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  • Linking ecology to genetics to better understand adaptation and evolution: a review in marine macrophytes
    Publication . Hu, Zi-Min; Zhong, Kai-Le; Weinberger, Florian; Duan, De-Lin; Draisma, Stefano G. A.; Serrao, Ester
    Ecological processes and intra-specific genetic diversity reciprocally affect each other. While the importance of uniting ecological variables and genetic variation to understand species’ plasticity, adaptation, and evolution is increasingly recognized, only few studies have attempted to address the intersection of population ecology and genetics using marine macrophyte as models. Representative empirical case studies on genetic diversity are reviewed that explore ecological and evolutionary processes in marine macrophytes. These include studies on environment-induced phenotypic plasticity and associated ecological adaptation; population genetic variation and structuring driven by ecological variation; and ecological consequences mediated by intraspecific and interspecific diversity. Knowledge gaps are also discussed that impede the connection of ecology and genetics in macrophytes and possible approaches to address these issues. Finally, an eco-evolutionary perspective is advocated, by incorporating structural-tofunctional genomics and life cycle complexity, to increase the understanding of the adaptation and evolution of macrophytes in response to environmental heterogeneity.
  • Population level variation in reproductive development and output in the golden kelp Laminaria ochroleuca under marine heat wave scenarios
    Publication . Strasser, Fiona-Elaine; Barreto, Luis M.; Kaidi, Soukaina; Sabour, Brahim; A, Serrão; Pearson, Gareth; Martins, Neusa
    Thermal tolerance is often interpreted as a species-wide thermal niche in the absence of studies focusing on the adaptive potential of populations to exhibit differential thermal tolerance. Thus, considering intraspecific thermal plasticity, local adaptation or both between populations along distributional gradients when interpreting and predicting species responses to warming is imperative. Removing the effect of environmental histories by raising kelp gametophyte generations in vitro under common garden conditions allows unbiased comparison between population-specific adaptive variation under different environmental conditions. Following this approach, this study aims to detect (potentially) adaptive differentiation in microscopic life-stages (gametophytes) between populations of a temperate forest forming kelp, Laminaria ochroleuca from locations with distinct thermal conditions. Gametophytes from four geographically distinct populations were subjected to different temperature treatments (17, marine heat waves of 23, 25 and 27 degrees C) and gametophyte survival during thermal stress as well as reproductive success and photosynthetic responses during recovery were investigated. Intraspecific variation in resilience and reproductive output to thermal stress was found in L. ochroleuca; gametophytes from the most northern population (Brittany, France) were the most thermally sensitive, with mortality onset at 23 degrees C, whereas mortality in the remaining populations was only apparent at 27 degrees C. Gametophytes from northern Spain and Morocco exhibited very low reproductive success during recovery from 23 and 25 degrees C. However, when recovering from the highest thermal treatment (27 degrees C) the reproductive development and sporophyte output was higher than in the gametophytes from France and Italy (Mediterranean). The population-specific responses of gametophyte resilience and reproductive success to temperature stress suggest genetic differentiation in response to variation in local thermal regimes.
  • Mates matter: gametophyte kinship recognition and inbreeding in the giant kelp, Macrocystis pyrifera (Laminariales, Phaeophyceae)
    Publication . Camus, Carolina; Solas, Maribel; Martinez, Camila; Vargas, Jaime; Garces, Cristobal; Gil-Kodaka, Patricia; Ladah, Lydia B.; Serrao, Ester A.; Faugeron, Sylvain
    Inbreeding, the mating between genetically related individuals, often results in reduced survival and fecundity of offspring, relative to outcrossing. Yet, high inbreeding rates are commonly observed in seaweeds, suggesting compensatory reproductive traits may affect the costs and benefits of the mating system. We experimentally manipulated inbreeding levels in controlled crossing experiments, using gametophytes from 19 populations of Macrocystis pyrifera along its Eastern Pacific coastal distribution (EPC). The objective was to investigate the effects of male-female kinship on female fecundity and fertility, to estimate inbreeding depression in the F1 progeny, and to assess the variability of these effects among different regions and habitats of the EPC. Results revealed that the presence and kinship of males had a significant effect on fecundity and fertility of female gametophytes. Females left alone or in the presence of sibling males express the highest gametophyte size, number, and size of oogonia, suggesting they were able to sense the presence and the identity of their mates before gamete contact. The opposite trend was observed for the production of embryos per female gametes, indicating higher costs of selfing and parthenogenesis than outcrossing on fertility. However, the increased fecundity compensated for the reduced fertility, leading to a stable overall reproductive output. Inbreeding also affected morphological traits of juvenile sporophytes, but not their heatwave tolerance. The male-female kinship effect was stronger in high-latitude populations, suggesting that females from low-latitude marginal populations might have evolved to mate with any male gamete to guarantee reproductive success.
  • Microbiome dynamics in the tissue and mucus of acroporid corals differ in relation to host and environmental parameters
    Publication . Marchioro, Giulia Manso; Glasl, Bettina; Engelen, Aschwin; Serrao, Ester; Bourne, David G.; Webster, Nicole; Rodrigues Frade, Pedro
    Corals are associated with diverse microbial assemblages; however, the spatial-temporal dynamics of intra-species microbial interactions are poorly understood. The coral-associated microbial community varies substantially between tissue and mucus microhabitats; however, the factors controlling the occurrence, abundance, and distribution of microbial taxa over time have rarely been explored for different coral compartments simultaneously. Here, we test (1) differentiation in microbiome diversity and composition between coral compartments (surface mucus and tissue) of two Acropora hosts (A. tenuis and A. millepora) common along inshore reefs of the Great Barrier Reef, as well as (2) the potential linkage between shifts in individual coral microbiome families and underlying host and environmental parameters. Amplicon based 16S ribosomal RNA gene sequencing of 136 samples collected over 14 months, revealed significant differences in bacterial richness, diversity and community structure among mucus, tissue and the surrounding seawater. Seawater samples were dominated by members of the Synechococcaceae and Pelagibacteraceae bacterial families. The mucus microbiome of Acropora spp. was dominated by members of Flavobacteriaceae, Synechococcaceae and Rhodobacteraceae and the tissue was dominated by Endozoicimonaceae. Mucus microbiome in both Acropora species was primarily correlated with seawater parameters including levels of chlorophyll a, ammonium, particulate organic carbon and the sum of nitrate and nitrite. In contrast, the correlation of the tissue microbiome to the measured environmental (i.e., seawater parameters) and host health physiological factors differed between host species, suggesting host-specific modulation of the tissue-associated microbiome to intrinsic and extrinsic factors. Furthermore, the correlation between individual coral microbiome members and environmental factors provides novel insights into coral microbiome-by-environment dynamics and hence has potential implications for current reef restoration and management efforts (e.g. microbial monitoring and observatory programs).
  • Predicted regime shift in the seagrass ecosystem of the Gulf of Arguin driven by climate change
    Publication . Chefaoui, Rosa M.; Duarte, Carlos M.; Tavares, Ana I; Frade, Duarte; Sidi Cheikh, M.A.; Abdoull Ba, M.; Serrao, Ester
    The Banc d′Arguin is a marine ecosystem of global conservation significance, the largest bird sanctuary of western Africa, supported by one of the most extensive seagrass beds in the world composed by three seagrass species, two temperate near their southern limit (Zostera noltei and Cymodocea nodosa) and one tropical at its northern limit (Halodule wrightii). Here we predict the fate of this seagrass ecosystem under climate change scenarios during the 21st century, using species distribution models and sea level rise estimates. We forecast a probable decline in total seagrass area of 3340 Km2 (78%) by 2100, involving the loss of both temperate seagrasses (Z. noltei, C. nodosa), the foundational ecosystem components. By 2050, only the tropical species (H. wrightii) would remain, which forms thin and sparse shallow stands functionally distinct from the previous tall dense meadows that span wider vertical ranges. Intertidal flats, the essential bird foraging habitats, would become unvegetated and also suffer a major reduction in area (114 km2 by 2050, 587 km2 by 2100). The large projected loss of foundational seagrass species portends a collapse of major ecosystem functions with profound impacts on biodiversity, fishery resources and ecosystem services.
  • Spatiotemporal variation of the epifaunal assemblages associated to Sargassum muticum on the NW Atlantic coast of Morocco
    Publication . Belattmania, Zahira; Chaouti, Abdellatif; Engelen, Aschwin; Serrao, Ester; Machado, Margarida; Reani, Abdeltif; Sabour, Brahim
    Epifaunal assemblages inhabiting the non-indigenous macroalga Sargassum muticum (Yendo) Fensholt were investigated on two physically distinct intertidal rocky (S1) and sandy (S2) sites along the Atlantic coast of Morocco. The objective of this study was to test whether the habitat-forming marine alga S. muticum invasive in these sites supported different epifaunal assemblages under different environmental conditions and through time. The gastropods Steromphala umbilicalis, S. pennanti, and Rissoa parva and the isopod Dynamene bidentata were the most contributive species to the dissimilarity of epifaunal assemblage structure between both sites throughout seasons. SIMPER analysis showed a dissimilarity of 58.3-78.5% in the associated species composition of S. muticum between study sites with respect to sampling season. Species diversity and total abundance were significantly higher at the rocky site compared to the sandy site. PERMANOVA analyses showed significant differences of associated epifaunal assemblage structure for the season and site interaction. Accordingly, site and season were determinant factors conditioning the role of habitat in structuring epifaunal assemblages.
  • eDNA metabarcoding reveals a rich but threatened and declining elasmobranch community in West Africa’s largest marine protected area, the Banc d’Arguin
    Publication . de la Hoz Schilling, Carolina; Jabado, Rima W.; Veríssimo, Ana; Caminiti, Luca; Sidina, Ebaye; Gandega, Cheikhna Yero; Serrao, Ester
    Elasmobranchs (sharks and rays) are the most threatened marine vertebrates, particularly in tropical and subtropical areas. Their population status is often poorly understood due to insufficient information. Despite reportedly harbouring critical elasmobranch habitats, the Banc d'Arguin National Park (PNBA) in Mauritania lacks comprehensive and updated information on the diversity of elasmobranch species in the area. We developed a baseline inventory based on morphological and molecular identification and metabarcoding. DNA barcoding of tissue samples from elasmobranch processing sites and freshly sampled specimens was used to build a genetic reference database of local elasmobranch species. The richness and diversity of species in the PNBA were described via metabarcoding of seawater eDNA samples using an elasmobranch-specific assay and our reference database. We detected 27 species, including 12 new species records for the PNBA. We further uncover potentially undescribed species of Gymnura and Torpedo, while taxonomic corrections are noted for previously reported species. In particular, the reportedly abundant Mustelus mustelus was absent from tissue and eDNA samples, while M. punctulatus was detected instead. Taxa that have anecdotally become regionally extinct or rare (e.g., sawfishes, wedgefishes, lemon sharks) were not detected, highlighting local species diversity shifts within the last few decades. Results show that 67.9% of elasmobranch species in the PNBA are threatened with extinction according to the IUCN Red List of Threatened Species. This study emphasises the importance of taxonomic identification in support of species management and provides a baseline to inform future studies and conservation measures to avoid further species losses.
  • Genetic diversity of a marine foundation species,Laminaria hyperborea(Gunnerus) Foslie, along the coast of Ireland
    Publication . Schoenrock, Kathryn M.; O'Connor, Aisha M.; Mauger, Stephane; Valero, Myriam; MACHADO, JOÃO NEIVA; Serrao, Ester; Krueger-Hadfield, Stacy A.
    Worldwide, kelp populations are stressed by warming, increased storms and other anthropogenic disturbances. Marine population distributions are projected to retreat poleward with climate change if they cannot adapt to changing conditions, which would potentially lead to a regime shift in subtidal habitats. In Northern Europe,Laminaria hyperboreais a subtidal ecosystem engineer whose distribution has shifted over millennia, leaving predicted areas of high genetic diversity from the last glacial maximum (LGM) near its southern distribution limit in the Iberian Peninsula. In Ireland,L. hyperboreastructures communities by supporting diverse faunal assemblages and producing large quantities of organic carbon throughout the year. We investigated the genetic diversity of eight populations, ranging from the southern coast to the north-west of Ireland, using nine microsatellite loci. Diversity was found to be highest in Lough Hyne, a Special Area of Conservation (SAC), near the predicted climate refugium. We found evidence of isolation by distance, with high connectivity between populations that were geographically close, probably driven by short range dispersal ofL. hyperboreapropagules. Genetic diversity (measured as expected heterozygosity and allelic richness) was highest at Lough Hyne, and decreased northwards, as predicted from past range shifts. Expected heterozygosity was highest at Lough Hyne (0.706) and decreased northward, with the lowest value at Bridges of Ross (0.283). Based on these patterns, further fine-scale investigation into population diversity, dispersal and potential resilience in Irish kelp forests are necessary as warming and non-native species are observed more and more frequently.
  • Non-indigenous seaweeds in the Northeast Atlantic Ocean, the Mediterranean Sea and Macaronesia: a critical synthesis of diversity, spatial and temporal patterns
    Publication . van der Loos, Luna M.; Bafort, Quinten; Bosch, Samuel; Ballesteros, Enric; Bárbara, Ignacio; Berecibar, Estibaliz; Blanfuné, Aurélie; Bogaert, Kenny; Bouckenooghe, Silke; Boudouresque, Charles-François; Brodie, Juliet; Cecere, Ester; Díaz-Tapia, Pilar; Engelen, Aschwin; Gunnarson, Karl; Shabaka, Soha Hamdy; Hoffman, Razy; Husa, Vivian; Israel, Álvaro; Karremans, Mart; Knoop, Jessica; Le Gall, Line; Maggs, Christine A.; Mineur, Frédéric; Parente, Manuela; Perk, Frank; Petrocelli, Antonella; Rodríguez-Prieto, Conxi; Ruitton, Sandrine; Sansón, Marta; A Serrao, Ester; Sfriso, Adriano; Sjøtun, Kjersti; Stiger-Pouvreau, Valérie; Surget, Gwladys; Taşkin, Ergün; Thibaut, Thierry; Tsiamis, Konstantinos; Van De Weghe, Lotte; Verlaque, Marc; Viard, Frédérique; Vranken, Sofie; Leliaert, Frederik; De Clerck, Olivier
    Effective monitoring of non-indigenous seaweeds and combatting their effects relies on a solid confirmation of the non-indigenous status of the respective species. We critically analysed the status of presumed non-indigenous seaweed species reported from the Mediterranean Sea, the Northeast Atlantic Ocean and Macaronesia, resulting in a list of 140 species whose non-indigenous nature is undisputed. For an additional 87 species it is unclear if they are native or non-indigenous (cryptogenic species) or their identity requires confirmation (data deficient species). We discuss the factors underlying both taxonomic and biogeographic uncertainties and outline recommendations to reduce uncertainty about the non-indigenous status of seaweeds. Our dataset consisted of over 19,000 distribution records, half of which can be attributed to only five species (Sargassum muticum, Bonnemaisonia hamifera, Asparagopsis armata, Caulerpa cylindracea and Colpomenia peregrina), while 56 species (40%) are recorded no more than once or twice. In addition, our analyses revealed considerable variation in the diversity of non-indigenous species between the geographic regions. The Eastern Mediterranean Sea is home to the largest fraction of non-indigenous seaweed species, the majority of which have a Red Sea or Indo-Pacific origin and have entered the Mediterranean Sea mostly via the Suez Canal. Non-indigenous seaweeds with native ranges situated in the Northwest Pacific make up a large fraction of the total in the Western Mediterranean Sea, Lusitania and Northern Europe, followed by non-indigenous species with a presumed Australasian origin. Uncertainty remains, however, regarding the native range of a substantial fraction of non-indigenous seaweeds in the study area. In so far as analyses of first detections can serve as a proxy for the introduction rate of non-indigenous seaweeds, these do not reveal a decrease in the introduction rate, indicating that the current measures and policies are insufficient to battle the introduction and spread of non-indigenous species in the study area.
  • Exploring the response of a key Mediterranean gorgonian to heat stress across biological and spatial scales
    Publication . Gómez-Gras, D.; Bensoussan, N.; Ledoux, J. B.; López-Sendino, P.; Cerrano, C.; Ferretti, E.; Kipson, S.; Bakran-Petricioli, T.; A, Serrão; Paulo, D.; Coelho, Márcio; Pearson, Gareth; Boavida, J.; Montero-Serra, I.; Pagès-Escolà, M.; Medrano, A.; López-Sanz, A.; Milanese, M.; Linares, C.; Garrabou, J.
    Understanding the factors and processes that shape intra-specific sensitivity to heat stress is fundamental to better predicting the vulnerability of benthic species to climate change. Here, we investigate the response of a habitat-forming Mediterranean octocoral, the red gorgonian Paramuricea clavata (Risso, 1826) to thermal stress at multiple biological and geographical scales. Samples from eleven P. clavata populations inhabiting four localities separated by hundreds to more than 1500 km of coast and with contrasting thermal histories were exposed to a critical temperature threshold (25 degrees C) in a common garden experiment in aquaria. Ten of the 11 populations lacked thermotolerance to the experimental conditions provided (25 days at 25 degrees C), with 100% or almost 100% colony mortality by the end of the experiment. Furthermore, we found no significant association between local average thermal regimes nor recent thermal history (i.e., local water temperatures in the 3 months prior to the experiment) and population thermotolerance. Overall, our results suggest that local adaptation and/or acclimation to warmer conditions have a limited role in the response of P. clavata to thermal stress. The study also confirms the sensitivity of this species to warm temperatures across its distributional range and questions its adaptive capacity under ocean warming conditions. However, important inter-individual variation in thermotolerance was found within populations, particularly those exposed to the most severe prior marine heatwaves. These observations suggest that P. clavata could harbor adaptive potential to future warming acting on standing genetic variation (i.e., divergent selection) and/or environmentally-induced phenotypic variation (i.e., intra- and/or intergenerational plasticity).