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- Habitat continuity and stepping-stone oceanographic distances explain population genetic connectivity of the brown alga Cystoseira amentaceaPublication . Buonomo, Roberto; Assis, J.; Fernandes, Francisco; Engelen, Aschwin H.; Airoldi, Laura; Serrao, Ester A.Effective predictive and management approaches for species occurring in a metapopulation structure require good understanding of interpopulation connectivity. In this study, we ask whether population genetic structure of marine species with fragmented distributions can be predicted by stepping-stone oceanographic transport and habitat continuity, using as model an ecosystem-structuring brown alga, Cystoseira amentacea var. stricta. To answer this question, we analysed the genetic structure and estimated the connectivity of populations along discontinuous rocky habitat patches in southern Italy, using microsatellite markers at multiple scales. In addition, we modelled the effect of rocky habitat continuity and ocean circulation on gene flow by simulating Lagrangian particle dispersal based on ocean surface currents allowing multigenerational stepping-stone dynamics. Populations were highly differentiated, at scales from few metres up to thousands of kilometres. The best possible model fit to explain the genetic results combined current direction, rocky habitat extension and distance along the coast among rocky sites. We conclude that a combination of variable suitable habitat and oceanographic transport is a useful predictor of genetic structure. This relationship provides insight into the mechanisms of dispersal and the role of life-history traits. Our results highlight the importance of spatially explicit modelling of stepping-stone dynamics and oceanographic directional transport coupled with habitat suitability, to better describe and predict marine population structure and differentiation. This study also suggests the appropriate spatial scales for the conservation, restoration and management of species that are increasingly affected by habitat modifications.
- Genetic and oceanographic tools reveal high population connectivity and diversity in the endangered pen shell Pinna nobilisPublication . Wesselmann, Marlene; Gonzalez-Wanguemert, Mercedes; Serrao, Ester A.; Engelen, Aschwin H.; Renault, Lionel; Garcia-March, Jose R.; Duarte, Carlos M.; Hendriks, IrisFor marine meta-populations with source-sink dynamics knowledge about genetic connectivity is important to conserve biodiversity and design marine protected areas (MPAs). We evaluate connectivity of a Mediterranean sessile species, Pinna nobilis. To address a large geographical scale, partial sequences of cytochrome oxidase I (COI, 590 bp) were used to evaluate phylogeographical patterns in the Western Mediterranean, and in the whole basin using overlapping sequences from the literature (243 bp). Additionally, we combined (1) larval trajectories based on oceanographic currents and early life-history traits and (2) 10 highly polymorphic microsatellite loci collected in the Western Mediterranean. COI results provided evidence for high diversity and low inter-population differentiation. Microsatellite genotypes showed increasing genetic differentiation with oceanographic transport time (isolation by oceanographic distance (IBD) set by marine currents). Genetic differentiation was detected between Banyuls and Murcia and between Murcia and Mallorca. However, no genetic break was detected between the Balearic populations and the mainland. Migration rates together with numerical Lagrangian simulations showed that (i) the Ebro Delta is a larval source for the Balearic populations (ii) Alicante is a sink population, accumulating allelic diversity from nearby populations. The inferred connectivity can be applied in the development of MPA networks in the Western Mediterranean.
- Marine forests of the Mediterranean-Atlantic Cystoseira tamariscifolia complex show a southern Iberian genetic hotspot and no reproductive isolation in parapatryPublication . 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.
- Response of kelps from different latitudes to consecutive heat shockPublication . Pereira, Tania R.; Engelen, Aschwin H.; Pearson, Gareth; Valero, Myriam; Serrao, Ester A.Although extensive work has focused on kelp responses to constant temperature, little is known about their response to the consecutive temperature shocks they are often exposed to in the shallow subtidal and intertidal pools. Here we characterized the responses of the two southernmost forest-forming kelp species in the Northeast Atlantic, Laminaria ochroleuca De La Pylaie and Saccorhiza polyschides (Lightf.) Batt. to multiple cycles of thermal stress. Individuals from the upper vertical limit of the geographical distribution edges where the two species co-occur forming forests, France and Portugal, were exposed to 4 consecutive cycles of thermal shock simulating a spring tide. A 24 h cycle consisted of culture at 15 degrees C, plus 1 h heat shock at one of five levels (20, 22.5, 25, 27.5 or 30 degrees C). The maximum quantum yield (Fv/Fm) of chlorophyll fluorescence of photosystem 2 (PS2) was used to detect impaired reaction center function, as a proxy for individual fitness costs, during recovery from heat shock. Both species showed resilience to temperatures from 20 to 25 degrees C. While exposure to 27.5 degrees C caused no inhibition to Fv/Fm of S. polyschides, a threshold was met above this temperature and exposure to 30 degrees C caused the death of all individuals. In contrast, L ochroleuca from France was damaged but able to survive 30 degrees C shocks and individuals from Portugal showed complete resilience to this treatment. In both species, blade elongation decreased with increasing temperature, with necrosis surpassing growth at higher temperatures. Resilience to high temperature exposure may confer an advantage to L ochroleuca to colonize intertidal pools on the Portuguese coast, in agreement with the observation that both species recruit in tide pools but only L ochroleuca reach adulthood. Our results indicate that as summer temperatures increase with climate change, the disappearance of S. polyschides from intertidal pools and a decrease in the density of L ochroleuca can be expected. (C) 2014 Elsevier B.V. All rights reserved.
- Acidification increases abundances of Vibrionales and Planctomycetia associated to a seaweed-grazer system: potential consequences for disease and prey digestion efficiencyPublication . Aires, Tânia; Serebryakova, Alexandra; Viard, Frederique; Serrao, Ester A.; Engelen, Aschwin H.Ocean acidification significantly affects marine organisms in several ways, with complex interactions. Seaweeds might benefit from rising CO2 through increased photosynthesis and carbon acquisition, with subsequent higher growth rates. However, changes in seaweed chemistry due to increased CO2 may change the nutritional quality of tissue for grazers. In addition, organisms live in close association with a diverse microbiota, which can also be influenced by environmental changes, with feedback effects. As gut microbiomes are often linked to diet, changes in seaweed characteristics and associated microbiome can affect the gut microbiome of the grazer, with possible fitness consequences. In this study, we experimentally investigated the effects of acidification on the microbiome of the invasive brown seaweed Sargassum muticum and a native isopod consumer Synisoma nadejda. Both were exposed to ambient CO2 conditions (380 ppm, pH 8.16) and an acidification treatment (1,000 ppm, pH 7.86) for three weeks. Microbiome diversity and composition were determined using high-throughput sequencing of the variable regions V5-7 of 16S rRNA. We anticipated that as a result of acidification, the seaweed-associated bacterial community would change, leading to further changes in the gut microbiome of grazers. However, no significant effects of elevated CO2 on the overall bacterial community structure and composition were revealed in the seaweed. In contrast, significant changes were observed in the bacterial community of the grazer gut. Although the bacterial community of S. muticum as whole did not change, Oceanospirillales and Vibrionales (mainly Pseudoalteromonas) significantly increased their abundance in acidified conditions. The former, which uses organic matter compounds as its main source, may have opportunistically taken advantage of the possible increase of the C/N ratio in the seaweed under acidified conditions. Pseudoalteromonas, commonly associated to diseased seaweeds, suggesting that acidification may facilitate opportunistic/pathogenic bacteria. In the gut of S. nadejda, the bacterial genus Planctomycetia increased abundance under elevated CO2. This shift might be associated to changes in food (S. muticum) quality under acidification. Planctomycetia are slow-acting decomposers of algal polymers that could be providing the isopod with an elevated algal digestion and availability of inorganic compounds to compensate the shifted C/N ratio under acidification in their food. In conclusion, our results indicate that even after only three weeks of acidified conditions, bacterial communities associated to ungrazed seaweed and to an isopod grazer show specific, differential shifts in associated bacterial community. These have potential consequences for seaweed health (as shown in corals) and isopod food digestion. The observed changes in the gut microbiome of the grazer seem to reflect changes in the seaweed chemistry rather than its microbial composition.
- The interaction between the proliferating macroalga Asparagopsis taxiformis and the coral Astroides calycularis induces changes in microbiome and metabolomic fingerprintsPublication . Greff, Stephane; Aires, Tânia; Serrao, Ester A.; Engelen, Aschwin H.; Thomas, Olivier P.; Perez, ThierryMediterranean Sea ecosystems are considered as hotspots of biological introductions, exposed to possible negative effects of non-indigenous species. In such temperate marine ecosystems, macroalgae may be dominant, with a great percentage of their diversity represented by introduced species. Their interaction with temperate indigenous benthic organisms have been poorly investigated. To provide new insights, we performed an experimental study on the interaction between the introduced proliferative red alga Asparagopsis taxiformis and the indigenous Mediterranean coral Astroides calycularis. The biological response measurements included meta-barcoding of the associated microbial communities and metabolomic fingerprinting of both species. Significant changes were detected among both associated microbial communities, the interspecific differences decreasing with stronger host interaction. No short term effects of the macroalga on the coral health, neither on its polyp activity or its metabolism, were detected. In contrast, the contact interaction with the coral induced a change in the macroalgal metabolomic fingerprint with a significant increase of its bioactivity against the marine bacteria Aliivibrio fischeri. This induction was related to the expression of bioactive metabolites located on the macroalgal surface, a phenomenon which might represent an immediate defensive response of the macroalga or an allelopathic offense against coral.
- Species specificity of bacteria associated to the brown seaweeds Lobophora (Dictyotales, Phaeophyceae) and their potential for Induction of rapid coral bleaching in Acropora muricataPublication . Vieira, Christophe; Engelen, Aschwin H.; Guentas, Linda; Aires, Tânia; Houlbreque, Fanny; Gaubert, Julie; Serrao, Ester A.; De Clerck, Olivier; Payri, Claude E.While reef degradation is occurring worldwide, it is not uncommon to see phase shifts from coral to macroalgal dominated reefs. Numerous studies have addressed the mechanisms by which macroalgae may outcompete corals and a few recent studies highlighted the putative role of bacteria at the interface between macroalgae and corals. Some studies suggest that macroalgae may act as vectors and/or foster proliferation of microorganisms pathogenic for corals. Using a combination of high throughput sequencing, bacterial culturing, and in situ bioassays we question if the adversity of macroalgal associated bacteria to corals is mediated by specific bacterial taxa. Using Illumina sequencing, we characterized and compared the bacterial community from two Lobophora (Dictyotales, Phaeophyceae) species. The two species presented distinctive bacterial communities. Both species shared approximately half of their OTUs, mainly the most abundant bacteria. Species-specific OTUs belong to Planctomycetes, Proteobacteria, and Bacteroidetes. In total, 16 culturable bacterial strain were isolated and identified from the Lobophora surface, consisting of 10 genera (from nine families, four classes, and three phyla), some of which are not known as, but are related to pathogens involved in coral diseases, and others are naturally associated to corals. When patches of marine agar with 24 h cultures of each of these bacteria were placed in direct contact with the branches of the scleractinian coral Acropora muricata, they caused severe bleaching after 24 h exposure. Results suggest that regardless of taxonomic affinities, increase in density of these bacteria can be adverse to corals. Nevertheless, the microbial community associated to macroalgal surface may not represent a threat to corals, because the specific bacterial screening and control exerted by the alga preventing specific bacterial proliferation.
- Some don't like it hot: microhabitat-dependent thermal and water stresses in a trailing edge populationPublication . Mota, Catarina F.; Engelen, Aschwin H.; Serrao, Ester A.; Pearson, Gareth A.The distributional limits of species in response to environmental change are usually studied at large temporal and/or geographical scales. However, organismal scale habitat variation can be overlooked when investigating large-scale averages of key factors such as temperature. We examine how microhabitat thermal conditions relate to physiological limits, which may contribute to recent range shifts in an intertidal alga. We defined the onset and maximum temperatures of the heat-shock response (HSR) for a southern edge population of Fucus vesiculosus, which has subsequently become extinct. The physiological threshold for resilience (assayed using chlorophyll fluorescence) coincided with declining HSR, determined from the temperature-dependent induction of seven heat-shock protein transcripts. In intertidal habitats, temperature affects physiology directly by controlling body temperature and indirectly through evaporative water loss. We investigated the relationship between the thermal environment and in situ molecular HSR at microhabitat scales. Over cm to m scales, four distinct microhabitats were defined in algal patches (canopy surface, patch edge, subcanopy, submerged channels), revealing distinct thermal and water stress environments during low-tide emersion. The in situ HSR agreed with estimated tissue temperatures in all but one microhabitat. Remarkably, in the most thermally extreme microhabitat (canopy surface), the HSR was essentially absent in desiccated tissue, providing a potential escape from the cellular metabolic costs of thermal stress. Meteorological records, microenvironmental thermal profiles and HSR data indicate that the maximum HSR is approached or exceeded in hydrated tissue during daytime low tides for much of the year. Furthermore, present-day summer seawater temperatures are sufficient to induce HSR during high-tide immersion, preventing recovery and resulting in continuous HSR during daytime low-tide cycles over the entire summer. HSR in the field matched microhabitat temperatures more closely than local seawater or atmospheric data, suggesting that the impacts of climatic change are best understood at the microhabitat scale, particularly in intertidal areas.