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- Genetic diversity of Saccharina latissima (Phaeophyceae) along a salinity gradient in the North Sea-Baltic Sea transition zonePublication . Nielsen, Mette Moller; Paulino, Cristina; Neiva, J.; Krause-Jensen, Dorte; Bruhn, Annette; Serrão, EsterThe North Sea-Baltic Sea transition zone constitutes a boundary area for the kelp species Saccharina latissima due to a strong salinity gradient operating in the area. Furthermore, the existence of S.latissima there, along Danish waters, is fairly patchy as hard bottom is scarce. In this study, patterns of genetic diversity of S.latissima populations were evaluated along the salinity gradient area of Danish waters (here designated brackish) and were compared to reference sites (here designated marine) outside the gradient area, using microsatellite markers. The results showed that the S.latissima populations were structured into two clusters corresponding to brackish versus marine sites, and that gene flow was reduced both between clusters and between populations within clusters. In addition, results provided empirical evidence that marginal populations of S.latissima in the salinity gradient area exhibited a distinct genetic structure when compared to marine ones. Brackish populations were less diverse, more related, and showed increased differentiation over distance compared to marine populations. The isolation of the brackish S.latissima populations within the salinity gradient area of Danish waters in conjunction with their general low genetic diversity makes these populations vulnerable to ongoing environmental and climate change, predicted to result in declining salinity in the Baltic Sea area that may alter the future distribution and performance of S.latissima in the area.
- Genetic structure of amphi-Atlantic Laminaria digitata (Laminariales, Phaeophyceae) reveals a unique range-edge gene pool and suggests post-glacial colonization of the NW AtlanticPublication . Neiva, J.; Serrao, Ester; Paulino, Cristina; Gouveia, Licínia; Want, Andrew; Tamigneaux, Éric; Ballenghien, Marion; Mauger, Stéphane; Fouqueau, Louise; Engel-Gautier, Carolyn; Destombe, Christophe; Valero, MyriamIn the North-east (NE) Atlantic, most intertidal fucoids and warm-temperate kelps show unique low-latitude gene pools matching long-term climatic refugia. For cold-temperate kelps data are scarcer despite their unique cultural, ecological and economic significance. Here we test whether the amphi-Atlantic range of Laminaria digitata is derived from past glacial survival (and vicariance) in both NE and North-west (NW) Atlantic refugia (as suggested by niche modelling), or post-glacial (re)colonization (as suggested by low mtDNA divergence). We screened 14 populations from across the species range for 12 microsatellite loci to identify and map major gene pools and refugia. We assessed if NW Atlantic survival was supported by unique endemic variation, and if genetic diversity and structure were, as predicted from larger hindcasted glacial ranges, higher in the NE Atlantic. Microsatellite data subdivided L. digitata into three main genetic groups matching Brittany, northern Europe and the NW Atlantic, with finer-scale sub-structuring within European clusters. The relatively diverse NE Atlantic lineages probably survived the Last Glacial Maximum along unglaciated periglacial shorelines of the Armorican and Celtic Seas (Brittany cluster) and Ireland (northern European cluster), and remain well differentiated despite their relative proximity. The unique Brittany gene pool, at the contemporary European rear edge, is projected to disappear in the near future under high greenhouse gas emission scenarios. Low allelic diversity and low endemism in the NW Atlantic are consistent with recent post-glacial colonization from Europe, challenging the long-standing hypothesis of in situ glacial survival. Confusion with Hedophyllum nigripes may have led to underestimation of regional diversity of L. digitata, but also to overestimation of its presence along putative trans-Atlantic migration routes. Partial incongruence between modelling and genetic-based biogeographic inferences highlights the benefits of comparing both approaches to understand how shifting climatic conditions affect marine species distributions and explain large-scale patterns of spatial genetic structure.
- Development and characterization of twelve microsatellite markers for Porphyra linearis GrevillePublication . E, Varela-Álvarez; Paulino, Cristina; Serrao, EsterThe genus Porphyra (and its sister genus Pyropia) contains important red algal species that are cultivated and/or harvested for human consumption, sustaining a billion-dollar aquaculture industry. A vast amount of research has been focused on species of this genus, including studies on genetics and genomics among other areas. Twelve novel microsatellite markers were developed here for Porphyra linearis. Markers were characterized using 32 individuals collected from four natural populations of P. linearis with total heterozygosity varying from 0.098 to 0.916. The number of alleles per locus ranged from 2 to 18. All markers showed cross amplification with Porphyra umbilicalis and/or Porphyra dioica. These polymorphic microsatellite markers are useful for investigating population genetic diversity and differentiation in P. linearis and may become useful for other genetic research on the reproductive biology of this important species.
- Ecological traits, genetic diversity and regional distribution of the macroalga Treptacantha elegans along the Catalan coast (NW Mediterranean Sea)Publication . Medrano, Alba; Hereu, Bernat; Mariani, Simone; Neiva, J.; Pagès-Escolà, Marta; Paulino, Cristina; Rovira, Graciel·la; Serrao, Ester; Linares, CristinaThe widespread decline of canopy-forming macroalgal assemblages has been documented in many regions during the last decades. This pattern is often followed by the replacement of structurally complex algal canopies by more simplified habitats (e.g., turfs or sea urchin barren grounds). Against all odds, the fucoid Treptacantha elegans, a large Mediterranean brown macroalga, broadened its depth range to deeper and exposed environments and displayed an unexpected range expansion along the northern coast of Catalonia over the last two decades. Here, we reconstruct the spread of T. elegans in time and space and unravel ecological and demographic traits such as population dynamics and genetic patterns to provide a comprehensive and integrated view of the current status and geographical expansion for this species. Fast-growing dynamics, early fertile maturity, and high turnover rate are the main competitive advantages that allow the exposed populations of T. elegans to colonize available substrata and maintain dense and patchy populations. We also provided evidence that the deeper and exposed populations of T. elegans constitute a single group across the Catalan coast, with little genetic differentiation among populations. This seems to support the hypothesis of a unique source of spread in the last decades from the Medes Islands No-Take Zone towards both southern and northern waters.
- Temporal windows of reproductive opportunity reinforce species barriers in a marine broadcast spawning assemblagePublication . Monteiro, Carla A.; Paulino, Cristina; Jacinto, Rita; Serrão, Ester; Pearson, GarethPrezygotic 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.
- Glacial vicariance drives phylogeographic diversification in the amphi-boreal kelp Saccharina latissimaPublication . MACHADO, JOÃO NEIVA; Paulino, Cristina; Nielsen, Mette M.; Krause-Jensen, Dorte; Saunders, Gary W.; Assis, Jorge; Barbara, Ignacio; Tamigneaux, Eric; Gouveia, Licínia; Aires, Tânia; Marba, Nuria; Bruhn, Annette; Pearson, Gareth; Serrao, Ester A.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.
- Algae as food in Europe: an overview of species diversity and their applicationPublication . Mendes, Madalena; Navalho, Sofia; Ferreira, Alice; Paulino, Cristina; Figueiredo, Daniel; Silva, Daniel; Gao, Fengzheng; Gama, Florinda; Bombo, Gabriel; Jacinto, Rita; Aveiro, Susana; Schulze, Peter S.C.; Gonçalves, Ana Teresa; Pereira, Hugo; Gouveia, Luisa; Patarra, Rita F.; Abreu, Maria Helena; Silva, Joana L.; Navalho, João; Varela, João; Galileu Speranza, LaisAlgae have been consumed for millennia in several parts of the world as food, food supplements, and additives, due to their unique organoleptic properties and nutritional and health benefits. Algae are sustainable sources of proteins, minerals, and fiber, with well-balanced essential amino acids, pigments, and fatty acids, among other relevant metabolites for human nutrition. This review covers the historical consumption of algae in Europe, developments in the current European market, challenges when introducing new species to the market, bottlenecks in production technology, consumer acceptance, and legislation. The current algae species that are consumed and commercialized in Europe were investigated, according to their status under the European Union (EU) Novel Food legislation, along with the market perspectives in terms of the current research and development initiatives, while evaluating the interest and potential in the European market. The regular consumption of more than 150 algae species was identified, of which only 20% are approved under the EU Novel Food legislation, which demonstrates that the current legislation is not broad enough and requires an urgent update. Finally, the potential of the European algae market growth was indicated by the analysis of the trends in research, technological advances, and market initiatives to promote algae commercialization and consumption.
- Cryptic diversity, geographical endemism and allopolyploidy in NE Pacific seaweedsPublication . Neiva, J.; Serrão, Ester; Anderson, Laura; Raimondi, Peter T.; Martins, Neusa; Gouveia, Licínia; Paulino, Cristina; Coelho, Nelson C.; Miller, Kathy A.; Reed, Daniel C.; Ladah, Lydia; Pearson, G. A.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.
- Characterization of 12 polymorphic microsatellite markers in the sugar kelp Saccharina latissimaPublication . Paulino, Cristina; Neiva, J.; Coelho, Nelson C.; Aires, Tânia; Marba, Núria; Krause-Jensen, Dorte; Serrão, EsterSaccharina latissima is an ecologically and economically important kelp species native to the coastal regions of the Northern Hemisphere. This species has considerable phylogeographic structure and morphological plasticity, but lack of resolution of available genetic markers prevents a finer characterization of its genetic diversity and structure. Here, we describe 12 microsatellite loci identified in silico in a genomic library, and assess their polymorphism in three distant populations. Allelic richness at the species level was relatively high (5-23 alleles per locus), as was gene diversity within populations (0.42 < H (E) < 0.62). In addition, individuals readily form distinct genotypic clusters matching their populations of origin. The variation detected confirms the great potential of these markers to investigate the biogeography and population dynamics of S. latissima, and to better characterize its genetic resources for the establishing farming industry.
- Polyploid lineages in the genus PorphyraPublication . Varela-Álvarez, Elena; Loureiro, João; Paulino, Cristina; Serrao, Ester A.Whole genome duplication is now accepted as an important evolutionary force, but the genetic factors and the life history implications affecting the existence and abundance of polyploid lineages within species are still poorly known. Polyploidy has been mainly studied in plant model species in which the sporophyte is the dominant phase in their life history. In this study, we address such questions in a novel system (Porphyra, red algae) where the gametophyte is the dominant phase in the life history. Three Porphyra species (P. dioica, P. umbilicalis, and P. linearis) were used in comparisons of ploidy levels, genome sizes and genetic differentiation using flow cytometry and 11 microsatellite markers among putative polyploid lineages. Multiple ploidy levels and genome sizes were found in Porphyra species, representing different cell lines and comprising several cytotype combinations among the same and different individuals. In P. linearis, genetic differentiation was found among three polyploid lineages: triploid, tetraploid and mixoploids, representing different evolutionary units. We conclude that the gametophytic phase (n) in Porphyra species is not haploid, contradicting previous theories. New hypotheses for the life histories of Porphyra species are discussed.