Gulf and Glacier or The Percivals in Alaska
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However, natural processes e. Eelgrass populations along the Alaska Peninsula Fig 1 and the eastern portion of the Aleutian Archipelago are of considerable phytogeographic interest because they occur along the southern margin of what was once the Bering Land Bridge. The Alaska Peninsula, together with the Aleutian Archipelago, functions as an important intercontinental bridge for dispersal for both marine and terrestrial organisms.
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For species that occur in coastal marine and terrestrial habitats along the Alaska Peninsula and the Aleutian chain, evolutionary dispersal gene flow between continents can occur in at least two directions: westward from North America along the Alaska Peninsula through the Aleutian Island Archipelago to Kamchatka, and eastward from Eurasia, toward interior Alaska and the Pacific coast [ 27 ]. Thus, while we are unaware of the existence of any specimens of Z. Gray areas in the water indicate trenches. Ocean current data are compiled, but not identical to, figures from Stabeno and Reed [ 30 , 31 ].
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Differences in gene flow polarity among populations of marine organisms in the different LMEs may reflect the different ocean current circulation patterns. Unlike other oceanic currents, which experience wide variations in localized kinetic energy such as the Gulf Stream , the Alaska Stream is a narrow and consistent high speed current [ 30 ], which may impact polarity of gene flow among populations of marine organisms [ 30 , 33 ].
Circulation is predominantly cyclonic counter clockwise in the Bering Sea basin [ 34 ]; the Aleutian North Slope Current flows eastward along the northern slope of the Aleutian Islands, then turns northwestern to form the Bering Slope Current, whereas the southward flowing Kamchatka Current forms the western boundary current [ 34 , 35 ].
Circulation in the Bering Sea is strongly influenced by the Alaska Stream, which enters the Bering Sea through 14 passes along the Aleutian Archipelago, which acts as a porous boundary between the North Pacific and the Bering Sea [ 35 ]. Inflow into the Bering Sea is balanced by outflow through the Kamchatka Current such that circulation is a continuation of the North Pacific subarctic gyre, moving eastward along waters off the northern shore of the Alaska Peninsula Fig 1.
Flow through the pass is predominantly baroclinic, with speed of northward transport maximizing in the fall and winter and minimizing in the late spring and summer.
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Eddies are also ubiquitous in the Bering Sea; these are often anticyclonic in both the eastern and western side of the basin, and may facilitate localized deviations from net ocean current flow. Ocean currents, oceanographic mixing patterns, geographic barriers, and distance all influence eelgrass distribution and apparently play a role in the differentiation of Z.
Although seed rafting on floating reproductive shoots may be an effective form of dispersal for eelgrass [ 40 , 41 ], dispersal of both pollen [ 42 ] and seeds [ 43 ] is typically limited to just a few meters even in areas with strong tidal currents. Thus, the species is expected to show significant interpopulational structuring. Further, extensive vegetative reproduction through branching of rhizomes and formation of shoots is expected to limit genetic diversity within local subpopulations and amplify genetic structure between populations.
Although flowering response apparently increases at the extremes of Z. Thus, levels of population differentiation likely increase latitudinally, while diversity will likely decrease, as observed in other plants [ 45 ] although see [ 37 ] for disparate signals in eelgrass of the North Atlantic. Given ocean currents play an important role in the movement of gametes and individuals between populations, gene flow between discrete populations as assayed using a coalescence approach [ 46 , 47 ] should correspond to net movement of ocean currents.
We expect eelgrass populations in high-latitude habitats to show lower levels of genetic diversity than southern populations, and be significantly partitioned at the interpopulational level. Further, at least regionally, prevailing direction of gene flow should correspond to ocean current patterns, which differ between the two LMEs separated by the Alaska Peninsula and Aleutian Island archipelago. However, unlike for peninsulas elsewhere on the Pacific coast of North America that may sharply restrict or prohibit gene flow among eelgrass populations [ 38 ], the boundary between the EBS- and GoA-LMEs may be relatively semipermeable for eelgrass, particularly at False Pass, east of Unimak Island where a portion of the Alaska Coastal Current flows northeastward into the Aleutian North Slope Current.
Thus, it is unclear whether the Alaska Peninsula, as well as different current velocities and mixing regimes in the EBS- and GoA-LMEs, have constituted an effective historical dispersal barrier for this species, as have similar landscape features and ocean currents elsewhere in North America [ 38 ], and whether interregional structure is present, as in some other marine species in the region [ 48 — 50 ]. The central aim of this study is to characterize genetic structure in largely undisturbed native populations of Z.
Using nuclear microsatellite markers and nucleotide sequence information from the chloroplast maturase K gene mat K and the nuclear 5. Because the population genetic structure of marine angiosperms, as in other species, has been influenced by Pleistocene environmental events [ 52 ], and because ice-free regions in the high latitude Pacific have been hypothesized as Last Glacial Maximum LGM refugia for eelgrass and a source of colonization for North Atlantic populations [ 37 ], we also v test for genetic signatures consistent with the presence of LGM refugia in these high latitude Northeast Pacific region populations.
All eelgrass samples collected in United States waters were obtained on public access lands, and all researchers sampling in United States waters, including California, received permission for sampling eelgrass from the appropriate state regulatory agencies where required e. Eelgrass samples from Yaquina Bay were obtained on public access lands and no permission was required because the plant species is not endangered or protected in the area sampled. In Alaska, permission was also obtained from the specific U.
Fish and Wildlife Service Refuges for sampling on Refuge lands. The species is not considered endangered or protected in areas where the sampling occurred in waters of either the United States, or Mexico. Eelgrass meadows from 12 sites along the mid-to-northern Pacific Coast of North America were sampled during summer months between — Fig 2. Eelgrass from the Kuskokwim Shoals KS inhabits small embayments associated with barrier islands forming the Kuskokwim Shoals in the northern Kuskokwim Bay.
Sample locales for Z. Arrows indicate direction of prevailing seasonal surface currents derived from Brower et al. At all but one study site KS , eight to sixty individuals of Z. Plants were scraped clean of visible epiphytes and invertebrates, blotted dry with paper towels and stored in powdered silica gel until DNA was extracted from leaf tissue.
All individuals in each population were sampled within an area smaller than , m 2. This area is much larger than the genetic neighborhood area — m 2 for eelgrass suggested by Ruckelshaus [ 42 , 55 ] and Reusch et al. See S1 Methods for details of laboratory analyses. Following extraction and quantification of DNA, nucleotide sequence data from basepairs bp of the Zostera chloroplast maturase K mat K gene and bp of the 5. Sequence data were collected from 3—12 samples at the 11 locales along the coast of Alaska.
Fragment data were collected at 10 polymorphic microsatellite loci [ 56 , 57 ] from the 12 locales in Alaska, following procedures outlined elsewhere [ 38 , 58 ]. As well, sequences were compared to homologous information from both loci obtained from accessioned specimens used by Talbot et al. Nevertheless, we assumed that if two different Zostera species occupied habitats within the two high latitude LMEs, and Z. Homologous sequence from three other species of Zostera Z. Details of analyses to assess levels of genetic diversity at microsatellite loci are provided in S1 Methods.
To determine the level of clonality and generate a dataset for subsequent population genetics analysis, we employed the match statistics option in Microsatellite Toolkit [ 65 ] to identify samples sharing identical multilocus genotypes, presumably representing a single clone, among the samples, and GenClone ver. Populations with a value of R at unity have 0. Following assessment of R, the dataset was pruned by eliminating data from all but one sample representing a genetic individual a genet.
This pruned dataset was used to test the power to detect individuals by calculating the probability of observing identical multilocus genotypes between two individuals sampled from a population P ID and P IDsib ; [ 68 ] , using the program GIMLET v.
We quantified genetic variation using data from genets only and tested for neutrality in microsatellite loci using a variety of computer programs routinely used to analyze genetic data [ 70 , 71 ]. In all cases of multiple tests, significance levels were adjusted using sequential Bonferroni corrections [ 72 ]. Details of analyses to assess levels of population and regional structure are provided in S1 Methods. Significance of tests based on random permutation of alleles between populations, and p-values were adjusted using Bonferroni corrections.
To further investigate the pattern of population structuring, we also applied a Bayesian clustering approach [ 81 ]. Each Bayesian clustering analysis was repeated 10 times to ensure consistency across runs. We also investigated genetic structuring and visualized regional and between-population by conducting discriminant analyses of principal components DAPC , using the R package adegenet [ 82 , 83 ]. Optimal cluster number within each region and population was determined using sequential k-means algorithm on principal components and discriminant functions transformed data and compared to original population identification, with probability of membership in each population determined for each sample [ 84 ].
Statistical significance of variance measures was assessed via non-parametric permutation [ 77 ]. We used IBD 3. Reduced-major-axis regression implemented in the program IBD was used to determine the slope of significant regression for the Pacific coast and Bering Sea graphs.
An inverse relationship between genetic diversity and latitude is expected if genetic diversity decreases constantly along a latitudinal gradient following an isolation-by-distance pattern. We estimated the magnitude and polarity of gene flow among populations within the two regions using the maximum likelihood approach implemented in MIGRATE 2. Competing models were evaluated for goodness-of-fit given the data using a log-likelihood ratio test. Combined with data from [ 16 ], a total of and samples were used to make inference from these gene region, respectively S1 Fig.
A A parsimony network of chloroplast mat K haplotypes assayed from Z. Homologous data from Z. The size of the node corresponds to the frequency of each haplotype within each LME or region, and length of branch corresponds to number of changes, unless noted with diagonal slant bars. The small white diamond indicates an intermediate ancestral allele that was not sampled. B Neighbor-joining tree illustrating relationships among Pacific coast populations of Z. D CE distances were generated by data from 10 microsatellite loci. Bootstrap values replications are listed at the node.
Black, white, and gray circles identify populations belonging to the three discrete groupings Model D uncovered via AMOVA analyses to reflect significant and highest allelic variance at the regional level see Results, in text, and S1 Table. In no instance were identical genotypes observed in samples from across two or more populations.
Number of alleles detected per locus ranged from four CT, GA-4 to 43 CT and the mean number of alleles per locus per population observed allelic diversity ranged from 2. Allelic richness, calculated based on the sample size at UNGA, varied from 1. Average H E within populations ranged from 0. Overall H E was 0. Overall H O was 0. This is lower than the number of spurious results expected for pairwise comparisons Given the general adherence to HWE expectations and lack of significant linkage disequilibrium, coupled with the results of the sequence analysis of chloroplast and nuclear loci, we conclude that our populations are comprised of Z.
All data from genets and across loci were retained for analysis of population structure. However, while AMOVA analyses based on the assumption of SMM also found variance to be significantly partitioned among populations within regions for all models e. Using 15 inferred clusters, YAB and WB were largely recovered as inferred populations 7 and 15, while other populations were divided among many inferred groupings with shared original sample populations, including SCC in 2, 4—6, and 8—10, KIL in 1, 4—6, 8—10, and 12 and IZL in 2, 4—6, and 8—10 S3A Fig.
A scatterplot of the first two discriminant functions of the DAPC, representing The first two discriminant functions represent the majority of the genetic variation in each dataset, including In the 12 populations distributed in a south-north latitudinal gradient, H E and AR correlated inversely with latitude, explaining These results emphasize a decrease in genetic diversity in a southern to northern latitudinal gradient in eelgrass distribution along the north Pacific coast of North America.
Mean expected heterozygosity H E and allelic richness AR for each of the 12 populations. Each point represents a population from this study or from previous studies [ 38 , 58 ]. Regression lines are shown for H E solid line and AR dashed line. Maximum likelihood estimates based on Markov Chain Monte Carlo simulations suggest that the direction of gene flow among populations on the Pacific coast is predominantly westward Fig 6 , S4 Table.
Similar analyses for Bering Sea populations suggested most comparisons involved cyclonic polarity, as movement was eastward, then northward S3 Table , Fig 6.
Gulf and Glacier; or, The Percivals in Alaska
Black arrows indicate symmetrical gene flow concordant with surface current flow; red arrows show asymmetrical gene flow that contrasts with surface current flow. This study represents the first characterization of macrogeographic population genetic parameters among undisturbed meadows of Z.
As such, it provides a foundational assessment of genetic diversity of eelgrass in the region. Fundamental to assessing genetic structure of Z.