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AimGlobal climate change has profound and diverse effects on biological diversity. Identifying present-day climate refugia is an increasingly recognized strategy for the management of biodiversity loss. Such refugia are potential safe havens that enhance environmental diversity by buffering the effects of large scale change, facilitating species persistence at regional scales and conserving unique genetic diversity. Although their ecological effects are well studied, the potential of upwelling centres to act as refugia in a scenario of climate warming remains largely unexplored. Here, we investigate whether upwelled waters act as refugia in a region heavily affected by recent climatic changes.LocationShores of south-western Iberia and north-western Africa.MethodsWe compared changes in distribution of the canopy-forming macroalga Fucus guiryi with sea surface temperature patterns in five upwelling areas and adjacent warmer regions. Population diversity and structure was inferred from genotypic analyses using nine microsatellite loci.ResultsFucus guiryi has disappeared from large expanses of non-upwelling shores, currently persisting in areas characterized by strong upwelling and reduced or non-significant rates of warming. Populations of F. guiryi were more abundant towards upwelling centres. Furthermore, the genetic characterization of populations revealed distinct genetic groups associated with each upwelling system.Main conclusionsWithin a large region of predominantly changing climate, we highlight the fundamental importance of upwelling areas as favourable, comparatively stable climates where F. guiryi has retreated and persists, preserving unique portions of the species' genetic pool.

The plasticity of different kelp populations to heat stress has seldom been investigated excluding environmental effects due to thermal histories, by raising a generation under common garden conditions. Comparisons of populations in the absence of environmental effects allow unbiased quantification of the meta-population adaptive potential and resolution of population-specific differentiation. Following this approach, we tested the hypothesis that genetically distinct arctic and temperate kelp exhibit different thermal phenotypes, by comparing the capacity of their microscopic life stages to recover from elevated temperatures. Gametophytes of Laminaria digitata (Arctic and North Sea) grown at 15°C for 3 years were subjected to common garden conditions with static or dynamic (i.e., gradual) thermal treatments ranging between 15 and 25°C and also to darkness. Gametophyte growth and survival during thermal stress conditions, and subsequent sporophyte recruitment at two recovery temperatures (5 and 15°C), were investigated. Population-specific responses were apparent; North Sea gametophytes exhibited higher growth rates and greater sporophyte recruitment than those from the Arctic when recovering from high temperatures, revealing differential thermal adaptation. All gametophytes performed poorly after recovery from a static 8-day exposure at 22.5°C compared to the response under a dynamic thermal treatment with a peak temperature of 25°C, demonstrating the importance of gradual warming and/or acclimation time in modifying thermal limits. Recovery temperature markedly affected the capacity of gametophytes to reproduce following high temperatures, regardless of the population. Recovery at 5°C resulted in higher sporophyte production following a 15°C and 20°C static exposure, whereas recovery at 15°C was better for gametophyte exposures to static 22.5°C or dynamic heat stress to 25°C. The subtle performance differences between populations originating from sites with contrasting local in situ temperatures support our hypothesis that their thermal plasticity has diverged over evolutionary time scales.

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.

The impact of climate change on biodiversity has stimulated the need to understand environmental stress responses, particularly for ecosystem engineers whose responses to climate affect large numbers of associated organisms. Distinct species differ substantially in their resilience to thermal stress but there are also within-species variations in thermal tolerance for which the molecular mechanisms underpinning such variation remain largely unclear. Intertidal mussels are well-known for their role as ecosystem engineers. First, we exposed two genetic lineages of the intertidal mussel Perna perna to heat stress treatments in air and water. Next, we ran a high throughput RNA sequencing experiment to identify differences in gene expression between the thermally resilient eastern lineage and the thermally sensitive western lineage. We highlight different thermal tolerances that concord with their distributional ranges. Critically, we also identified lineage-specific patterns of gene expression under heat stress and revealed intraspecific differences in the underlying transcriptional pathways in response to warmer temperatures that are potentially linked to the within-species differences in thermal tolerance. Beyond the species, we show how unravelling within-species variability in mechanistic responses to heat stress promotes a better understanding of global evolutionary trajectories of the species as a whole in response to changing climate.

FCT (Portuguese Science Foundation) [BIODIVERSA/0004/2015, PTDC/MAR-EST/6053/2014, UID/Multi/04326/2013, SFRH/BPD/63/03/2009, SFRH/BPD/107878/2015, SFRH/BD/74436/2010]; European Commission (ATP) [226248]

Pew Foundation (USA); Portuguese FCT (Fundacao para a Ciencia e a Tecnologia) through program GENEKELP [PTDC/MAR-EST/6053/2014]; Portuguese FCT (Fundacao para a Ciencia e a Tecnologia) through program MARFOR [Biodiversa/0004/2015]; Portuguese FCT (Fundacao para a Ciencia e a Tecnologia) [UID/Multi/04326/2013, SFRH/BPD/88935/2012, SFRH/BPD/111003/2015]; NSERC; FRQNT; Canada Foundation for Innovation; New Brunswick Innovation Foundation; European Union's Seventh Framework Programme [226248]; Danish Environmental Protection Agency within the Danish Cooperation for Environment in the Arctic (DANCEA)

To understand the thermal plasticity of a coastal foundation species across its latitudinal distribution, we assess physiological responses to high temperature stress in the kelp Laminaria digitata in combination with population genetic characteristics and relate heat resilience to genetic features and phylogeography. We hypothesize that populations from Arctic and cold‐temperate locations are less heat resilient than populations from warm distributional edges. Using meristems of natural L. digitata populations from six locations ranging between Kongsfjorden, Spitsbergen (79°N), and Quiberon, France (47°N), we performed a common‐garden heat stress experiment applying 15°C to 23°C over eight days. We assessed growth, photosynthetic quantum yield, carbon and nitrogen storage, and xanthophyll pigment contents as response traits. Population connectivity and genetic diversity were analyzed with microsatellite markers. Results from the heat stress experiment suggest that the upper temperature limit of L. digitata is nearly identical across its distribution range, but subtle differences in growth and stress responses were revealed for three populations from the species’ ecological range margins. Two populations at the species’ warm distribution limit showed higher temperature tolerance compared to other populations in growth at 19°C and recovery from 21°C (Quiberon, France), and photosynthetic quantum yield and xanthophyll pigment responses at 23°C (Helgoland, Germany). In L. digitata from the northernmost population (Spitsbergen, Norway), quantum yield indicated the highest heat sensitivity. Microsatellite genotyping revealed all sampled populations to be genetically distinct, with a strong hierarchical structure between southern and northern clades. Genetic diversity was lowest in the isolated population of the North Sea island of Helgoland and highest in Roscoff in the English Channel. All together, these results support the hypothesis of moderate local differentiation across L. digitata's European distribution, whereas effects are likely too weak to ameliorate the species’ capacity to withstand ocean warming and marine heatwaves at the southern range edge. We aimed to understand the intraspecific thermal variation of a coastal foundation species, the kelp Laminaria digitata. Marginal populations in particular differed in their response to heat stress treatments, while multilocus genotypes showed a clear and broad separation of L. digitata populations into a “northern” and a “southern” clade. These results imply that L. digitata populations have phenotypically diverged under the influence of the Quaternary glacial cycles.

In haplodiplontic lineages, sexual reproduction occurs in haploid parents without meiosis. Although widespread in multicellular lineages such as brown algae (Phaeophyceae), haplodiplontic gametogenesis has been little studied at the molecular level. We addressed this by generating an annotated reference transcriptome for the gametophytic phase of the sugar kelp, Saccharina latissima. Transcriptional profiles of microscopic male and female gametophytes were analysed at four time points during the transition from vegetative growth to gametogenesis. Gametogenic signals resulting from a switch in culture irradiance from red to white light activated a core set of genes in a sex-independent manner, involving rapid activation of ribosome biogenesis, transcription and translation related pathways, with several acting at the post-transcriptional or post-translational level. Additional genes regulating nutrient acquisition and key carbohydrate-energy pathways were also identified. Candidate sex-biased genes under gametogenic conditions had potentially key roles in controlling female- and male-specific gametogenesis. Among these were several sex-biased or -specific E3 ubiquitin-protein ligases that may have important regulatory roles. Females specifically expressed several genes that coordinate gene expression and/or protein degradation, and the synthesis of inositol-containing compounds. Other female-biased genes supported parallels with oogenesis in divergent multicellular lineages, in particular reactive oxygen signalling via an NADPH-oxidase. Males specifically expressed the hypothesised brown algal sex-determining factor. Male-biased expression mainly involved upregulation of genes that control mitotic cell proliferation and spermatogenesis in other systems, as well as multiple flagella-related genes. Our data and results enhance genome-level understanding of gametogenesis in this ecologically and economically important multicellular lineage.

Marine macrophytes are the foundation of algal forests and seagrass meadows–some of the most productive and diverse coastal marine ecosystems on the planet. These ecosystems provide nursery grounds and food for fish and invertebrates, coastline protection from erosion, carbon sequestration, and nutrient fixation. For marine macrophytes, temperature is generally the most important range limiting factor, and ocean warming is considered the most severe threat among global climate change factors. Ocean warming induced losses of dominant macrophytes along their equatorial range edges, as well as range extensions into polar regions, are predicted and already documented. While adaptive evolution based on genetic change is considered too slow to keep pace with the increasing rate of anthropogenic environmental changes, rapid adaptation may come about through a set of non-genetic mechanisms involving the functional composition of the associated microbiome, as well as epigenetic modification of the genome and its regulatory effect on gene expression and the activity of transposable elements. While research in terrestrial plants demonstrates that the integration of non-genetic mechanisms provide a more holistic picture of a species’ evolutionary potential, research in marine systems is lagging behind. Here, we aim to review the potential of marine macrophytes to acclimatize and adapt to major climate change effects via intraspecific variation at the genetic, epigenetic, and microbiome levels. All three levels create phenotypic variation that may either enhance fitness within individuals (plasticity) or be subject to selection and ultimately, adaptation. We review three of the most important phenotypic variations in a climate change context, including physiological variation, variation in propagation success, and in herbivore resistance. Integrating different levels of plasticity, and adaptability into ecological models will allow to obtain a more holistic understanding of trait variation and a realistic assessment of the future performance and distribution of marine macrophytes. Such multi-disciplinary approach that integrates various levels of intraspecific variation, and their effect on phenotypic and physiological variation, is of crucial importance for the effective management and conservation of seagrasses and macroalgae under climate change.

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.