Cryptic diversity in southern African kelp.

The southern coast of Africa is one of the few places in the world where water temperatures are predicted to cool in the future. This endemism-rich coastline is home to two sister species of kelps of the genus Ecklonia maxima and Ecklonia radiata, each associated with specific thermal niches, and occuring primarily on opposite sides of the southern tip of Africa. Historical distribution records indicate that E. maxima has recently shifted its distribution ~ 70 km eastward, to sites where only E. radiata was previously reported. The contact of sister species with contrasting thermal affinities and the occurrence of mixed morphologies raised the hypothesis that hybridization might be occurring in this contact zone. Here we describe the genetic structure of the genus Ecklonia along the southern coast of Africa and investigate potential hybridization and cryptic diversity using a combination of nuclear microsatellites and mitochondrial markers. We found that both species have geographically discrete genetic clusters, consistent with expected phylogeographic breaks along this coastline. In addition, depth-isolated populations were found to harbor unique genetic diversity, including a third Ecklonia lineage. Mito-nuclear discordance and high genetic divergence in the contact zones suggest multiple hybridization events between Ecklonia species. Discordance between morphological and molecular identification suggests the potential influence of abiotic factors leading to convergent phenotypes in the contact zones. Our results highlight an example of cryptic diversity and hybridization driven by contact between two closely related keystone species with contrasting thermal affinities.

Past climate-driven range shifts structuring intraspecific biodiversity levels of the giant kelp (Macrocystis pyrifera) at global scales.

The paradigm of past climate-driven range shifts structuring the distribution of marine intraspecific biodiversity lacks replication in biological models exposed to comparable limiting conditions in independent regions. This may lead to confounding effects unlinked to climate drivers. We aim to fill in this gap by asking whether the global distribution of intraspecific biodiversity of giant kelp (Macrocystis pyrifera) is explained by past climate changes occurring across the two hemispheres. We compared the species' population genetic diversity and structure inferred with microsatellite markers, with range shifts and long-term refugial regions predicted with species distribution modelling (SDM) from the last glacial maximum (LGM) to the present. The broad antitropical distribution of Macrocystis pyrifera is composed by six significantly differentiated genetic groups, for which current genetic diversity levels match the expectations of past climate changes. Range shifts from the LGM to the present structured low latitude refugial regions where genetic relics with higher and unique diversity were found (particularly in the Channel Islands of California and in Peru), while post-glacial expansions following ~ 40% range contraction explained extensive regions with homogenous reduced diversity. The estimated effect of past climate-driven range shifts was comparable between hemispheres, largely demonstrating that the distribution of intraspecific marine biodiversity can be structured by comparable evolutionary forces across the global ocean. Additionally, the differentiation and endemicity of regional genetic groups, confers high conservation value to these localized intraspecific biodiversity hotspots of giant kelp forests.

Long range gene flow beyond predictions from oceanographic transport in a tropical marine foundation species.

The transport of passively dispersed organisms across tropical margins remains poorly understood. Hypotheses of oceanographic transportation potential lack testing with large scale empirical data. To address this gap, we used the seagrass species, Halodule wrightii, which is unique in spanning the entire tropical Atlantic. We tested the hypothesis that genetic differentiation estimated across its large-scale biogeographic range can be predicted by simulated oceanographic transport. The alternative hypothesis posits that dispersal is independent of ocean currents, such as transport by grazers. We compared empirical genetic estimates and modelled predictions of dispersal along the distribution of H. wrightii. We genotyped eight microsatellite loci on 19 populations distributed across Atlantic Africa, Gulf of Mexico, Caribbean, Brazil and developed a biophysical model with high-resolution ocean currents. Genetic data revealed low gene flow and highest differentiation between (1) the Gulf of Mexico and two other regions: (2) Caribbean-Brazil and (3) Atlantic Africa. These two were more genetically similar despite separation by an ocean. The biophysical model indicated low or no probability of passive dispersal among populations and did not match the empirical genetic data. The results support the alternative hypothesis of a role for active dispersal vectors like grazers.

Transcriptome wide analyses reveal intraspecific diversity in thermal stress responses of a dominant habitat-forming species.

The impact of climate change on biodiversity has stimulated the need to understand environmental stress responses, particularly for ecosystem engineers whose responses to climate affect large numbers of associated organisms. Distinct species differ substantially in their resilience to thermal stress but there are also within-species variations in thermal tolerance for which the molecular mechanisms underpinning such variation remain largely unclear. Intertidal mussels are well-known for their role as ecosystem engineers. First, we exposed two genetic lineages of the intertidal mussel Perna perna to heat stress treatments in air and water. Next, we ran a high throughput RNA sequencing experiment to identify differences in gene expression between the thermally resilient eastern lineage and the thermally sensitive western lineage. We highlight different thermal tolerances that concord with their distributional ranges. Critically, we also identified lineage-specific patterns of gene expression under heat stress and revealed intraspecific differences in the underlying transcriptional pathways in response to warmer temperatures that are potentially linked to the within-species differences in thermal tolerance. Beyond the species, we show how unravelling within-species variability in mechanistic responses to heat stress promotes a better understanding of global evolutionary trajectories of the species as a whole in response to changing climate.

Not out of the Mediterranean: Atlantic populations of the gorgonian Paramuricea clavata are a separate sister species under further lineage diversification.

The accurate delimitation of species boundaries in nonbilaterian marine taxa is notoriously difficult, with consequences for many studies in ecology and evolution. Anthozoans are a diverse group of key structural organisms worldwide, but the lack of reliable morphological characters and informative genetic markers hampers our ability to understand species diversification. We investigated population differentiation and species limits in Atlantic (Iberian Peninsula) and Mediterranean lineages of the octocoral genus Paramuricea previously identified as P. clavata. We used a diverse set of molecular markers (microsatellites, RNA-seq derived single-copy orthologues [SCO] and mt-mutS [mitochondrial barcode]) at 49 locations. Clear segregation of Atlantic and Mediterranean lineages was found with all markers. Species-tree estimations based on SCO strongly supported these two clades as distinct, recently diverged sister species with incomplete lineage sorting, P. cf. grayi and P. clavata, respectively. Furthermore, a second putative (or ongoing) speciation event was detected in the Atlantic between two P. cf. grayi color morphotypes (yellow and purple) using SCO and supported by microsatellites. While segregating P. cf. grayi lineages showed considerable geographic structure, dominating circalittoral communities in southern (yellow) and western (purple) Portugal, their occurrence in sympatry at some localities suggests a degree of reproductive isolation. Overall, our results show that previous molecular and morphological studies have underestimated species diversity in Paramuricea occurring in the Iberian Peninsula, which has important implications for conservation planning. Finally, our findings validate the usefulness of phylotranscriptomics for resolving evolutionary relationships in octocorals.

Complete mitochondrial genome of the branching octocoral Paramuricea grayi (Johnson, 1861), phylogenetic relationships and divergence analysis.

The Gray's sea fan, Paramuricea grayi (Johnson, 1861), typically inhabits deep littoral and circalittoral habitats of the eastern temperate and tropical Atlantic Ocean. Along the Iberian Peninsula, where P. grayi is a dominant constituent of circalittoral coral gardens, two segregating lineages (yellow and purple morphotypes) were recently identified using single-copy nuclear orthologues. The mitochondrial genomes of 9 P. grayi individuals covering both color morphotypes were assembled from RNA-seq data, using samples collected at three sites in southern (Sagres and Tavira) and western (Cape Espichel) Portugal. The complete circular mitogenome is 18,668 bp in length, has an A + T-rich base composition (62.5%) and contains the 17 genes typically found in Octocorallia: 14 protein-coding genes (atp6, atp8, cob, cox1-3, mt-mutS, nad1-6, and nad4L), the small and large subunit rRNAs (rns and rnl), and one transfer RNA (trnM). The mitogenomes were nearly identical for all specimens, though we identified a noteworthy polymorphism (two SNPs 9 bp apart) in the mt-mutS of one purple individual that is shared with the sister species P. clavata. The mitogenomes of the two species have a pairwise sequence identity of 99.0%, with nad6 and mt-mutS having the highest rates of non-synonymous substitutions.

A low-latitude species pump: Peripheral isolation, parapatric speciation and mating-system evolution converge in a marine radiation.

Geologically recent radiations can shed light on speciation processes, but incomplete lineage sorting and introgressive gene flow render accurate evolutionary reconstruction and interpretation challenging. Independently evolving metapopulations of low dispersal taxa may provide an additional level of phylogeographic information, given sufficiently broad sampling and genome-wide sequencing. Evolution in the marine brown algal genus Fucus in the south-eastern North Atlantic was shaped by Quaternary climate-driven range shifts. Over this timescale, divergence and speciation occurred against a background of expansion-contraction cycles from multiple refugia, together with mating-system shifts from outcrossing (dioecy) to selfing hermaphroditism. We tested the hypothesis that peripheral isolation of range edge (dioecious) F. vesiculosus led to parapatric speciation and radiation of hermaphrodite lineages. Species tree methods using 876 single-copy nuclear genes and extensive geographic coverage produced conflicting topologies with respect to geographic clades of F. vesiculosus. All methods, however, revealed a new and early diverging hermaphrodite species, Fucus macroguiryi sp. nov. Both the multispecies coalescent and polymorphism-aware models (in contrast to concatenation) support sequential paraphyly in F. vesiculosus resulting from distinct evolutionary processes. Our results support (1) peripheral isolation of the southern F. vesiculosus clade prior to parapatric speciation and radiation of hermaphrodite lineages-a "low-latitude species pump". (2) Directional introgressive gene flow into F. vesiculosus around the present-day secondary contact zone (sympatric-allopatric boundary) between dioecious/hermaphrodite lineages as hermaphrodites expanded northwards, supported by concordance analysis and statistical tests of introgression. (3) Species boundaries in the extensive sympatric range are probably maintained by reproductive system (selfing in hermaphrodites) and reinforcement.

Heat stress responses and population genetics of the kelp Laminaria digitata (Phaeophyceae) across latitudes reveal differentiation among North Atlantic populations.

To understand the thermal plasticity of a coastal foundation species across its latitudinal distribution, we assess physiological responses to high temperature stress in the kelp Laminaria digitata in combination with population genetic characteristics and relate heat resilience to genetic features and phylogeography. We hypothesize that populations from Arctic and cold-temperate locations are less heat resilient than populations from warm distributional edges. Using meristems of natural L. digitata populations from six locations ranging between Kongsfjorden, Spitsbergen (79°N), and Quiberon, France (47°N), we performed a common-garden heat stress experiment applying 15°C to 23°C over eight days. We assessed growth, photosynthetic quantum yield, carbon and nitrogen storage, and xanthophyll pigment contents as response traits. Population connectivity and genetic diversity were analyzed with microsatellite markers. Results from the heat stress experiment suggest that the upper temperature limit of L. digitata is nearly identical across its distribution range, but subtle differences in growth and stress responses were revealed for three populations from the species' ecological range margins. Two populations at the species' warm distribution limit showed higher temperature tolerance compared to other populations in growth at 19°C and recovery from 21°C (Quiberon, France), and photosynthetic quantum yield and xanthophyll pigment responses at 23°C (Helgoland, Germany). In L. digitata from the northernmost population (Spitsbergen, Norway), quantum yield indicated the highest heat sensitivity. Microsatellite genotyping revealed all sampled populations to be genetically distinct, with a strong hierarchical structure between southern and northern clades. Genetic diversity was lowest in the isolated population of the North Sea island of Helgoland and highest in Roscoff in the English Channel. All together, these results support the hypothesis of moderate local differentiation across L. digitata's European distribution, whereas effects are likely too weak to ameliorate the species' capacity to withstand ocean warming and marine heatwaves at the southern range edge.

Thermal traits for reproduction and recruitment differ between Arctic and Atlantic kelp Laminaria digitata.

The plasticity of different kelp populations to heat stress has seldom been investigated excluding environmental effects due to thermal histories, by raising a generation under common garden conditions. Comparisons of populations in the absence of environmental effects allow unbiased quantification of the meta-population adaptive potential and resolution of population-specific differentiation. Following this approach, we tested the hypothesis that genetically distinct arctic and temperate kelp exhibit different thermal phenotypes, by comparing the capacity of their microscopic life stages to recover from elevated temperatures. Gametophytes of Laminaria digitata (Arctic and North Sea) grown at 15°C for 3 years were subjected to common garden conditions with static or dynamic (i.e., gradual) thermal treatments ranging between 15 and 25°C and also to darkness. Gametophyte growth and survival during thermal stress conditions, and subsequent sporophyte recruitment at two recovery temperatures (5 and 15°C), were investigated. Population-specific responses were apparent; North Sea gametophytes exhibited higher growth rates and greater sporophyte recruitment than those from the Arctic when recovering from high temperatures, revealing differential thermal adaptation. All gametophytes performed poorly after recovery from a static 8-day exposure at 22.5°C compared to the response under a dynamic thermal treatment with a peak temperature of 25°C, demonstrating the importance of gradual warming and/or acclimation time in modifying thermal limits. Recovery temperature markedly affected the capacity of gametophytes to reproduce following high temperatures, regardless of the population. Recovery at 5°C resulted in higher sporophyte production following a 15°C and 20°C static exposure, whereas recovery at 15°C was better for gametophyte exposures to static 22.5°C or dynamic heat stress to 25°C. The subtle performance differences between populations originating from sites with contrasting local in situ temperatures support our hypothesis that their thermal plasticity has diverged over evolutionary time scales.

Sex-dependent and -independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissima.

In haplodiplontic lineages, sexual reproduction occurs in haploid parents without meiosis. Although widespread in multicellular lineages such as brown algae (Phaeophyceae), haplodiplontic gametogenesis has been little studied at the molecular level. We addressed this by generating an annotated reference transcriptome for the gametophytic phase of the sugar kelp, Saccharina latissima. Transcriptional profiles of microscopic male and female gametophytes were analysed at four time points during the transition from vegetative growth to gametogenesis. Gametogenic signals resulting from a switch in culture irradiance from red to white light activated a core set of genes in a sex-independent manner, involving rapid activation of ribosome biogenesis, transcription and translation related pathways, with several acting at the post-transcriptional or post-translational level. Additional genes regulating nutrient acquisition and key carbohydrate-energy pathways were also identified. Candidate sex-biased genes under gametogenic conditions had potentially key roles in controlling female- and male-specific gametogenesis. Among these were several sex-biased or -specific E3 ubiquitin-protein ligases that may have important regulatory roles. Females specifically expressed several genes that coordinate gene expression and/or protein degradation, and the synthesis of inositol-containing compounds. Other female-biased genes supported parallels with oogenesis in divergent multicellular lineages, in particular reactive oxygen signalling via an NADPH-oxidase. Males specifically expressed the hypothesised brown algal sex-determining factor. Male-biased expression mainly involved upregulation of genes that control mitotic cell proliferation and spermatogenesis in other systems, as well as multiple flagella-related genes. Our data and results enhance genome-level understanding of gametogenesis in this ecologically and economically important multicellular lineage.

Increased evolutionary rates and conserved transcriptional response following allopolyploidization in brown algae.

Genome mergers between independently evolving lineages, via allopolyploidy, can potentially lead to instantaneous sympatric speciation. However, little is known about the consequences of allopolyploidy and the resultant "genome shock" on genome evolution and expression beyond the plant and fungal branches of the Tree of Life. The aim of this study was to compare substitution rates and gene expression patterns in two allopolyploid brown algae (Phaeophyceae and Heterokonta) and their progenitors in the genus Pelvetiopsis N. L. Gardner in the north-east Pacific, and to date their relationships. We used RNA-seq data, all potential orthologues, and putative single-copy loci for phylogenomic, divergence, and gene expression analyses. The multispecies coalescent placed the origin of allopolyploids in the late Pleistocene (0.35-0.05 Ma). Homoeologues displayed increased nonsynonymous divergence compared with parental orthologues, consistent with relaxed selective constraint following allopolyploidization, including for genes with no evidence of pseudogenization or neofunctionalization. Patterns of homoeologue-orthologue expression conservation and expression level dominance were largely shared with both natural plant and fungal allopolyploids. Our results provide further support for common cross-Kingdom patterns of allopolyploid genome evolution and transcriptional responses, here in the evolutionarily distinct marine heterokont brown algae.

Differentiation in fitness-related traits in response to elevated temperatures between leading and trailing edge populations of marine macrophytes.

The nature of species distribution boundaries is a key subject in ecology and evolution. Edge populations are potentially more exposed to climate-related environmental pressures. Despite research efforts, little is known about variability in fitness-related traits in leading (i.e., colder, high latitude) versus trailing (i.e., warmer, low latitude) edge populations. We tested whether the resilience, i.e. the resistance and recovery, of key traits differs between a distributional cold (Greenland) and warm (Portugal) range edge population of two foundation marine macrophytes, the intertidal macroalga Fucus vesiculosus and the subtidal seagrass Zostera marina. The resistance and recovery of edge populations to elevated seawater temperatures was compared under common experimental conditions using photosynthetic efficiency and expression of heat shock proteins (HSP). Cold and warm edge populations differed in their response, but this was species specific. The warm edge population of F. vesiculosus showed higher thermal resistance and recovery whereas the cold leading edge was less tolerant. The opposite was observed in Z. marina, with reduced recovery at the warm edge, while the cold edge was not markedly affected by warming. Our results confirm that differentiation of thermal stress responses can occur between leading and trailing edges, but such responses depend on local population traits and are thus not predictable just based on thermal pressures.

Marine forests of the Mediterranean-Atlantic Cystoseira tamariscifolia complex show a southern Iberian genetic hotspot and no reproductive isolation in parapatry.

Climate-driven range-shifts create evolutionary opportunities for allopatric divergence and subsequent contact, leading to genetic structuration and hybrid zones. We investigate how these processes influenced the evolution of a complex of three closely related Cystoseira spp., which are a key component of the Mediterranean-Atlantic seaweed forests that are undergoing population declines. The C. tamariscifolia complex, composed of C. tamariscifolia s.s., C. amentacea and C. mediterranea, have indistinct boundaries and natural hybridization is suspected. Our aims are to (1) infer the genetic structure and diversity of these species throughout their distribution ranges using microsatellite markers to identify ancient versus recent geographical populations, contact zones and reproductive barriers, and (2) hindcast past distributions using niche models to investigate the influence of past range shifts on genetic divergence at multiple spatial scales. Results supported a single, morphologically plastic species the genetic structure of which was incongruent with a priori species assignments. The low diversity and low singularity in northern European populations suggest recent colonization after the LGM. The southern Iberian genetic hotspot most likely results from the role of this area as a climatic refugium or a secondary contact zone between differentiated populations or both. We hypothesize that life-history traits (selfing, low dispersal) and prior colonization effects, rather than reproductive barriers, might explain the observed genetic discontinuities.

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

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.

Mitochondrial genomes of the key zooplankton copepods Arctic Calanus glacialis and North Atlantic Calanus finmarchicus with the longest crustacean non-coding regions.

We determined the nearly complete mitochondrial genomes of the Arctic Calanus glacialis and its North Atlantic sibling Calanus finmarchicus, which are key zooplankton components in marine ecosystems. The sequenced part of C. glacialis mitogenome is 27,342 bp long and consists of two contigs, while for C. finmarchicus it is 29,462 bp and six contigs, what makes them the longest reported copepod mitogenomes. The typical set of metazoan mitochondrial genes is present in these mitogenomes, although the non-coding regions (NCRs) are unusually long and complex. The mitogenomes of the closest species C. glacialis and C. finmarchicus, followed by the North Pacific C. sinicus, are structurally similar and differ from the much more typical of deep-water, Arctic C. hyperboreus. This evolutionary trend for the expansion of NCRs within the Calanus mitogenomes increases mitochondrial DNA density, what resulted in its similar density to the nuclear genome. Given large differences in the length and structure of C. glacialis and C. finmarchicus mitogenomes, we conclude that the species are genetically distinct and thus cannot hybridize. The molecular resources presented here: the mitogenomic and rDNA sequences, and the database of repetitive elements should facilitate the development of genetic markers suitable in pursuing evolutionary research in copepods.

Cryptic diversity, geographical endemism and allopolyploidy in NE Pacific seaweeds.

BACKGROUND: Molecular markers are revealing a much more diverse and evolutionarily complex picture of marine biodiversity than previously anticipated. Cryptic and/or endemic marine species are continually being found throughout the world oceans, predominantly in inconspicuous tropical groups but also in larger, canopy-forming taxa from well studied temperate regions. Interspecific hybridization has also been found to be prevalent in many marine groups, for instance within dense congeneric assemblages, with introgressive gene-flow being the most common outcome. Here, using a congeneric phylogeographic approach, we investigated two monotypic and geographically complementary sister genera of north-east Pacific intertidal seaweeds (Hesperophycus and Pelvetiopsis), for which preliminary molecular tests revealed unexpected conflicts consistent with unrecognized cryptic diversity and hybridization. RESULTS: The three recovered mtDNA clades did not match a priori species delimitations. H. californicus was congruent, whereas widespread P. limitata encompassed two additional narrow-endemic species from California - P. arborescens (here genetically confirmed) and P. hybrida sp. nov. The congruence between the genotypic clusters and the mtDNA clades was absolute. Fixed heterozygosity was apparent in a high proportion of loci in P. limitata and P. hybrida, with genetic analyses showing that the latter was composed of both H. californicus and P. arborescens genomes. All four inferred species could be distinguished based on their general morphology. CONCLUSIONS: This study confirmed additional diversity and reticulation within NE Pacific Hesperophycus/Pelvetiopsis, including the validity of the much endangered, modern climatic relict P. arborescens, and the identification of a new, stable allopolyploid species (P. hybrida) with clearly discernable ancestry (♀ H. californicus x ♂ P. arborescens), morphology, and geographical distribution. Allopolyploid speciation is otherwise completely unknown in brown seaweeds, and its unique occurrence within this genus (P. limitata possibly representing a second example) remains enigmatic. The taxonomic separation of Hesperophycus and Pelvetiopsis is not supported and the genera should be synonymized; we retain only the latter. The transitional coastline between Point Conception and Monterey Bay represented a diversity hotspot for the genus and the likely sites of extraordinary evolutionary events of allopolyploid speciation at sympatric range contact zones. This study pinpoints how much diversity (and evolutionary processes) potentially remains undiscovered even on a conspicuous seaweed genus from the well-studied Californian intertidal shores let alone in other, less studied marine groups and regions/depths.

Temporal windows of reproductive opportunity reinforce species barriers in a marine broadcast spawning assemblage.

Prezygotic isolating mechanisms act to limit hybridization and maintain the genetic identity of closely-related species. While synchronous intraspecific spawning is a common phenomenon amongst marine organisms and plays an important role in reproductive success, asynchronous spawning between potentially hybridizing lineages may also be important in maintaining species boundaries. We tested this hypothesis by comparing reproductive synchrony over daily to hourly timescales in a sympatric assemblage of intertidal fucoid algae containing selfing hermaphroditic (Fucus spiralis and Fucus guiryi) and dioecious (Fucus vesiculosus and Fucus serratus) species. Our results confirm that gametes are released on semi-lunar cycles in all species. However, sister species with different mating systems showed asynchronous spawning at finer circadian timescales, thus providing evidence for a partial reproductive barrier between hermaphroditic and dioecious species. Finally, our data also emphasize the ecological, developmental, and/or physiological constraints that operate to restrict reproduction to narrow temporal windows of opportunity in the intertidal zone and more generally the role of ecological factors in marine speciation.

The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea.

Seagrasses colonized the sea on at least three independent occasions to form the basis of one of the most productive and widespread coastal ecosystems on the planet. Here we report the genome of Zostera marina (L.), the first, to our knowledge, marine angiosperm to be fully sequenced. This reveals unique insights into the genomic losses and gains involved in achieving the structural and physiological adaptations required for its marine lifestyle, arguably the most severe habitat shift ever accomplished by flowering plants. Key angiosperm innovations that were lost include the entire repertoire of stomatal genes, genes involved in the synthesis of terpenoids and ethylene signalling, and genes for ultraviolet protection and phytochromes for far-red sensing. Seagrasses have also regained functions enabling them to adjust to full salinity. Their cell walls contain all of the polysaccharides typical of land plants, but also contain polyanionic, low-methylated pectins and sulfated galactans, a feature shared with the cell walls of all macroalgae and that is important for ion homoeostasis, nutrient uptake and O2/CO2 exchange through leaf epidermal cells. The Z. marina genome resource will markedly advance a wide range of functional ecological studies from adaptation of marine ecosystems under climate warming, to unravelling the mechanisms of osmoregulation under high salinities that may further inform our understanding of the evolution of salt tolerance in crop plants.

Reproductive investment, synchrony and recruitment success in marine broadcast spawners: Effects of mating system and habitat (exposed shore versus estuary).

The timing and synchrony of gamete release in broadcast spawners have important implications for fertilization success, recruitment and to explain differences in reproductive success under distinct reproductive modes in sympatry. Our objective was to compare the reproductive timing and investment for sister species with contrasting mating systems; Fucus guiryi (selfing hermaphroditic) and Fucus vesiculosus (dioecious) in habitats with different wave exposures (exposed shore and estuary). Over two months, daily gamete release, recruitment and population structure were recorded. Our results show spawning synchrony between species and habitats, but release events in hermaphrodites occupied broader temporal windows in estuarine than exposed shore habitats. On the exposed shore both species increased the synchrony of release and amount of eggs. In the estuary, hermaphrodites relied on broader temporal spawning windows and a larger canopy, and the dioecious species had higher recruitment success, important factors determining persistence.