacial vicariance drives phylogeographic diversification in the amphi-boreal kelp Saccharina latissima

Abstract

Glacial vicariance is regarded as one of the most prevalent drivers of phylogeographic structure and speciation among high-latitude organisms, but direct links between ice advances and range fragmentation have been more difficult to establish in marine than in terrestrial systems. Here we investigate the evolution of largely disjunct (and potentially reproductively isolated) phylogeographic lineages within the amphi-boreal kelp Saccharina latissima s. l. Using molecular data (COI, microsatellites) we confirm that S. latissima comprises also the NE Pacific S. cichorioides complex and is composed of divergent lineages with limited range overlap and genetic admixture. Only a few genetic hybrids were detected throughout a Canadian Arctic/NW Greenland contact zone. The degree of genetic differentiation and sympatric isolation of phylogroups suggest that S. latissima s. l. represents a complex of incipient species. Phylogroup distributions compared with paleo-environmental reconstructions of the cryosphere further suggest that diversification within S. latissima results from chronic glacial isolation in disjunct persistence areas intercalated with ephemeral interglacial poleward expansions and admixture at high-latitude (Arctic) contact zones. This study thus supports a role for glaciations not just in redistributing pre-existing marine lineages but also as a speciation pump across multi-glacial cycles for marine organisms otherwise exhibiting cosmopolite amphi-boreal distributions.

Figure 1

Genealogic relationships within Saccharina based on mtCOI sequence data. (a) Bayesian 50% majority-rule consensus tree based on 62 unique sequences. Numbers above and below the branches are Bayesian posterior probabilities (>0.90) and maximum likelihood bootstrap support values (>60), respectively. Horizontal triangles represent collapsed branches, with length (horizontal) representing the distance from the branches’ common node to the tip of the longest branch, and height (vertical) scaled to the number of (unique) sequences collapsed. (b) COI haplotype network of S. latissima sensu lato, showing the four (A–D) inferred mitotypes. Haplotypes are represented by circles sized to their frequency. Black dots represent inferred, unsampled haplotypes.

Figure 2

Range of K2P sequence divergences (%) within recovered genetic entities of Saccharina spp. Boxplots are grouped according to the type of pairwise comparison: intra-specific (left, intra-phylogroup in the case of S. latissima s.l.), inter-phylogroup (mid graph, in orange) and inter-specific (right).

Figure 3

Glacial vicariance and post-glacial secondary contact of Atlantic phylogroups of S. latissima. The hypothetical glacial ranges and re-distribution of mtCOI phylogroups since the LGM (as inferred from indirect phylogeographic and paleoenvironmental data) are illustrated with a sequence of time points starting with (a) maximum ice-sheet size, (b) the opening of the Bering Strait, (c) the collapse of the Laurentide ice-sheet and the transgression of the Hudson Bay and (d) the present. Phylogroups are coloured as in Fig. 1 (COI-A: yellow, COI-B: light green; COI-C: red, COI-D: white). Sites that were also genotyped for microsatellite markers are marked as circles, otherwise stars. Sites in grey correspond to inhospitable areas (emerged, or under ice-sheets and perennial sea-ice) or beyond ice barriers. Maps were generated with QGIS 2.17 (http://qgis.osgeo.org) using modelled ice-sheet and land extent data.

Figure 4

FCA plot based on all individual multilocus genotypes of S. latissima s. l. Solid lines denote mtDNA phylogroups (note the correspondence with microsatellite-based genotypic clusters) and dashed lines further geographic sub-divisions inferred with genotypic data alone. All putative hybrids were detected in NW Greenland (NW Atlantic) within mixed COI-A/COI-C populations. The “temperate” COI-C outlier could result from backcrossing, genotyping error, or other.

Figure 5

Population structure of Saccharina latissima s. l. based on LEA analyses. (a) Percentage ancestry of each genotyped individual (vertical bars) from the northeast Pacific and north Atlantic/Arctic, when the number of ancestral genetic clusters (k) is set to k = 3 (top) and k = 4 (bottom). (b) Percentage ancestry of individuals from the northwest Atlantic and northwest Greenland, for k = 2 (top) and k = 3 (bottom). COI phylogroups are shown on top of each plot for comparison. Population codes as in Table 1, colour codes as in previous figures.

Figure 6

Diagram of the most likely demographic scenarios chosen by the (a) first and (b) second hierarchal levels of ABC analyses.