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  • Genetic affinities and biogeography of putative Levantine-endemic seaweed Treptacantha rayssiae (Ramon) M.Mulas, J.Neiva & A.Israel, comb. nov. (Phaeophyceae)
    Publication . Mulas, Martina; Neiva, J.; Sadogurska, Sofia S.; Ballesteros, Enric; Serrao, Ester; Rilov, Gil; Israel, Alvaro
    Cystoseira sensu lato (Ochrophyta) forests are important habitat formers in the Mediterranean Sea, but they have mostly been studied in the western basin where many species are under decline. In the eastern basin, where fewer species occur, Cystoseira rayssiae Ramon was described in the year 2000 as an endemic species based on morphological characteristics from herbaria samples collected on the Israeli coast. No further investigations have been conducted on this peculiar species since, but recently it has been recorded in contiguous Lebanon and outside the Mediterranean. Our work was aimed at confirming the taxonomic validity and endemic nature of this species, including its position among the recently split Cystoseira sensu stricto, Carpodesmia Greville and Treptacantha Kutzing genera, by sequencing the mitochondrial COI gene and by examining morphological characteristics in samples from three different sites in northern Israel. Notwithstanding considerable morphological plasticity, molecular analyses revealed a single unique COI sequence. Phylogenetic analyses show that Cystoseira rayssiae belongs to the resurrected genus Treptacantha and hence, the new combination Treptacantha rayssiae (Ramon) M.Mulas, J.Neiva & A.Israel, comb. nov., is proposed. Unique sequences and a restricted range support its Levantine-endemic status. Intriguing extra-Mediterranean reports from the Red Sea and the Persian Gulf are probably misidentifications rather than reflecting a disjunct distribution or recent invasion.
  • The genus Cystoseira s.l. (Ochrophyta, Fucales, Sargassaceae) in the Black Sea: morphological variability and molecular taxonomy of Gongolaria barbata and endemic Ericaria crinita f. bosphorica comb. nov.
    Publication . Sadogurska, Sofia S.; Neiva, João; Falace, Annalisa; Serrao, Ester; Israel, Alvaro
    Brown algae of the genus Cystoseira sensu lato form the most diverse and productive marine ecosystems throughout the Mediterranean Sea and have equal roles also in the Black Sea where they have been decreasing in the recent years. The taxonomy of Cystoseira s.l. taxa from the Black Sea is still not well understood, and questions arise when related taxa have to be delimited. In addition to morphological descriptions, this study provides for the first time molecular data of the Black Sea Cystoseira s.l. distinct morphologies as an additional tool to clarify their identities and phylogenetic affinities. The analysis of two mitochondrial markers (cytochrome oxidase subunit 1-COI, and 23S-tRNAVal intergenic spacer-mt-spacer) showed that Cystoseira s.l. specimens from the Black Sea belong to two recently resurrected genera, namely Gongolaria and Ericaria. Molecular data confirm the morphological identification of G. barbata, which is characterized by high morphological plasticity in the Black Sea. The morphological data presented in this study support the transition of G. barbata to the genus Gongolaria, which was previously proposed based solely on genetic data. For the Black Sea endemic taxon C. bosphorica, sequence divergence suggests conspecificity with Mediterranean Sea species E. crinita and E. barbatula. However, considering original morphological characteristics of the taxon, its geographical isolation, and endemism, the new combination Ericaria crinita f. bosphorica comb. nov. is proposed.
  • Genetic diversity of Saccharina latissima (Phaeophyceae) along a salinity gradient in the North Sea-Baltic Sea transition zone
    Publication . Nielsen, Mette Moller; Paulino, Cristina; Neiva, J.; Krause-Jensen, Dorte; Bruhn, Annette; Serrão, Ester
    The 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 Atlantic
    Publication . Neiva, J.; Serrao, Ester; Paulino, Cristina; Gouveia, Licínia; Want, Andrew; Tamigneaux, Éric; Ballenghien, Marion; Mauger, Stéphane; Fouqueau, Louise; Engel-Gautier, Carolyn; Destombe, Christophe; Valero, Myriam
    In 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.
  • Shift happens: trailing edge contraction associated with recent warming trends threatens a distinct genetic lineage in the marine macroalga Fucus vesiculosus
    Publication . Nicastro, Katy R; I Zardi, Gerardo; Teixeira, Sara; Neiva, J.; Serrão, Ester; Pearson, G. A.
    Significant effects of recent global climate change have already been observed in a variety of ecosystems, with evidence for shifts in species ranges, but rarely have such consequences been related to the changes in the species genetic pool. The stretch of Atlantic coast between North Africa and North Iberia is ideal for studying the relationship between species distribution and climate change as it includes the distributional limits of a considerable number of both cold- and warm-water species. We compared temporal changes in distribution of the canopy-forming alga Fucus vesiculosus with historical sea surface temperature (SST) patterns to draw links between range shifts and contemporary climate change. Moreover, we genetically characterized with microsatellite markers previously sampled extinct and extant populations in order to estimate resulting cryptic genetic erosion. Results Over the past 30 years, a geographic contraction of the southern range edge of this species has occurred, with a northward latitudinal shift of approximately 1,250 km. Additionally, a more restricted distributional decline was recorded in the Bay of Biscay. Coastal SST warming data over the last three decades revealed a significant increase in temperature along most of the studied coastline, averaging 0.214°C/decade. Importantly, the analysis of existing and extinct population samples clearly distinguished two genetically different groups, a northern and a southern clade. Because of the range contraction, the southern group is currently represented by very few extant populations. This southern edge range shift is thus causing the loss of a distinct component of the species genetic background. Conclusions We reveal a climate-correlated diversity loss below the species level, a process that could render the species more vulnerable to future environmental changes and affect its evolutionary potential. This is a remarkable case of genetic uniqueness of a vanishing cryptic genetic clade (southern clade).
  • Increased evolutionary rates and conserved transcriptional response following allopolyploidization in brown algae
    Publication . Sousa, Filipe; Neiva, J.; Martins, Neusa; Jacinto, Rita; Anderson, Laura; Raimondi, Peter T.; Serrao, Ester; Pearson, Gareth
    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.
  • Drifting fronds and drifting alleles: range dynamics, local dispersal and habitat isolation shape the population structure of the estuarine seaweed Fucus ceranoides
    Publication . Neiva, J.; Pearson, G. A.; Valero, Myriam; Serrão, Ester
    Aim: The seaweed Fucus ceranoides is restricted to spatially discrete estuarine habitats and lacks planktonic dispersal phases; it is therefore expected to exhibit strong population differentiation. Its cold-temperate affinities and mtDNA variation imply that the northern part of the species’ range, where F. ceranoides is now ubiquitous, was recently colonized after the onset of the last deglaciation, potentially resulting in areas with greater genetic homogeneity. Here we examine the population structure of F. ceranoides to test these predictions, emphasizing the contrasting genetic signatures of limited dispersal in refugial versus recently colonized regions. Location: North-eastern Atlantic estuaries from Portugal to Norway. Methods: A total of 504 individuals from 21 estuarine sites spanning the entire range of F. ceranoides were sampled and genotyped for nine microsatellite loci. Population structure was inferred from several genotypic and allele-frequency analyses. Geographical patterns of genetic diversity were used to reconstruct the historical biogeography of the species. Results: Genetic diversity and regional population differentiation showed a consistent decline with increasing latitude. Southernmost populations harboured most of the endemic variation, whereas the northern populations (> 55 N) were almost fixed for the same alleles across loci. In southern and central regions of its distribution, F. ceranoides showed striking population subdivision, with many of the sampled estuaries corresponding to coherent genetic units that were easily discriminated from one another with standard clustering methods. Main conclusions: The geographical pattern of genetic diversity supports the long-term refugial status of Iberia and a post-glacial range expansion of F. ceranoides into previously glaciated latitudes. Despite the species’ capacity to colonize newly available habitats, the genetic structure of F. ceranoides outside the recently (re)colonized range reveals that gene flow between populations is extremely low. This study provides a remarkable example of how infrequent and spatially limited dispersal can have contrasting effects at the scales of metapopulation (connectivity) versus range dynamics (habitat tracking), and of how dispersal restrictions can result in either genetic divergence or homogeneity depending on the maturity and demographic conditions of the populations.
  • Genes left behind: Climate change threatens cryptic genetic diversity in the canopy-forming seaweed bifurcaria bifurcata
    Publication . Neiva, J.; Assis, J.; Coelho, Nelson; Fernandes, Francisco; Pearson, Gareth; Serrao, Ester A.
    The global redistribution of biodiversity will intensify in the coming decades of climate change, making projections of species range shifts and of associated genetic losses important components of conservation planning. Highly-structured marine species, notably brown seaweeds, often harbor unique genetic variation at warmer low-latitude rear edges and thus are of particular concern. Here, a combination of Ecological Niche Models (ENMs) and molecular data is used to forecast the potential near-future impacts of climate change for a warm-temperate, canopy forming seaweed, Bifurcaria bifurcata. ENMs for B. bifurcata were developed using marine and terrestrial climatic variables, and its range projected for 2040-50 and 2090-2100 under two greenhouse emission scenarios. Geographical patterns of genetic diversity were assessed by screening 18 populations spawning the entire distribution for two organelle genes and 6 microsatellite markers. The southern limit of B. bifurcata was predicted to shift northwards to central Morocco by the mid-century. By 2090-2100, depending on the emission scenario, it could either retreat further north to western Iberia or be relocated back to Western Sahara. At the opposing margin, B. bifurcata was predicted to expand its range to Scotland or even Norway. Microsatellite diversity and endemism were highest in Morocco, where a unique and very restricted lineage was also identified. Our results imply that B. bifurcata will maintain a relatively broad latitudinal distribution. Although its persistence is not threatened, the predicted extirpation of a unique southern lineage or even the entire Moroccan diversity hotspot will erase a rich evolutionary legacy and shrink global diversity to current (low) European levels. NW Africa and similarly understudied southern regions should receive added attention if expected range changes and diversity loss of warm-temperate species is not to occur unnoticed.
  • Ocean currents shape the genetic structure of a kelp in southwestern Africa
    Publication . Assis, Jorge; Neiva, J.; Bolton, John J.; Rothman, Mark D.; Gouveia, Licínia; Paulino, Cristina; Mohdnasir, Hasliza; Anderson, Robert J.; Reddy, Maggie M.; Kandjengo, Lineekela; Kreiner, Anja; Pearson, Gareth; Serrao, Ester
    Aim Drivers of extant population genetic structure include past climate-driven range shifts and vicariant events, as well as gene flow mediated by dispersal and habitat continuity. Their integration as alternative or complementary drivers is often missing or incomplete, potentially overlooking relevant processes and time scales. Here we ask whether it is the imprint of past range shifts or habitat connectivity driven by oceanographic transport that best explain genetic structure in a poorly understood model, a forest-forming African kelp. Location Southwestern coast of Africa (Benguela current region). Taxon Laminaria pallida. Methods We estimated genetic variability along the species distributional range using 14 microsatellite markers. This genetic variability was compared to estimates of past range shifts derived from species distribution modelling for the Last Glacial Maximum (LGM), the mid-Holocene (MH) and the present, and estimates of habitat connectivity derived from oceanographic biophysical modelling. Results The species is structured in two clusters, a southern cluster with much richer (allelic richness A: 10.40 +/- 0.33) and unique (private alleles PA: 56.69 +/- 4.05) genetic diversity, and a northern cluster (A: 4.75 +/- 0.17; PA: 6.70 +/- 1.45). These clusters matched well-known biogeographical regions and their transition coincided with a dispersal barrier formed by upwelled offshore transport. No major range shifts or vicariant events were hindcasted along the present range, suggesting population stability from the LGM to the present. Main conclusions Habitat connectivity, rather than past range shifts, explains the extant population structure. Future environmental requirements of the species along the Benguela upwelling system are projected to persist or even intensify, likely preserving the observed genetic patterns for the years to come. Yet, the differentiation and endemicity between clusters, and the isolation structured by the regional oceanography, implies high conservation value for genetic biodiversity, and even more if considering the ecological, social and economic services provided by kelp forests.
  • Marine forests of the Mediterranean-Atlantic Cystoseira tamariscifolia complex show a southern Iberian genetic hotspot and no reproductive isolation in parapatry
    Publication . Bermejo, Ricardo; Chefaoui, Rosa M.; Engelen, Aschwin H.; Buonomo, Roberto; Neiva, J.; Ferreira-Costa, Joana; Pearson, Gareth; Marba, Nuria; Duarte, Carlos M.; Airoldi, Laura; Hernandez, Ignacio; Guiry, Michael D.; Serrao, Ester A.
    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.