Ocean currents drive the worldwide colonization of the most widespread marine plant, eelgrass (Zostera marina) (original) (raw)
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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...
Molecular Ecology, 2004
As the most widespread seagrass in temperate waters of the Northern Hemisphere, Zostera marina provides a unique opportunity to investigate the extent to which the historical legacy of the last glacial maximum ( LGM18 000 -10 000 years BP ) is detectable in modern population genetic structure. We used sequences from the nuclear rDNA-internal transcribed spacer (ITS) and chloroplast mat K-intron, and nine microsatellite loci to survey 49 populations (> 2000 individuals) from throughout the species' range. Minimal sequence variation between Pacific and Atlantic populations combined with biogeographical groupings derived from the microsatellite data, suggest that the trans -Arctic connection is currently open. The east Pacific and west Atlantic are more connected than either is to the east Atlantic. Allelic richness was almost two-fold higher in the Pacific. Populations from putative Atlantic refugia now represent the southern edges of the distribution and are not genetically diverse. Unexpectedly, the highest allelic diversity was observed in the North Sea-Wadden Sea-southwest Baltic region. Except for the Mediterranean and Black Seas, significant isolation-by-distance was found from ~150 to 5000 km. A transition from weak to strong isolation-by-distance occurred at ~150 km among northern European populations suggesting this scale as the natural limit for dispersal within the metapopulation. Links between historical and contemporary processes are discussed in terms of the projected effects of climate change on coastal marine plants. The identification of a high genetic diversity hotspot in Northern Europe provides a basis for restoration decisions.
Genomic Comparison of Two Independent Seagrass Lineages Reveals Habitat-driven Convergent Evolution
Journal of experimental botany, 2018
Seagrasses are marine angiosperms that live fully submerged in the sea. They evolved from land plant ancestors, with multiple species representing at least three independent return to the sea events. This raises the question whether these marine angiosperms followed the same adaptation pathway to allow them to live and reproduce under the hostile marine conditions. To compare the basis of marine adaptation between seagrass lineages, we generated genomic data for Halophila ovalis and compared this with recently published genomes for two members of Zosteraceae, as well as genomes of five non-marine plant species (Arabidopsis thaliana, Oryza sativa, Phoenix dactylifera, Musa acuminata, and Spirodela polyrhiza). Halophila and Zosteraceae represent two independent seagrass lineages separated by around 30 My. Genes that are lost or conserved in both lineages were identified. All three species lost genes associated with ethylene and terpenoid biosynthesis, and retained genes related to sal...
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.
Biological Conservation, 2017
While our knowledge of species distributions and diversity in the terrestrial biosphere has increased sharply over the last decades, we lack equivalent knowledge of the marine world. Here, we use the phylogenetic tree of seagrasses along with their global distributions and a metric of phylogenetic beta diversity to generate a phylogenetically-based delimitation of marine phytoregions (phyloregions). We then evaluate their evolutionary affinities and explore environmental correlates of phylogenetic turnover between them. We identified 11 phyloregions based on the clustering of phylogenetic beta diversity values. Most phyloregions can be classified as either temperate or tropical, and even geographically disjunct temperate regions can harbor closely related species assemblages. Geographic differences in sea surface temperatures account for more phylogenetic turnover than either water salinity or bathymetry. We also found a strong temperate-tropical gradient in evolutionary distinctiveness, with temperate phyloregions being the most evolutionarily unique. Our results highlight differences between the marine and terrestrial worlds, and suggest that the interplay between long-distance dispersal and phylogenetic niche conservatism played a central role in determining the contemporary distributions of seagrasses worldwide.
An Unrecognized Ancient Lineage of Green Plants Persists in Deep Marine WATERS1
Journal of Phycology, 2010
We provide molecular phylogenetic evidence that the obscure genera Palmophyllum Kütz. and Verdigellas D. L. Ballant. et J. N. Norris form a distinct and early diverging lineage of green algae. These palmelloid seaweeds generally persist in deep waters, where grazing pressure and competition for space are reduced. Their distinctness warrants recognition as a new order, the Palmophyllales. Although phylogenetic analyses of both the 18S rRNA gene and two chloroplast genes (atpB and rbcL) are in agreement with a deep-branching Palmophyllales, the genes are in conflict about its exact phylogenetic placement. Analysis of the nuclear ribosomal DNA allies the Palmophyllales with the prasinophyte genera Prasinococcus and Prasinoderma (Prasinococcales), while the plastid gene phylogeny placed Palmophyllum and Verdigellas as sister clade to all other Chlorophyta.
Molecular Ecology, 2007
The rhodophyte seaweed Asparagopsis armata Harvey is distributed in the northern and southern temperate zones, and its congener Asparagopsis taxiformis (Delile) Trevisan abounds throughout the tropics and subtropics. Here, we determine intraspecific phylogeographic patterns to compare potential causes of the disjunctions in the distributions of both species. We obtained specimens throughout their ranges and inferred phylogenies from the hypervariable domains D1-D3 of the nuclear rDNA LSU, the plastid spacer between the large and small subunits of RuBisCo and the mitochondrial cox 2-3 intergenic spacer. The cox spacer acquired base changes the fastest and the RuBisCo spacer the slowest. Median-joining networks inferred from the sequences revealed the absence of phylogeographic structure in the introduced range of A. armata , corroborating the species' reported recent introduction. A. taxiformis consisted of three nuclear, three plastid and four mitochondrial genetically distinct, lineages (1-4). Mitochondrial lineage 3 is found in the western Atlantic, the Canary Islands and the eastern Mediterranean. Mitochondrial lineages 1, 2, and 4 occur in the Indo-Pacific, but one of them (lineage 2) is also found in the central Mediterranean and southern Portugal. Phylogeographic results suggest separation of Atlantic and Indo-Pacific lineages resulted from the emergence of the Isthmus of Panama, as well as from dispersal events postdating the closure event, such as the invasion of the Mediterranean Sea by mitochondrial lineages 2 and 3. Molecular clock estimates using the Panama closure event as a calibration for the split of lineages 3 and 4 suggest that A. taxiformis diverged into two main cryptic species (1 + 2 and 3 + 4) about 3.2-5.5 million years ago (Ma), and that the separation of the mitochondrial lineages 1 and 2 occurred 1-2.3 Ma.
An unrecognized ancient lineage of green plants persists in deep marine waters
We provide molecular phylogenetic evidence that the obscure genera Palmophyllum Kütz. and Verdigellas D. L. Ballant. et J. N. Norris form a distinct and early diverging lineage of green algae. These palmelloid seaweeds generally persist in deep waters, where grazing pressure and competition for space are reduced. Their distinctness warrants recognition as a new order, the Palmophyllales. Although phylogenetic analyses of both the 18S rRNA gene and two chloroplast genes (atpB and rbcL) are in agreement with a deep-branching Palmophyllales, the genes are in conflict about its exact phylogenetic placement. Analysis of the nuclear ribosomal DNA allies the Palmophyllales with the prasinophyte genera Prasinococcus and Prasinoderma (Prasinococcales), while the plastid gene phylogeny placed Palmophyllum and Verdigellas as sister clade to all other Chlorophyta.
The genome of a southern hemisphere seagrass species (Zostera muelleri)
Plant physiology, 2016
Seagrasses are marine angiosperms that evolved from land plants, but returned to the sea around 140 Mya during the early evolution of monocotyledonous plants. They successfully adapted to abiotic stresses associated with growth in the marine environment, and today seagrasses are distributed in coastal waters worldwide. Seagrass meadows are an important oceanic carbon sink and provide food and breeding grounds for diverse marine species. Here we report the assembly and characterisation of the Zostera muelleri genome, a southern hemisphere temperate species. Multiples genes were lost or modified in Z. muelleri compared to terrestrial or floating aquatic plants that are associated with their adaptation to life in the ocean. These include genes for hormone biosynthesis and signalling, and cell wall catabolism. There is evidence of whole genome duplication in Z. muelleri however, an ancient pan-Commelinid duplication event is absent, highlighting the early divergence of this species from...