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  • Population genetics of Zostera noltii along the west Iberian coast: Consequences of small population size, habitat discontinuity and near-shore currents
    Publication . Diekmann, O. E.; Coyer, J. A.; Ferreira, J.; Olsen, J. L.; Stam, W. T.; Pearson, G. A.; Serrão, Ester
    The effects of oceanographic patterns on marine genetic biodiversity along the SW Iberian Peninsula are poorly understood. We addressed the question of whether gene flow in this region depends solely on geographic distance between isolated patches of suitable habitat or if there are superimposed effects correlated with other factors such as current patterns. Zostera noltii, the dwarf eelgrass, is the keystone habitat-structuring seagrass species on intertidal mudflats along the Iberian west coast. We used 9 microsatellite loci to analyze population genetic diversity and differentiation for all existing 8 populations from NW Spain (Ria de Vigo) to SW Spain (Puerto Real, Cadiz). Populations are highly genetically differentiated as shown by high significant FST,Wright’s fixation index, (0.08 to 0.26) values. A neighbor-joining tree based on Reynold’s distances computed from allele frequencies revealed a split between northern and southern populations (bootstrap support of 84%). This pattern of differentiation can be explained by (1) ocean surface current patterns present during Z. noltii’s reproductive season which cause a dispersal barrier between the northern and southern populations of this region, (2) habitat isolation, due to large geographic distances between suitable habitats, preventing frequent gene flow, and (3) small effective population sizes, causing high drift and thus faster differentiation rates.
  • 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.
  • Canopy microclimate modification in central and marginal populations of a marine macroalga
    Publication . Monteiro, Cátia; Zardi, Gerardo I.; McQuaid, Christopher D.; Serrao, Ester; Pearson, Gareth; Nicastro, Katy
    The effects of environmental changes on species distribution are generally studied at large geographical scales. However, aggregations of individuals can significantly moderate the impact of the environment at smaller, organismal scales. We focused on the intertidal macroalga Fucus guiryi and carried out field and laboratory common garden experiments to evaluate how the different individual morphologies and canopy densities typical of central and peripheral populations modify microhabitat conditions and associated levels of stress. We show that F. guiryi canopies significantly alter environmental conditions (i.e., temperature, humidity and light regimes) and mitigate the levels of stress experienced by individuals within the group. Southern algae are more branched and form denser canopies but, unexpectedly, despite these considerable differences, the mitigating effects of northern and southern canopies did not differ significantly. Microhabitat conditions beneath canopies were more stressful at marginal locations, indicating that southern populations are not more effective than northern algae at mitigating the harsher climate at the edge of the species distribution. Our findings highlight the importance of assessing structural changes in aggregating species across their distribution and relating these to local climates to understand the impact of environmental changes at scales relevant to individual organisms.
  • Temperature effects on the microscopic haploid stage development of laminaria ochroleuca and sacchoriza polyschides, kelps with contrasting life histories
    Publication . Pereira, T. R.; Engelen, Aschwin; Pearson, G. A.; Serrão, Ester; Destombe, C.; Valero, Myriam
    Kelp forests are one of the most diverse and productive ecosystems worldwide. Global climate change and human exploitation threaten the stability of many of these ecosystems.
  • Broad scale agreement between intertidal habitats and adaptive traits on a basis of contrasting population genetic structure
    Publication . I Zardi, Gerardo; Nicastro, Katy R; Ferreira Costa, J.; Serrão, Ester; Pearson, G. A.
    Understanding the extent to which neutral processes and adaptive divergence shape the spatial structure of natural populations is a major goal in evolutionary biology and is especially important for the identification of significant levels of biodiversity. Our results identified replicated habitat-specific (adaptive) phenotypic divergence in the brown macroalga Fucus vesiculosus that is independent of population (neutral) genetic structure. F. vesiculosus inhabits contiguous and contrasting marine to estuarine intertidal habitats. Combining analyses of genetic and phenotypic traits of populations living under differential selective regimes (estuaries and open coast), we investigated levels of neutral genetic differentiation and adaptive physiological responses to emersion stress. In southwest England (SW UK) and northern Iberia (N. Iberia), populations living in estuaries and marine coastal habitats were genetically characterized at six microsatellite loci. In N. Iberia, two clades with limited admixture were recovered, each including one open coast site and the adjacent estuarine location. In contrast, SW UK samples clustered according to habitat and formed three distinct groups of genotypes; one including the two open coast locations and the other two representing each of the estuarine sites. Temperature loggers revealed distinct emersion regimes that characterized each habitat type independently of the region, while water and air temperature profiles showed site-specific trends. Despite acclimation under usual conditions, trait means of emersion stress resilience showed a strong phenotypic divergence between habitats, consistent with environmental clines in exposure time observed in the different habitats. We demonstrate that neutral genetic clusters do not reflect locally adapted population units. Our results identified replicated habitat-specific (adaptive) phenotypic divergence that is independent of population (neutral) genetic structure in F. vesiculosus. The significance of such findings extends beyond the theoretical evolutionary and ecological interest of discovering parallel adaptive responses to the broader implications for conservation of intraspecific biodiversity.
  • 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).
  • Increased heat resilience of intraspecific outbred compared to inbred lineages in the Kelp Laminaria digitata: physiology and transcriptomics
    Publication . Liesner, Daniel; Pearson, Gareth Anthony; Bartsch, Inka; Rana, Shivani; Harms, Lars; Heinrich, Sandra; Bischof, Kai; Glöckner, Gernot; Valentin, Klaus
    Marine forests and kelps as their foundation species are threatened by ocean warming especially at the warm distributional edges. Previously identified genetic divergence and ecotypic differentiation within kelp species may allow to produce more resilient lineages by intraspecific outbreeding among populations. In a mechanistic investigation of heat stress, heterosis (hybrid vigour), and underlying gene expression patterns, we assessed the thermal performance of inbred (selfings) and outbred (reciprocal crosses) sporophytes of the N-Atlantic kelp Laminaria digitata among clonal isolates from two divergent populations; one from the temperate North Sea (Helgoland) and one from the Arctic (Spitsbergen). First, we investigated the upper thermal tolerance of microscopic sporophytes in a 14-day experiment applying sublethal to lethal 20-23 degrees C. The upper survival temperature of microscopic sporophytes was lower for the inbred Arctic selfing (21 degrees C) than for the temperate selfing and the reciprocal crosses (22 degrees C). Only in the temperate selfing, 4.5% of sporophytes survived 23 degrees C. We then subjected 4-7 cm long sporophytes to a control temperature (10 degrees C), moderate (19 degrees C) and sublethal to lethal heat stress (20.5 degrees C) for 18 days to assess gene expression in addition to physiological parameters. Growth and optimum quantum yield decreased similarly in the reciprocal crosses and the temperate selfing at 19 and 20.5 degrees C, while inbred Arctic sporophytes died within seven days at both 19 and 20.5 degrees C. In response to 20.5 degrees C, 252 genes were constitutively regulated across all surviving lineages, which we use to describe metabolic regulation patterns in response to heat stress in kelp. At sublethal 20.5 degrees C, ca. 150 genes were differentially expressed by either crossed lineage in comparison to the temperate selfing, indicating that they maintained a growth response similar to the temperate selfing with differential metabolic regulation during sublethal heat stress. Subtle differences in physiology and the differential expression of nine genes between the reciprocal crosses at 20.5 degrees C indicate that female and male gametophytes may contribute differently to offspring traits. We consider potential inbreeding depression in the Spitsbergen selfing and quantify the better performance of both crosses using heterosis-related parameters. We discuss the potential and risks of outbreeding to produce more resilient crops for mariculture and marine forest restoration.
  • Polar marine biology science in Portugal and Spain: Recent advances and future perspectives
    Publication . Xavier, J.; Barbosa, Ana B.; Agustí, S.; Alonso-Sáez, L.; Alvito, P.; Ameneiro, J.; Ávila, C.; Baeta, A.; Canário, J.; Carmona, R.; Catry, P.; Ceia, F.; Clark, M. S.; Cristobo, F. J.; Cruz, B.; Duarte, C. M.; Figuerola, B.; Gili, J.-M.; Gonçalves, A. R.; Gordillo, F. J. L.; Granadeiro, J. P.; Guerreiro, M.; Isla, Enrique; Jiménez, C.; López-González, P. J.; Lourenço, S.; Marques, J. C.; Moreira, E.; Mota, A. M.; Nogueira, M.; Núñez-Pons, L.; Orejas, C.; Paiva, V. H.; Palanques, A.; Pearson, G. A.; Pedrós-Alió, C.; Peña Cantero, T. L.; Power, Deborah; Ramos, J. A.; Rossi, S.; Serrão, Ester
    Polar marine ecosystems have global ecological and economic importance because of their unique biodiversity and their major role in climate processes and commercial fisheries, among others. Portugal and Spain have been highly active in a wide range of disciplines in marine biology of the Antarctic and the Arctic. The main aim of this paper is to provide a synopsis of some of the results and initiatives undertaken by Portuguese and Spanish polar teams within the field of marine sciences, particularly on benthic and pelagic biodiversity (species diversity and abundance, including microbial, molecular, physiological and chemical mechanisms in polar organisms), conservation and ecology of top predators (particularly penguins, albatrosses and seals), and pollutants and evolution of marine organisms associated with major issues such as climate change, ocean acidification and UV radiation effects. Both countries have focused their polar research more in the Antarctic than in the Arctic. Portugal and Spain should encourage research groups to continue increasing their collaborations with other countries and develop multi-disciplinary research projects, as well as to maintain highly activememberships within major organizations, such as the Scientific Committee for Antarctic Research (SCAR), the International Arctic Science Council (IASC) and the Association of Polar Early Career Scientists (APECS), and in international research projects.
  • Past climate-driven range shifts structuring intraspecific biodiversity levels of the giant kelp (Macrocystis pyrifera) at global scales
    Publication . Assis, Jorge; Alberto, Filipe; Macaya, Erasmo C.; Coelho, Nelson; Faugeron, Sylvain; Pearson, Gareth; Ladah, Lydia; Reed, Daniel C.; Raimondi, Peter; Mansilla, Andrés; Brickle, Paul; Zuccarello, Giuseppe C.; Serrao, Ester
    The paradigm of past climate-driven range shifts structuring the distribution of marine intraspecific biodiversity lacks replication in biological models exposed to comparable limiting conditions in independent regions. This may lead to confounding effects unlinked to climate drivers. We aim to fill in this gap by asking whether the global distribution of intraspecific biodiversity of giant kelp (Macrocystis pyrifera) is explained by past climate changes occurring across the two hemispheres. We compared the species' population genetic diversity and structure inferred with microsatellite markers, with range shifts and long-term refugial regions predicted with species distribution modelling (SDM) from the last glacial maximum (LGM) to the present. The broad antitropical distribution of Macrocystis pyrifera is composed by six significantly differentiated genetic groups, for which current genetic diversity levels match the expectations of past climate changes. Range shifts from the LGM to the present structured low latitude refugial regions where genetic relics with higher and unique diversity were found (particularly in the Channel Islands of California and in Peru), while post-glacial expansions following similar to 40% range contraction explained extensive regions with homogenous reduced diversity. The estimated effect of past climate-driven range shifts was comparable between hemispheres, largely demonstrating that the distribution of intraspecific marine biodiversity can be structured by comparable evolutionary forces across the global ocean. Additionally, the differentiation and endemicity of regional genetic groups, confers high conservation value to these localized intraspecific biodiversity hotspots of giant kelp forests.
  • Seagrass connectivity on the West Coast of Africa supports the Hypothesis of Grazer-Mediated Seed Dispersal
    Publication . Tavares, Ana I; Assis, Jorge; Patrício, A. R.; Ferreira, Rogério; Cheikh, Mohamed Ahmed Sidi; Bandeira, Salomão; Regalla, Aissa; Santos, Iderlindo; Potouroglou, Maria; Nicolau, Suzana; Teodosio, Maria; Almada, Carmen; Santos, Rui; Pearson, Gareth; Serrao, Ester
    Population connectivity influences the distribution of genetic diversity and divergence along a species range, as the likelihood of extinction or differentiation increases in isolated populations. However, there is still poor understanding of the processes mediating inter-population dispersal in marine species that are sessile and lack planktonic life stages. One such case is the seagrass species Halodule wrightii, which produces basal seeds, although detached plants can drift. Along the tropical western coast of Africa, this species occurs in distant discontinuous habitats, raising the question of how interpopulation dispersal is mediated. The species is a key source of ecosystem functions including feeding large migratory grazers. This study aims to infer whether genetic differentiation of the seagrass H. wrightii along the western coast of Africa supports a hypothesis of predominant transportation of rafting seagrass by ocean currents, versus the hypothesis of biotic vectors of dispersal. Additional hypotheses were addressed concerning range-wide clonality and genetic diversity, assessed with microsatellite markers on populations of the west coast of Africa from Mauritania to Angola. Population genetic diversity and structure were compared with predictions from biophysical models of dispersal by oceanographic currents. The genetic data revealed low divergence among most populations, in strong contrast with predictions of very low probability of connectivity mediated by currents along the western African coastline. Moderate to high genotypic diversity showed important seed recruitment, but genetic and genotypic diversities were lower at range edges. Populations north and south of the equator were differentiated, and remarkably, so were neighboring equatorial populations despite their proximity. These results reveal independent sources of colonization of meadows in these islands, which are major habitat for migratory grazing green turtles, also supporting the hypothesis of biotically mediated seed transport. The importance of seagrass for conservation of endangered macrofauna has been widely reported; here we report evidence supporting the reciprocal role, that macrofauna protection can also plays a role in long-term survival and reproductive success of seagrass.