North Atlantic phylogeography and large-scale population differentiation of the seagrass Zostera marina L (original) (raw)

Range-edge genetic diversity: locally poor extant southern patches maintain a regionally diverse hotspot in the seagrass Zostera marina

Refugial populations at the rear edge are predicted to contain higher genetic diversity than those resulting from expansion, such as in post-glacial recolonizations. However, peripheral populations are also predicted to have decreased diversity compared to the centre of a species’ distribution. We aim to test these predictions by comparing genetic diversity in populations at the limits of distribution of the seagrass Zostera marina, with populations in the species’ previously described central diversity ‘hotspot’. Zostera marina populations show decreased allelic richness, heterozygosity and genotypic richness in both the ‘rear’ edge and the ‘leading’ edge compared to the diversity ‘hotspot’ in the North Sea ⁄ Baltic region. However, when populations are pooled, genetic diversity at the southern range is as high as in the North Sea ⁄ Baltic region while the ‘leading edge’ remains low in genetic diversity. The decreased genetic diversity in these southern Iberian populations compared to more central populations is possibly the effect of drift because of small effective population size, as a result of reduced habitat, low sexual reproduction and low gene flow. However, when considering the whole southern edge of distribution rather than per population, diversity is as high as in the central ‘hotspot’ in the North Sea ⁄ Baltic region. We conclude that diversity patterns assessed per population can mask the real regional richness that is typical of rear edge populations, which have played a key role in the species biogeographical history and as marginal diversity hotspots have very high conservation value.

The Structure of Genetic Diversity in Eelgrass (Zostera marina L.) along the North Pacific and Bering Sea Coasts of Alaska

PLOS ONE, 2016

Eelgrass (Zostera marina) populations occupying coastal waters of Alaska are separated by a peninsula and island archipelago into two Large Marine Ecosystems (LMEs). From populations in both LMEs, we characterize genetic diversity, population structure, and polarity in gene flow using nuclear microsatellite fragment and chloroplast and nuclear sequence data. An inverse relationship between genetic diversity and latitude was observed (heterozygosity: R 2 = 0.738, P < 0.001; allelic richness: R 2 = 0.327, P = 0.047), as was significant genetic partitioning across most sampling sites (θ = 0.302, P < 0.0001). Variance in allele frequency was significantly partitioned by region only in cases when a population geographically in the Gulf of Alaska LME (Kinzarof Lagoon) was instead included with populations in the Eastern Bering Sea LME (θ p = 0.128-0.172; P < 0.003), suggesting gene flow between the two LMEs in this region. Gene flow among locales was rarely symmetrical, with notable exceptions generally following net coastal ocean current direction. Genetic data failed to support recent proposals that multiple Zostera species (i.e. Z. japonica and Z. angustifolia) are codistributed with Z. marina in Alaska. Comparative analyses also failed to support the hypothesis that eelgrass populations in the North Atlantic derived from eelgrass retained in northeastern Pacific Last Glacial Maximum refugia. These data suggest northeastern Pacific populations are derived from populations expanding northward from temperate populations following climate amelioration at the terminus of the last Pleistocene glaciation.

Eelgrass Zostera marina populations in northern Norwegian fjords are genetically isolated and diverse

Marine Ecology Progress Series, 2013

Populations along the northern boundary of a marine species' distributional range in the NE Atlantic are expected to harbor lower standing genetic variation as a consequence of postglacial expansion following the last glacial maximum. Founder events and marginal habitat availability may render the edge populations more vulnerable to anthropogenic stress and less capable of rapid adaptation to global climate change, a concern for conservation and management. We analyzed meadow architecture, persistence and connectivity within and among 15 locations (600 samples genotyped with 8 microsatellite loci) in 3 fjords in Troms County, Norway (69°N). Whereas global mean allelic diversity (standardized for sample size) was in accordance with previous studies using the same markers, more extensive sampling revealed a broader range of allelic richness (mean = 2.85; range = 1.84 to 4.21) in the regional pool. Genotypic diversity was typically high, whereas large genets were rare (2 out of 15 locations). Population differentiation (F ST) was 2 to 6 times higher between fjords than within fjords. A Bayesian (STRUCTURE) analysis also strongly supported the genetic distinctness of each fjord. Although 9 locations within the 60 km long Balsfjord were connected by gene flow, demographic connectivity may actually be low, as fixed differences were observed at 6 of the 9 locations, along with significantly positive inbreeding coefficients and strong substructure. Overall, our results suggest that these northern, leading-edge meadows are healthy, but vigilance is required to avoid further losses. Fjord-level management, especially of the larger fjords, will be sufficient to capture the range of variation.

Genetic characteristics of three Baltic Zostera marina populations**This work was financially supported by the project: ‘ZOSTERA: Restoration of ecosystem key elements in the inner Puck Bay’

Oceanologia, 2014

We performed genetic analyses of three Baltic eelgrass (Zostera marina) populations in Puck Bay (PB), Cudema Bay (CB) and Greifswalder Bodden (GB). The aim of this study was to identify the eelgrass population genetically closest to that from the PB, which could potentially serve as a reservoir for the restoration of the underwater meadows in this bay, seriously degraded in the past. We applied a 12-microsatellite assay to test the genetic distance between the target eelgrass populations. We found that the allelic richness values of the GB, PB and CB populations were 2.25, 3.77 and 3.50 respectively. The genetic diversity found in GB was low and could be explained by the population's history, whereas the diversity of CB was higher than expected in a population located at the edge of the species' range. Analyses of genetic differentiation and structure showed that of the three populations studied, PB and CB were closer to each other than to the GB population. The reasons for this differentiation in eelgrass populations and the implications of the results of their genetic analysis on the planned restoration of the PB populations are discussed.

Population genetics of dwarf eelgrass Zostera noltii throughout its biogeographic range

Marine Ecology-progress Series, 2004

The marine angiosperm Zostera noltii (dwarf eelgrass), an important facilitator species and food source for invertebrates and waterfowl, predominantly inhabits intertidal habitats along eastern Atlantic shores from Mauritania to southern Norway/Kattegat Sea and throughout the Mediterranean, Black and Azov seas. We used 9 microsatellite loci to characterize population structure at a variety of spatial scales among 33 populations from 11 localities throughout the entire biogeographic range. Isolation by distance analysis suggested a panmictic genetic neighborhood of 100 to 150 km. At the global scale, a neighbor-joining tree based on Reynolds distances revealed strongly-supported groups corresponding to northern Europe, Mauritania and the Black/Azov Sea; separate Mediterranean and Atlantic-Iberian groups were poorly supported. Clones (genets with multiple ramets) were present in most populations but were generally small (ca. < 3 m 2 ). Exceptions were found in Mauritania (ca. 29 m in length), the Azov Sea (ca. 40 m in length) and the Black Sea (ca. 50 m in length). Although genetic diversity and allelic richness generally decreased from Mauritania to Denmark, the putative post-glacial recolonization route, both were unexpectedly high among populations from the German Wadden Sea.

Holocene re-colonisation, central-marginal distribution and habitat specialisation shape population genetic patterns within an Atlantic European grass species

Plant biology (Stuttgart, Germany), 2014

Corynephorus canescens (L.) P.Beauv. is an outbreeding, short-lived and wind-dispersed grass species, highly specialised on scattered and disturbance-dependent habitats of open sandy sites. Its distribution ranges from the Iberian Peninsula over Atlantic regions of Western and Central Europe, but excludes the two other classical European glacial refuge regions on the Apennine and Balkan Peninsulas. To investigate genetic patterns of this uncommon combination of ecological and biogeographic species characteristics, we analysed AFLP variation among 49 populations throughout the European distribution range, expecting (i) patterns of SW European glacial refugia and post-glacial expansion to the NE; (ii) decreasing genetic diversity from central to marginal populations; and (iii) interacting effects of high gene flow and disturbance-driven genetic drift. Decreasing genetic diversity from SW to NE and distinct gene pool clustering imply refugia on the Iberian Peninsula and in western Fran...

Ocean current patterns drive the worldwide colonization of eelgrass (Zostera marina)

Nature Plants

Currents are unique drivers of oceanic phylogeography and thus determine the distribution of marine coastal species, along with past glaciations and sea-level changes. Here we reconstruct the worldwide colonization history of eelgrass (Zostera marina L.), the most widely distributed marine flowering plant or seagrass from its origin in the Northwest Pacific, based on nuclear and chloroplast genomes. We identified two divergent Pacific clades with evidence for admixture along the East Pacific coast. Two west-to-east (trans-Pacific) colonization events support the key role of the North Pacific Current. Time-calibrated nuclear and chloroplast phylogenies yielded concordant estimates of the arrival of Z. marina in the Atlantic through the Canadian Arctic, suggesting that eelgrass-based ecosystems, hotspots of biodiversity and carbon sequestration, have only been present there for ~243 ky (thousand years). Mediterranean populations were founded ~44 kya, while extant distributions along w...

Low genotypic diversity and long-term ecological decline in a spatially structured seagrass population

Scientific Reports, 2019

In isolated or declining populations, viability may be compromised further by loss of genetic diversity. Therefore, it is important to understand the relationship between long-term ecological trajectories and population genetic structure. However, opportunities to combine these types of data are rare, especially in natural systems. Using an existing panel of 15 microsatellites, we estimated allelic diversity in seagrass, Zostera marina, at five sites around the Isles of Scilly Special Area of Conservation, UK, in 2010 and compared this to 23 years of annual ecological monitoring (1996–2018). We found low diversity and long-term declines in abundance in this relatively pristine but isolated location. Inclusion of the snapshot of genotypic, but less-so genetic, diversity improved prediction of abundance trajectories; however, this was spatial scale-dependent. Selection of the appropriate level of genetic organization and spatial scale for monitoring is, therefore, important to identif...

Ocean currents drive the worldwide colonization of the most widespread marine plant, eelgrass (Zostera marina)

Currents are unique drivers of oceanic phylogeography and so determine the distribution of marine coastal species, along with past glaciations and sea level changes. Here, we reconstruct the worldwide colonization history of eelgrass (Zostera marinaL.), the most widely distributed marine flowering plant or seagrass from its origin in the Northwest Pacific, based on nuclear and chloroplast genomes. We identified two divergent Pacific clades with evidence for admixture along the East Pacific coast. Multiple west to east (trans-Pacific) colonization events support the key role of the North Pacific Current. Time-calibrated nuclear and chloroplast phylogenies yielded concordant estimates of the arrival ofZ. marinain the Atlantic through the Canadian Arctic, suggesting that eelgrass-based ecosystems, hotspots of biodiversity and carbon sequestration, have only been present since ∼208 Kya (thousand years ago). Mediterranean populations were founded ∼53 Kya while extant distributions along ...

Genetic characteristics of three Baltic Zostera marina populations

We performed genetic analyses of three Baltic eelgrass (Zostera marina) populations in Puck Bay (PB), Cudema Bay (CB) and Greifswalder Bodden (GB). The aim of this study was to identify the eelgrass population genetically closest to that from the PB, which could potentially serve as a reservoir for the restoration of the underwater meadows in this bay, seriously degraded in the past. We applied a 12-microsatellite assay to test the genetic distance between the target eelgrass populations. We found that the allelic richness values of the GB, PB and CB populations were 2.25, 3.77 and 3.50 respectively. The genetic diversity found in GB was low and could be explained by the population's history, whereas the diversity of CB was higher than expected in a population located at the edge of the species' range. Analyses of genetic differentiation and structure showed that of the three populations studied, PB and CB were closer to each other than to the GB population. The reasons for this differentiation in eelgrass populations and the implications of the results of their genetic analysis on the planned restoration of the PB populations are discussed.