Evolutionary dynamics of sex-biased gene expression in a young XY system: insights from the brown alga genus Fucus.

Sex-biased gene expression is considered to be an underlying cause of sexually dimorphic traits. Although the nature and degree of sex-biased expression have been well documented in several animal and plant systems, far less is known about the evolution of sex-biased genes in more distant eukaryotic groups. Here, we investigate sex-biased gene expression in two brown algal dioecious species, Fucus serratus and Fucus vesiculosus, where male heterogamety (XX/XY) has recently emerged. We find that in contrast to evolutionary distant plant and animal lineages, male-biased genes do not experience high turnover rates, but instead reveal remarkable conservation of bias and expression levels between the two species, suggesting their importance in sexual differentiation. Genes with consistent male bias were enriched in functions related to gamete production, along with sperm competition and include three flagellar proteins under positive selection. We present one of the first reports, outside of the animal kingdom, showing that male-biased genes display accelerated rates of coding sequence evolution compared with female-biased or unbiased genes. Our results imply that evolutionary forces affect male and female sex-biased genes differently on structural and regulatory levels, resulting in unique properties of differentially expressed transcripts during reproductive development in Fucus algae.

The Seagrass Methylome Is Associated With Variation in Photosynthetic Performance Among Clonal Shoots.

Evolutionary theory predicts that clonal organisms are more susceptible to extinction than sexually reproducing organisms, due to low genetic variation and slow rates of evolution. In agreement, conservation management considers genetic variation as the ultimate measure of a population's ability to survive over time. However, clonal plants are among the oldest living organisms on our planet. Here, we test the hypothesis that clonal seagrass meadows display epigenetic variation that complements genetic variation as a source of phenotypic variation. In a clonal meadow of the seagrass Zostera marina, we characterized DNA methylation among 42 shoots. We also sequenced the whole genome of 10 shoots to correlate methylation patterns with photosynthetic performance under exposure to and recovery from 27°C, while controlling for somatic mutations. Here, we show for the first time that clonal seagrass shoots display DNA methylation variation that is independent from underlying genetic variation, and associated with variation in photosynthetic performance under experimental conditions. It remains unknown to what degree this association could be influenced by epigenetic responses to transplantation-related stress, given that the methylomes showed a strong shift under acclimation to laboratory conditions. The lack of untreated control samples in the heat stress experiment did not allow us to distinguish methylome shifts induced by acclimation from such induced by heat stress. Notwithstanding, the co-variation in DNA methylation and photosynthetic performance may be linked via gene expression because methylation patterns varied in functionally relevant genes involved in photosynthesis, and in the repair and prevention of heat-induced protein damage. While genotypic diversity has been shown to enhance stress resilience in seagrass meadows, we suggest that epigenetic variation plays a similar role in meadows dominated by a single genotype. Consequently, conservation management of clonal plants should consider epigenetic variation as indicator of resilience and stability.

Decadal stability in genetic variation and structure in the intertidal seaweed Fucus serratus (Heterokontophyta: Fucaceae).

BACKGROUND: The spatial distribution of genetic diversity and structure has important implications for conservation as it reveals a species' strong and weak points with regard to stability and evolutionary capacity. Temporal genetic stability is rarely tested in marine species other than commercially important fishes, but is crucial for the utility of temporal snapshots in conservation management. High and stable diversity can help to mitigate the predicted northward range shift of seaweeds under the impact of climate change. Given the key ecological role of fucoid seaweeds along rocky shores, the positive effect of genetic diversity may reach beyond the species level to stabilize the entire intertidal ecosystem along the temperate North Atlantic. In this study, we estimated the effective population size, as well as temporal changes in genetic structure and diversity of the seaweed F. serratus using 22 microsatellite markers. Samples were taken across latitudes and a range of temperature regimes at seven locations with decadal sampling (2000 and 2010). RESULTS: Across latitudes, genetic structure and diversity remained stable over 5-10 generations. Stable small-scale structure enhanced regional diversity throughout the species' range. In accordance with its biogeographic history, effective population size and diversity peaked in the species' mid-range in Brittany (France), and declined towards its leading and trailing edge to the north and south. At the species' southern edge, multi-locus-heterozygosity displayed a strong decline from 1999 to 2010. CONCLUSION: Temporally stable genetic structure over small spatial scales is a potential driver for local adaptation and species radiation in the genus Fucus. Survival and adaptation of the low-diversity leading edge of F. serratus may be enhanced by regional gene flow and 'surfing' of favorable mutations or impaired by the accumulation of deleterious mutations. Our results have clear implications for the conservation of F. serratus at its genetically unique southern edge in Northwest Iberia, where increasing temperatures are likely the major cause for the decline not only of F. serratus, but also other intertidal and subtidal macroalgae. We expect that F. serratus will disappear from Northwest Iberia by 2100 if genetic rescue is not induced by the influx of genetic variation from Brittany.

The fate of the Arctic seaweed Fucus distichus under climate change: an ecological niche modeling approach.

Rising temperatures are predicted to melt all perennial ice cover in the Arctic by the end of this century, thus opening up suitable habitat for temperate and subarctic species. Canopy-forming seaweeds provide an ideal system to predict the potential impact of climate-change on rocky-shore ecosystems, given their direct dependence on temperature and their key role in the ecological system. Our primary objective was to predict the climate-change induced range-shift of Fucus distichus, the dominant canopy-forming macroalga in the Arctic and subarctic rocky intertidal. More specifically, we asked: which Arctic/subarctic and cold-temperate shores of the northern hemisphere will display the greatest distributional change of F. distichus and how will this affect niche overlap with seaweeds from temperate regions? We used the program MAXENT to develop correlative ecological niche models with dominant range-limiting factors and 169 occurrence records. Using three climate-change scenarios, we projected habitat suitability of F. distichus - and its niche overlap with three dominant temperate macroalgae - until year 2200. Maximum sea surface temperature was identified as the most important factor in limiting the fundamental niche of F. distichus. Rising temperatures were predicted to have low impact on the species' southern distribution limits, but to shift its northern distribution limits poleward into the high Arctic. In cold-temperate to subarctic regions, new areas of niche overlap were predicted between F. distichus and intertidal macroalgae immigrating from the south. While climate-change threatens intertidal seaweeds in warm-temperate regions, seaweed meadows will likely flourish in the Arctic intertidal. Although this enriches biodiversity and opens up new seaweed-harvesting grounds, it will also trigger unpredictable changes in the structure and functioning of the Arctic intertidal ecosystem.

Variation in thermal stress response in two populations of the brown seaweed, Fucus distichus, from the Arctic and subarctic intertidal.

It is unclear whether intertidal organisms are 'preadapted' to cope with the increase of temperature and temperature variability or if they are currently at their thermal tolerance limits. To address the dichotomy, we focused on an important ecosystem engineer of the Arctic intertidal rocky shores, the seaweed Fucus distichus and investigated thermal stress responses of two populations from different temperature regimes (Svalbard and Kirkenes, Norway). Thermal stress responses at 20°C, 24°C and 28°C were assessed by measuring photosynthetic performance and expression of heat shock protein (HSP) genes (shsp, hsp90 and hsp70). We detected population-specific responses between the two populations of F. distichus, as the Svalbard population revealed a smaller decrease in photosynthesis performance but a greater activation of molecular defence mechanisms (indicated by a wider repertoire of HSP genes and their stronger upregulation) compared with the Kirkenes population. Although the temperatures used in our study exceed temperatures encountered by F. distichus at the study sites, we believe response to these temperatures may serve as a proxy for the species' potential to respond to climate-related stresses.

Seascape drivers of Macrocystis pyrifera population genetic structure in the northeast Pacific.

At small spatial and temporal scales, genetic differentiation is largely controlled by constraints on gene flow, while genetic diversity across a species' distribution is shaped on longer temporal and spatial scales. We assess the hypothesis that oceanographic transport and other seascape features explain different scales of genetic structure of giant kelp, Macrocystis pyrifera. We followed a hierarchical approach to perform a microsatellite-based analysis of genetic differentiation in Macrocystis across its distribution in the northeast Pacific. We used seascape genetic approaches to identify large-scale biogeographic population clusters and investigate whether they could be explained by oceanographic transport and other environmental drivers. We then modelled population genetic differentiation within clusters as a function of oceanographic transport and other environmental factors. Five geographic clusters were identified: Alaska/Canada, central California, continental Santa Barbara, California Channel Islands and mainland southern California/Baja California peninsula. The strongest break occurred between central and southern California, with mainland Santa Barbara sites forming a transition zone between the two. Breaks between clusters corresponded approximately to previously identified biogeographic breaks, but were not solely explained by oceanographic transport. An isolation-by-environment (IBE) pattern was observed where the northern and southern Channel Islands clustered together, but not with closer mainland sites, despite the greater distance between them. The strongest environmental association with this IBE pattern was observed with light extinction coefficient, which extends suitable habitat to deeper areas. Within clusters, we found support for previous results showing that oceanographic connectivity plays an important role in the population genetic structure of Macrocystis in the Northern hemisphere.

Biodiversity mediates top-down control in eelgrass ecosystems: a global comparative-experimental approach.

Nutrient pollution and reduced grazing each can stimulate algal blooms as shown by numerous experiments. But because experiments rarely incorporate natural variation in environmental factors and biodiversity, conditions determining the relative strength of bottom-up and top-down forcing remain unresolved. We factorially added nutrients and reduced grazing at 15 sites across the range of the marine foundation species eelgrass (Zostera marina) to quantify how top-down and bottom-up control interact with natural gradients in biodiversity and environmental forcing. Experiments confirmed modest top-down control of algae, whereas fertilisation had no general effect. Unexpectedly, grazer and algal biomass were better predicted by cross-site variation in grazer and eelgrass diversity than by global environmental gradients. Moreover, these large-scale patterns corresponded strikingly with prior small-scale experiments. Our results link global and local evidence that biodiversity and top-down control strongly influence functioning of threatened seagrass ecosystems, and suggest that biodiversity is comparably important to global change stressors.

Genome-wide transcriptomic responses of the seagrasses Zostera marina and Nanozostera noltii under a simulated heatwave confirm functional types.

Genome-wide transcription analysis between related species occurring in overlapping ranges can provide insights into the molecular basis underlying different ecological niches. The co-occurring seagrass species, Zostera marina and Nanozostera noltii, are found in marine coastal environments throughout the northern hemisphere. Z. marina is often dominant in subtidal environments and subjected to fewer temperature extremes compared to the predominately intertidal and more stress-tolerant N. noltii. We exposed plants of both species to a realistic heat wave scenario in a common-stress-garden experiment. Using RNA-seq (~7million reads/library), four Z. marina and four N. noltii libraries were compared representing northern (Denmark) and southern (Italy) locations within the co-occurring range of the species' European distribution. A total of 8977 expressed genes were identified, of which 78 were directly related to heat stress. As predicted, both species were negatively affected by the heat wave, but showed markedly different molecular responses. In Z. marina the heat response was similar across locations in response to the heatwave at 26°C, with a complex response in functions related to protein folding, synthesis of ribosomal chloroplast proteins, proteins involved in cell wall modification and heat shock proteins (HSPs). In N. noltii the heat response markedly differed between locations, while HSP genes were not induced in either population. Our results suggest that as coastal seawater temperatures increase, Z. marina will disappear along its southern most ranges, whereas N. noltii will continue to move north. As a consequence, sub- and intertidal habitat partitioning may weaken in more northern regions because the higher thermal tolerance of N. noltii provides a competitive advantage in both habitats. Although previous studies have focused on HSPs, the present study clearly demonstrates that a broader examination of stress related genes is necessary.

Thermal stress resistance of the brown alga Fucus serratus along the North-Atlantic coast: acclimatization potential to climate change.

Seaweed-dominated communities are predicted to disappear south of 45° latitude on North-Atlantic rocky shores by 2200 because of climate change. The extent of predicted habitat loss, however, could be mitigated if the seaweeds' physiology is sufficiently plastic to rapidly acclimatize to the warmer temperatures. The main objectives of this study were to identify whether the thermal tolerance of the canopy-forming seaweed Fucus serratus is population-specific and where temperatures are likely to exceed its tolerance limits in the next 200 years. We measured the stress response of seaweed samples from four populations (Norway, Denmark, Brittany and Spain) to common-garden heat stress (20 °C-36 °C) in both photosynthetic performance and transcriptomic upregulation of heat shock protein genes. The two stress indicators did not correlate and likely measured different cellular components of the stress response, but both indicators revealed population-specific differences, suggesting ecotypic differentiation. Our results confirmed that thermal extremes will regularly reach physiologically stressful levels in Brittany (France) and further south by the end of the 22nd century. Although heat stress resilience in photosynthetic performance was higher at the species' southern distributional edge in Spain, the hsp expression pattern suggested that this edge-population experienced reduced fitness and limited responsiveness to further stressors. Thus, F. serratus may be unable to mitigate its predicted northward shift and may be at high risk to lose its center of genetic diversity and adaptability in Brittany (France). As it is an important intertidal key species, the disappearance of this seaweed will likely trigger major ecological changes in the entire associated ecosystem.

Climate change impact on seaweed meadow distribution in the North Atlantic rocky intertidal.

The North-Atlantic has warmed faster than all other ocean basins and climate change scenarios predict sea surface temperature isotherms to shift up to 600 km northwards by the end of the 21st century. The pole-ward shift has already begun for many temperate seaweed species that are important intertidal foundation species. We asked the question: Where will climate change have the greatest impact on three foundational, macroalgal species that occur along North-Atlantic shores: Fucus serratus, Fucus vesiculosus, and Ascophyllum nodosum? To predict distributional changes of these key species under three IPCC (Intergovernmental Panel on Climate Change) climate change scenarios (A2, A1B, and B1) over the coming two centuries, we generated Ecological Niche Models with the program MAXENT. Model predictions suggest that these three species will shift northwards as an assemblage or "unit" and that phytogeographic changes will be most pronounced in the southern Arctic and the southern temperate provinces. Our models predict that Arctic shores in Canada, Greenland, and Spitsbergen will become suitable for all three species by 2100. Shores south of 45° North will become unsuitable for at least two of the three focal species on both the Northwest- and Northeast-Atlantic coasts by 2200. If these foundational species are unable to adapt to the rising temperatures, they will lose their centers of genetic diversity and their loss will trigger an unpredictable shift in the North-Atlantic intertidal ecosystem.

Stress ecology in fucus: abiotic, biotic and genetic interactions.

Stress regimes defined as the synchronous or sequential action of abiotic and biotic stresses determine the performance and distribution of species. The natural patterns of stress to which species are more or less well adapted have recently started to shift and alter under the influence of global change. This was the motivation to review our knowledge on the stress ecology of a benthic key player, the macroalgal genus Fucus. We first provide a comprehensive review of the genus as an ecological model including what is currently known about the major lineages of Fucus species with respect to hybridization, ecotypic differentiation and speciation; as well as life history, population structure and geographic distribution. We then review our current understanding of both extrinsic (abiotic/biotic) and intrinsic (genetic) stress(es) on Fucus species and how they interact with each other. It is concluded that (i) interactive stress effects appear to be equally distributed over additive, antagonistic and synergistic categories at the level of single experiments, but are predominantly additive when averaged over all studies in a meta-analysis of 41 experiments; (ii) juvenile and adult responses to stress frequently differ and (iii) several species or particular populations of Fucus may be relatively unaffected by climate change as a consequence of pre-adapted ecotypes that collectively express wide physiological tolerences. Future research on Fucus should (i) include additional species, (ii) include marginal populations as models for responses to environmental stress; (iii) assess a wider range of stress combinations, including their temporal fluctuations; (iv) better differentiate between stress sensitivity of juvenile versus adult stages; (v) include a functional genomic component in order to better integrate Fucus' ecological and evolutionary responses to stress regimes and (vi) utilize a multivariate modelling approach in order to develop and understand interaction networks.

An evaluation of small-scale genetic diversity and the mating system in Zostera noltii on an intertidal sandflat in the Wadden Sea.

BACKGROUND AND AIMS: The dwarf eelgrass, Zostera noltii, is a predominant inhabitant of soft-bottom intertidal regions along the coasts of northern Europe. It is a monoecious, protogynous angiosperm in which the potential for self-fertilization and inbreeding are high, especially if clone sizes exceed pollen dispersal distances. The aim of the present study was to determine the relationship between mating system and clonal structure, examine the relative roles of geitonogamous selfing and biparental inbreeding, measure pollen availability (multiple paternities) and estimate pollen dispersal. METHODS: A 100-m(2) plot was established in a large, intertidal Z. noltii meadow on the island of Sylt in the German Wadden Sea. A total of 256 adult shoots was sampled: one from the centre of 100 fixed 1-m(2) quadrats (large scale resolution) and an additional 156 from within eight randomly selected 1-m(2) sub-quadrats (small-scale resolution). DNA was extracted from seeds and leaf tissue of all samples and genotyped with nine microsatellite loci. KEY RESULTS: Mating system analysis revealed high multilocus and single locus outcrossing rates. Average pollen dispersal distance was nearly the same as the average genet (clone) size. Multiple paternity was common and 20-30 % of mature seeds originated from matings within the plot. Among inbred seeds, most resulted from geitonogamy rather than biparental inbreeding. CONCLUSIONS: Moderate disturbances intrinsic to the intertidal habitat appear to facilitate seed recruitment by gap formation. Pollen dispersal distances are sufficient to maintain outcrossing and high clonal diversity.

An expressed sequence tag analysis of the intertidal brown seaweeds Fucus serratus (L.) and F. vesiculosus (L.) (Heterokontophyta, Phaeophyceae) in response to abiotic stressors.

In order to aid gene discovery and uncover genes responding to abiotic stressors in stress-tolerant brown algae of the genus Fucus, expressed sequence tags (ESTs) were studied in two species, Fucus serratus and Fucus vesiculosus. Clustering of over 12,000 ESTs from three libraries for heat shock/recovery and desiccation/rehydration resulted in identification of 2,503, 1,290, and 2,409 unigenes from heat-shocked F. serratus, desiccated F. serratus, and desiccated F. vesiculosus, respectively. Low overall annotation rates (18-31%) were strongly associated with the presence of long 3' untranslated regions in Fucus transcripts, as shown by analyses of predicted protein-coding sequence in annotated and nonannotated tentative consensus sequences. Posttranslational modification genes were overrepresented in the heat shock/recovery library, including many chaperones, the most abundant of which were a family of small heat shock protein transcripts, Hsp90 and Hsp70 members. Transcripts of LI818-like light-harvesting genes implicated in photoprotection were also expressed during heat shock in high light. The expression of several heat-shock-responsive genes was confirmed by quantitative reverse transcription polymerase chain reaction. However, candidate genes were notably absent from both desiccation/rehydration libraries, while the responses of the two species to desiccation were divergent, perhaps reflecting the species-specific physiological differences in stress tolerance previously established. Desiccation-tolerant F. vesiculosus overexpressed at least 17 ribosomal protein genes and two ubiquitin-ribosomal protein fusion genes, suggesting that ribosome function and/or biogenesis are important during cycles of rapid desiccation and rehydration in the intertidal zone and possibly indicate parallels with other poikilohydric organisms such as desiccation-tolerant bryophytes.

Historical invasions of the intertidal zone of Atlantic North America associated with distinctive patterns of trade and emigration.

Early invasions of the North American shore occurred mainly via deposition of ballast rock, which effectively transported pieces of the intertidal zone across the Atlantic. From 1773-1861, >880 European ships entered Pictou Harbor, Nova Scotia, as a result of emigration and trade from Europe. The rockweed Fucus serratus (1868) and the snail Littorina littorea ( approximately 1840) were found in Pictou during this same period. With shipping records (a proxy for propagule pressure) to guide sampling, we used F. serratus as a model to examine the introductions because of its relatively low genetic diversity and dispersal capability. Microsatellite markers and assignment tests revealed 2 introductions of the rockweed into Nova Scotia: 1 from Galway (Ireland) to Pictou and the other from Greenock (Scotland) to western Cape Breton Island. To examine whether a high-diversity, high-dispersing species might have similar pathways of introduction, we analyzed L. littorea, using cytochrome b haplotypes. Eight of the 9 Pictou haplotypes were found in snails collected from Ireland and Scotland. Our results contribute to a broader understanding of marine communities, because these 2 conspicuous species are likely to be the tip of an "invasion iceberg" to the NW Atlantic from Great Britain and Ireland in the 19th Century.

Clonal architecture in an intertidal bed of the dwarf eelgrass Zostera noltii in the Northern Wadden Sea: persistence through extreme physical perturbation and the importance of a seed bank.

Genotypic structure and temporal dynamics of the dwarf seagrass, Zostera noltii, were studied in an intertidal meadow that has persisted since prior to 1936 near the Wadden Sea island of Sylt. Samples were collected from two 10 × 10 m plots separated by 250 m from May 2002 to June 2005 and from four 1 × 1 m plots from June 2003 to September 2004. All the samples were genotyped with nine microsatellite loci. No genotypes were shared between the plots separated by 250 m. Genetic diversity was higher in the Wadden Sea than in the other regions of its geographic range. The average clone size (genets) (SD) in the two plots was 1.38 (0.26) and 1.46 (0.4) m², respectively, with a range up to 9 m² and <20% persisted for >4 years. A high genetic and genotypic diversity was maintained by annual recruitment of seedlings despite a dramatic decrease in ramet density that coincided with the severe heat stress event of 2003. Fine-scale (1 m²) analysis suggested that extensive loss of seagrass cover precluded space competition among the genets, while a persistent seed bank prevented local extinction. Long-term persistence of Z. noltii meadows in the intertidal Wadden Sea was achieved by high genet turnover and frequent seedling recruitment from a seed bank, in contrast to the low diversity observed in large and long-living clones of Z. noltii and other seagrasses in subtidal habitats.

PATERNAL LEAKAGE OF MITOCHONDRIAL DNA IN A FUCUS (PHAEOPHYCEAE) HYBRID ZONE(1).

Eukaryotic mitochondria are mostly uniparentally (maternally) inherited, although mtDNA heteroplasmy has been reported in all major lineages. Heteroplasmy, the presence of more than one mitochondrial genome in an individual, can arise from recombination, point mutations, or by occasional transmission of the paternal mtDNA (=paternal leakage). Here, we report the first evidence of mtDNA paternal leakage in brown algae. In Denmark, where Fucus serratus L. and Fucus evanescens C. Agardh have hybridized for years, we found eight introgressed individuals that possessed the very distinct haplotypes of each parental species. The finding of heteroplasmy in individuals resulting from several generations of backcrosses suggests that paternal leakage occurred in earlier generations and has persisted through several meiotic bottlenecks.

Isolation and characterization of 11 microsatellite primers for a temperate reef fish, the California sheephead (Semicossyphus pulcher).

Eleven microsatellites were characterized for Semicossyphus pulcher (California sheephead) using an enrichment protocol. The number of alleles varied from three to 14 for a sample of 40 individuals from two populations. Expected heterozygosities ranged from 0.311 to 0.891. All loci but one were in Hardy-Weinberg equilibrium. No evidence for linkage disequilibrium was observed. These polymorphic microsatellites will be useful for genetic diversity and connectivity analyses of S. pulcher.

Being abundant is not enough: a decrease in effective population size over eight generations in a Norwegian population of the seaweed, Fucus serratus.

The brown alga Fucus serratus is a key foundation species on rocky intertidal shores of northern Europe. We sampled the same population off the coast of southern Norway in 2000 and 2008, and using 26 microsatellite loci, we estimated the changes in genetic diversity and effective population size (Ne). The unexpectedly low Ne (73-386) and Ne/N ratio (10-3-10-4), in combination with a significant decrease (14%) in allelic richness over the 8-year period, suggests an increased local extinction risk. If small Ne proves to be a common feature of F. serratus, then being abundant may not be enough for the species to weather future environmental changes.

Convergent adaptation to a marginal habitat by homoploid hybrids and polyploid ecads in the seaweed genus Fucus.

Hybridization and polyploidy are two major sources of genetic variability that can lead to adaptation in new habitats. Most species of the brown algal genus Fucus are found along wave-swept rocky shores of the Northern Hemisphere, but some species have adapted to brackish and salt marsh habitats. Using five microsatellite loci and mtDNA RFLP, we characterize two populations of morphologically similar, muscoides-like Fucus inhabiting salt marshes in Iceland and Ireland. The Icelandic genotypes were consistent with Fucus vesiculosus x Fucus spiralis F1 hybrids with asymmetrical hybridization, whereas the Irish ones consisted primarily of polyploid F. vesiculosus.

A mtDNA-based phylogeny of the brown algal genus Fucus (Heterokontophyta; Phaeophyta).

Species of Fucus are among the dominant seaweeds along Northern Hemisphere shores, but taxonomic designations often are confounded by significant intraspecific morphological variability. We analyzed intra- and inter-specific phylogenetic relationships within the genus (275 individuals representing 16 taxa) using two regions of the mitochondrion: a variable intergenic spacer and a conserved portion of the 23S subunit. Bayesian ML and MP analyses verified a shallow phylogeny with two major lineages (previously reported) and resolved some intra-lineage relationships. Significant species-level paraphyly/polyphyly was observed within lineages 1A and 2. Despite higher species richness in the North Atlantic, a North Pacific origin of the genus is supported by a gradient of decreasing haplotype and nucleotide diversities in F. distichus from the North Pacific to the East Atlantic.