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PeerJ
2022 Oct 06;10:e13930. doi: 10.7717/peerj.13930.
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Trans-Arctic vicariance in Strongylocentrotus sea urchins.
Addison JA
,
Kim J
.
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The sea urchins Strongylocentotus pallidus and S. droebachiensis first invaded the Atlantic Ocean from the Pacific following the opening of the Bering seaway in the late Miocene. While trans-Arctic dispersal during the Pleistocene is thought to have maintained species' integrity, a recent genomic analysis identified a reproductively isolated cryptic species within S. droebachiensis. Based on previous studies, the distribution of one of these lineages (S. droebachiensis W) includes the shallow water habitats of the northwest Atlantic and Pacific, while the other (S. droebachiensis E) is found throughout the shallow habitat in the northeast but is mostly restricted to deep habitats (>65 m) in the northwest Atlantic. However, since genetic variation within S. droebachiensis has been largely unstudied in the north Pacific and Arctic oceans, the biogeography of the cryptic species is not well known, and it is difficult to identify the mechanisms driving population subdivision and speciation. Here we use population genetic analyses to characterize the distribution of each species, and to test hypotheses about the role of vicariance in the evolution of systematic and genomic divergence within the genus. We collected individuals of all three Strongylocentrotus species (n = 365) from 10 previously unsampled locations in the northeast Pacific and north Atlantic (Labrador Sea and Norway), and generated mtDNA sequence data for a 418 bp fragment of cytochrome c oxidase subunit I (COI). To assess the biogeography of all three species, we combined our alignment with five previously published data sets (total n = 789) and used statistical parsimony and maximum likelihood to identify species and characterize their distribution within and among oceans. Patterns of haplotype sharing, pairwise F ST , and hierarchical analyses of molecular variance (AMOVA) identified trans-Arctic dispersal in S. pallidus and S. droebachiensis W, but other than 5 previously reported singletons we failed to detect additional mtDNA haplotypes of S. droebachiensis E in the north Pacific. Within the Atlantic, patterns of habitat segregation suggests that temperature may play a role in limiting the distribution of S. droebachiensis E, particularly throughout the warmer coastal waters along the coast of Nova Scotia. Our results are consistent with the cycles of trans-Arctic dispersal and vicariance in S. pallidus and S. droebachiensis W, but we suggest that the evolution of Atlantic populations of S. droebachiensis E has been driven by persistent trans-Arctic vicariance that may date to the initial invasion in the late Pliocene.
Figure 1. (A) Sample sites of Strongylocentrotus sea urchins throughout the North Pacific and north Atlantic oceans (see Table 1 for abbreviations). Pie charts represent the proportion of mtDNA haplotypes (418 bp COI) belonging to each of the three lineages. (B) Inset map of samples collected throughout Atlantic Canada. (C) TCS haplotype network of COI mtDNA sequences from all three lineages of Strongylocentrotus sea urchins (n = 789) included in this study. Circle area is proportionate to the number of haplotypes sequenced and the colours of each lineage match the pie charts from A and B.Node support indicated by nonparametric bootstrap (1,000 replicates) and Bayesian posterior probability, respectively. Overall mean K2P distances are within each lineage is indicated in the boxes, and mean pairwise distances are indicated along the vectors.
Figure 2. Sampling locations, haplotype distribution, and TCS haplotype network of COI mtDNAsequences for Strongylocentrotus pallidus (n = 156).Asterisks (*) indicate the mtDNA haplotypes removed from analyses of population genetic structure because they were recovered in individuals whose nuclear genomes (SNPs or microsatellites) were characterized as being 100% S. droebachiensis W (# tested/# individuals with the haplotype).
Figure 3. Sampling locations, haplotype distribution, and TCS haplotype network of COI mtDNA sequences for Strongylocentrotus droebachiensis E (n = 148).
Figure 4. Sampling locations, haplotype distribution, and TCS haplotype network of COI mtDNA sequences for Strongylocentrotus droebachiensis W (n = 485).
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